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Thesis Diagnosing Cerebral Visual Dysfunctions in Children-Looking Beyond Visual Acuity and Visual Field
Thesis Diagnosing Cerebral Visual Dysfunctions in Children-Looking Beyond Visual Acuity and Visual Field
Visual Dysfunctions in
Children:
visual field
visual acuity and
looking beyond
https://epubs.ogc.nl/?epub=y.vanderzee
ISBN: 978-94-6361-255-5
Proefschrift
door
Summary 213
Samenvatting 223
Dankwoord 235
About the author 241
PhD Portfolio 245
Chapter
Chapter 1
1
General introduction
General introduction 9
Introduction
1
To understand and interact with the world around us, we humans are highly
dependent on the quality of our senses (vision, hearing, touch, smell, and
taste), cognition and motor abilities. An extensive network is involved in the
processing of sensory information, and includes the sensors, such as eyes,
ears and skin, and our brain. People are inclined to use their own sensorial
input and interpretation of the world around them as reference. This makes it
difficult or even impossible for people with effectively working senses to imag-
ine, understand and acknowledge what it is like to be sensorially impaired,
as in people with a visual impairment. To understand and recognise sensorial
impairments, we need knowledge of sensorial systems and functions, and the
effect that function loss or impairment has on interaction with our environ-
ment. Vision in particular, is regarded as the primary sense for developing
many skills. Therefore, in this thesis, I focus on visual impairments in children.
1 Although this term suggests that there is a total lack of vision, there may be some
vision left.
10 Chapter 1
Table 1. Definition of low vision and blindness as described in ICD-10 H54, 1993.
Definition
In the better eye with best possible
correction Low vision Blindness
Visual acuity less than 6/18 and equal to or better less than 3/60
than 3/60
or or
Visual field less than 30 degrees and less than 10
equal to or better than 10 degrees degrees
Although visual acuity and visual field are important properties, there is
more to this than meets the eye when it comes to visual perception, the
ability to recognise and interpret visual aspects of the surrounding environ-
ment. Visual perception highly depends on the development of an extensive
brain network and several visual functions, which are assigned to different
brain areas. It starts with processing light that falls on the retina. The retinal
information is conveyed via the optic nerve and lateral geniculate nucleus
(LGN) to the primary visual cortical areas, such as the occipital lobe (V1), and
extrastriate areas (V2). Next, the visual brain can be described in a simpli-
fied hierarchical model with two anatomically and functionally distinguishable
[8, 9]
main streams: the ventral stream and the dorsal stream. The ventral
[10, 11]
stream ends in the inferior temporal cortex and is involved in object
[11]
and face recognition. The dorsal stream leads into the posterior parietal
cortex and extends towards the anterior parietal and posterior frontal cortex,
[12, 13] [10]
and is involved in motion perception, visuomotor integration, visual
[14, 15] [16, 17]
attention, and object recognition in suboptimal representations.
Habilitation specialists generally acknowledge that a lack or loss of cerebral
visual functions can impede a child’s development and participation as well.
Thus cerebral visual disfunctions, for example, may hinder the ability to visu-
[18-20]
ally recognise persons or objects or to perceive motion. Difficulties in the
perception of a person’s identity hinder discrimination of familiar and unfamiliar
persons, and proper social communication. Object recognition problems not
only complicate learning by means of objects, but make exercises in school-
books, which often contain illustrations, difficult or even impossible to do.
Visual spatial attention and motion perception are essential for understanding
and predicting the constantly changing world around us. For blind people or
people with impaired visual motion perception, crossing a street without aids
such as traffic lights with a signal system is very risky, especially now that
car engines become more silent. The combination of spatial awareness and
motion perception also helps us to direct our object handling, such as catching
General introduction 11
[27]
recognition of typical behaviours and problems associated with it. Profes-
sionals involved in the expert diagnostic process indicated multiple problems,
1
such as the lack of neuropsychological tests for children under the age of
four years. As a result, they are forced to rely on structural observations with
no or limited quantitative outcome measures. In addition, they stressed the
lack of quantitative tests for specific cerebral visual functions applicable to
children older than four years, with a special emphasis on motion perception
tests. Still, most tests have been developed for normally sighted children,
excluding children with low vision. Therefore, the effect of low vision on test
outcomes is unknown. The presence of a cognitive impairment can also affect
the performance of perception tests. That raises a very practical question:
what entry should be used when using norm tables: the developmental or the
chronological age of a child?
Study approach
Neuropsychology aims to understand how behaviour and cognition are in-
fluenced by brain functioning. During several tests, the processing of visual
information plays an important role, because many tasks consist of visual
representations. Here, the ability to visualize a complete whole even when
presented incomplete information or a partial picture, also known as Gestalt,
is crucial for optimum performance. The general aim of my thesis was to
provide new information to advance evidence-based diagnostic procedures in
children at risk for cerebral visual dysfunction (children with brain damage),
which ultimately should be efficient (burden and costs, use of valid tests).
I decided to focus on school-aged children with a developmental age be-
tween 4 and 7 years. The selected tests are relatively easily to integrate in
the assessment and provide a quantitative outcome of cerebral visual func-
tions associated with dorsal stream vulnerability of the visual system. Here, I
consider object recognition under suboptimal conditions, motion perception,
visuomotor abilities and visual attention as dorsal stream functions.
Data collection
We assessed oculomotor functions, visual acuity, visual fields and contrast
sensitivity, performance age, object recognition under suboptimal conditions,
motion perception, visuomotor abilities and visual attention in children at
risk for cerebral visual dysfunction (children with brain damage) as well as
in children not at risk (normally developing children and children with ocular
disorders).
14 Chapter 1
Remarks on terminology
Terms like cortical visual impairment or cerebral visual impairment (CVI) can
cause confusion about the visual functions of interest. The term visual impair-
ment is often used to indicate low vision and blindness. In the above text and
in the following chapters the term visual impairment is used for both low vision
and blindness and cerebral visual dysfunctions.
16 Chapter 1
References
1. Brambring, M., Divergent development of verbal skills in children who are blind or
sighted. Journal of Visual Impairment & Blindness, 2007. 101(12): p. pp.
2. Houwen, S., et al., Gross motor skills and sports participation of children with
visual impairments. Res Q Exerc Sport, 2007. 78(2): p. 16-23.
3. Houwen, S., et al., Motor skill performance of school-age children with visual
impairments. Dev Med Child Neurol, 2008. 50(2): p. 139-45.
4. Dyck, M.J., et al., Emotion recognition/understanding ability in hearing or vision-
impaired children: do sounds, sights, or words make the difference? Journal of
Child Psychology and Psychiatry, 2004. 45(4): p. 789-800.
5. Tadić, V., L. Pring, and N. Dale, Are language and social communication intact in
children with congenital visual impairment at school age? Journal of Child Psy-
chology and Psychiatry, 2010. 51(6): p. 696-705.
6. O’Donnell, L.M. and R.L. Livingston, Active exploration of the environment by
young children with low vision: A review of the literature. Journal of Visual Im-
pairment & Blindness, 1991. 85(7): p. 287-291.
7. World Health Organization, International Statistical Classification of diseases,
injuries and causes of death, tenth revision., in H54 Blindness and low vision.
1993, WHO: Geneva.
8. Merigan, W.H. and J.H. Maunsell, How parallel are the primate visual pathways?
Annu Rev Neurosci, 1993. 16: p. 369-402.
9. Goodale, M.A. and A.D. Milner, Separate visual pathways for perception and ac-
tion. Trends in Neurosciences, 1992. 15(1): p. 20-5.
10. James, T.W., et al., Ventral occipital lesions impair object recognition but not
object-directed grasping: an fMRI study. Brain, 2003. 126(Pt 11): p. 2463-75.
11. Atkinson, J., et al., Neurobiological models of visuospatial cognition in children
with Williams syndrome: measures of dorsal-stream and frontal function. Devel-
opmental Neuropsychology, 2003. 23(1-2): p. 139-72.
12. Braddick, O.J., et al., Brain areas sensitive to coherent visual motion. Perception,
2001. 30(1): p. 61-72.
13. Stiers, P., et al., Mapping multiple visual areas in the human brain with a short
fMRI sequence. Neuroimage, 2006. 29(1): p. 74-89.
14. Pollmann, S., et al., Separating distractor rejection and target detection in poste-
rior parietal cortex--an event-related fMRI study of visual marking. Neuroimage,
2003. 18(2): p. 310-23.
15. Marini, F. and C.A. Marzi, Gestalt Perceptual Organization of Visual Stimuli Cap-
tures Attention Automatically: Electrophysiological Evidence. Front Hum Neurosci,
2016. 10: p. 446.
16. Vuilleumier, P., et al., Multiple levels of visual object constancy revealed by event-
related fMRI of repetition priming. Nat Neurosci, 2002. 5(5): p. 491-9.
17. Eger, E., et al., Mechanisms of top-down facilitation in perception of visual objects
studied by FMRI. Cereb Cortex, 2007. 17(9): p. 2123-33.
18. Ahmed, M. and G.N. Dutton, Cognitive visual dysfunction in a child with cerebral
damage. Dev Med Child Neurol, 1996. 38(8): p. 736-9.
General introduction 17
19. Dutton, G.N., R.E. Day, and D.L. McCulloch, ‘Who is a visually impaired child? A
model is needed to address this question for children with cerebral visual impair- 1
ment’. Dev Med Child Neurol, 1999. 41(3): p. 212-3.
20. Jacobson, L., et al., Visual and perceptual characteristics, ocular motility and stra-
bismus in children with periventricular leukomalacia. Strabismus, 2002. 10(2): p.
179-83.
21. Besseling, J., et al., Toename gebruik ondersteuning voor jongeren met een
gezondheidsbeperking. 2007, TNO KvL: Hoofddorp.
22. Oogheelkundige richtlijn. Verwijzing van slechtzienden en blinden. 2004, Neder-
lands Oogheelkundig Gezelschap.
23. van Rens, G., H. Vreeken, and R. van Nispen, Richtlijn Visusstoornissen, revalidatie
en verwijzing (Ophthalmological guideline Visual impairments, Rehabilitation and
Referral). 2011, Nederlands Oogheelkundig Gezelschap (Dutch Ophthalmological
Society).
24. Dutton, G.N., E.C. McKillop, and S. Saidkasimova, Visual problems as a result of
brain damage in children. Br J Ophthalmol, 2006. 90(8): p. 932-3.
25. Gronqvist, S., et al., Association between visual impairment and functional and
morphological cerebral abnormalities in full-term children. Acta Ophthalmol
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Chapter
Chapter 2
2
van der Zee, Y.J., P. Stiers, and H.M. Evenhuis, Should we add
visual acuity ratios to referral criteria for potential cerebral visual
impairment? J Optom, 2017. 10(2): p. 95-103.
20 Chapter 2
Abstract
Purpose
To determine whether the assessment of visual acuity ratios might improve
the referral of children with (sub)normal visual acuity but at risk of cerebral
visual impairment.
Methods
In an exploratory study, we assessed visual acuity, crowding ratio and the
ratios between grating acuity (Teller Acuity Cards-II) and optotype acuity
(Cambridge Crowding Cards) in 60 typically developing school children (mean
age 5y8m ± 1y1m), 21 children with ocular abnormalities only (5y7m ± 1y9m)
and 26 children with (suspected) brain damage (5y7m ± 1y11m). Sensitivities
and specificities were calculated for targets and controls from the perspective
of different groups of diagnosticians: youth health care professionals (target:
children with any visual abnormalities), ophthalmologists and low vision ex-
perts (target: children at risk of cerebral visual impairment).
Results
For youth health care professionals subnormal visual acuity had the best
sensitivity (76%) and specificity (70%). For ophthalmologists and low vision
experts the crowding ratio had the best sensitivity (67%) and specificity (79
and 86%).
Conclusion
Youth health care professionals best continue applying subnormal visual acuity
for screening, whereas ophthalmologists and low vision experts best add the
crowding ratio to their routine diagnostics, to distinguish children at risk of
visual impairment in the context of brain damage from children with ocular
pathology only.
Key words: visual acuity; visual acuity ratios; brain damage; referral criteria
Visual acuity ratios as referral criteria? 21
Introduction
[15]
brain damage than in normally developing children and children with ocular
[11, 15]
disorders.
Therefore, the first aim of this exploratory study was to assess whether
the crowding ratio, estimated by the Cambridge Crowding Cards (optotypes),
and the ratio between grating acuity and optotype acuity, differentiate better
than visual acuity alone between children without any neurological and ocular
abnormalities, children with ocular disorders only, and children with (indica-
tions of) brain damage.
In clinical practice, different levels in the care supply chain, i.e. youth health
care physicians or nurses, ophthalmologists, and experts in low vision services,
see different populations and have different detection goals and indications for
referral.
Therefore, our second aim was to study which parameter (visual acuity
alone, different ratios) for each level has the best sensitivity and specificity to
meet their detection goal.
Methods
To this end, the following child characteristics were collected from the clinical
files: visual acuity, refractive errors, use of glasses or lenses, strabismus, con-
trast sensitivity, other ocular abnormalities, and if present, aetiology of brain
damage. Visual fields were checked using the confrontation test. Although 2
refractive errors and strabismus are associated with crowding problems, these
children were not excluded from the analyses, because this reflects clinical
practice.
The study adhered to the Declaration of Helsinki and the protocol has been
approved by the Medical Ethical Testing Committee of the Erasmus University
Medical Center Rotterdam (MEC nr: 2006-056).
In the period June 2006-September 2010, visual acuity was assessed in all
[16]
participants with the Cambridge Crowding Cards to assess uncrowded and
[17]
crowded optotype acuity, and the Teller Acuity Cards-II to assess grating
acuity. The uncrowded Cambridge Crowding Cards show a single letter and the
crowded cards show a target letter surrounded by four letters, with a distance
between letters of half a letter width. To minimise the effect of differences in
test distance, the Teller Acuity Cards as well as the Cambridge Crowding Cards
were presented at a distance of 3 meters. Outcomes of the Teller Acuity Cards
were corrected for the greater than recommended presentation distance, using
the following formula: cycl/deg = (test distance/57)*cycl/cm. Children were
assessed binocularly, if applicable wearing their own glasses. Grating acuity
was assessed first, followed by single and crowded optotype acuities. During
Teller Acuity Card assessment, children were asked to actively point out the
location of the stripes (left or right), and during optotype assessment, they
had to name or match the target letter. All tests were started with coarse grat-
ings/large letter sizes. Finer gratings/smaller letter sizes were presented until
the child was unable to identify the correct position/letter. Maximally three
cards were presented per visual acuity level and the visual acuity threshold
was defined as the highest visual acuity level with two out of three correctly
identified grating positions/letters. All assessments were performed by trained
orthoptists.
To enable comparisons between grating and optotype acuities, we expressed
all acuities in cycl/deg. We determined two cut-off values for crowded visual
acuity, because in youth health care, children with ‘subnormal vision’ should be
referred for ophthalmological examination, whereas ‘low vision’ is a traditional
eligibility requirement for low vision services. Subnormal visual acuity was
defined as a crowded acuity lower than 20 cycl/deg (Snellen equivalent 6/9)
for 3½-4½ year olds and lower than 30 cycl/deg (Snellen equivalent 6/6) for
older children (norms from The Cambridge Crowding Cards leaflet), whereas
24 Chapter 2
low vision was defined as a crowded acuity equal to or lower than 10 cycl/deg
[18]
(Snellen equivalent 6/18).
Crowding was quantified as a crowding ratio (CR), which is defined as the
acuity presenting a single optotype, divided by the acuity presenting several
optotypes (linear optotype acuity). Because linear acuity tests mostly result in
lower visual acuities than single optotype testing, the crowding ratio is usually
[16]
higher than 1. In typically developing children, there is a developmental
effect, with a mean crowding ratio (CR 1.8) in 3-4 year olds, decreasing with
[19]
age. Therefore, a crowding ratio ≥ 2 (i.e. halving of the visual acuity out-
come) was considered as the standard for abnormal crowding, irrespective of
age or developmental level.
The following ratios were calculated for each participant: crowding ratio
(uncrowded/crowded optotype acuity), grating acuity/uncrowded acuity, grat-
ing acuity/crowded acuity. Mean (SD) and median ratios were calculated for
the three participant groups. Between-test differences were analysed with
Friedman and Wilcoxon Signed Rank tests and between-group differences with
Kruskall-Wallis tests.
To answer the second study question, per specialist discipline, the propor-
tion of correctly identified children-at-risk within the target group (sensitivity)
and the proportion of correctly identified non-targets within the control group
(specificity) were calculated. We plotted ROC-curves for crowded visual acu-
ity and each ratio, to check which outcome and cut-off value could be used
best by each discipline. If visual acuity, measured during the study, appeared
different from the received information, the child was not excluded from the
analysis or transferred to a different group, because we wanted to act on clini-
cally defined risks. To be certain that the presence of abnormal crowding could
not be explained by the presence of strabismus – risk factor for amblyopia -,
we calculated the correlation (Spearman’s ρ) between a crowding ratio ≥ 2
and manifest or latent strabismus in the total study population.
Results
Participants
Sixty of the 107 children (25 boys, 35 girls) were included in group 1, 21 (11
boys, 10 girls) in group 2, and 26 (13 boys, 13 girls) in group 3. Ages of groups
2 and 3 did not differ significantly, whereas group 1 included significantly more
young children (H(2) = 9.17, p = .01). Ocular abnormalities in groups 2 and
3 are presented in Table 1.
Visual acuity ratios as referral criteria? 25
Table 1. Ocular abnormalities present in subgroups of children with ocular abnormalities only and
with brain damage
Group 2 Group 3
Ocular abnormalities n = 21 n = 17
Microphthalmus unilateral - 1
Lens 6 1
Congenital cataract 6 1
Stickler Syndrome 2
Uvea and Fundus 8 2
Idiopathic chronic uveitis 1
Choreoretinitis 1
Aniridia 1
Iris and peripheral choridea coloboma 1
x-linked retinoschizis 1
Retinoblastoma 1
Cone dysfunction 1
Cone-rod dysfunction 1
Cone-rod dystrophy 1
Red-green deficiency 1
Macula 2 1
abnormality 1 1
Bull’s eye 1
Oculocutaneous albinism 1
26 Chapter 2
Table 1. Ocular abnormalities present in subgroups of children with ocular abnormalities only and
with brain damage (continued)
Group 2 Group 3
Ocular abnormalities n = 21 n = 17
Neuro-ophthalmological 9 8
Nystagmus 8 5
Congenital nystagmus 4
Manifest 3 4
Latent 1 1
Torticollis 5 4
Optic nerve hypoplasia 1
Septo-optic dysplasia 1*
Opticopathy 1
Retrograde optic nerve atrophy 2
Strabismus 11 14
Esotropia (only trace) 6 (0) 5
Exotropia (only trace) 3 (1) 5
Intermittent mixed (only trace) 1
Hypertropia (only trace) 1 (1) 1
Esophoria (only trace) 1 (1)
Exophoria (only trace)
Upshoot in adduction 2
Convergence limited 1
Refractive errors 8 6
Myopia
high 1
moderate 2
Hyperopia
high 4 1
moderate 1 2
mild 2
Anisohyperopia 1
* this child was missing the right eye and had a prechiasmatic abnormality of the optic nerve
Visual acuities
All visual acuity tasks were completed by 59/60 children in group 1, 15/21 in
group 2 and 19/26 in group 3. Grating acuity was missing in 9 participants
because of logistical reasons; optotype acuities were missing in five children
with brain damage, because of low vision, short attention or problems with
the test distance.
Results of the acuity tests are reported in Table 2. As was to be expected,
within all groups, visual acuity varied with the test used: Teller Acuity Cards
resulted in a significantly higher median visual acuity than the uncrowded
Cambridge cards (p < .01) and median uncrowded acuity was significantly
Visual acuity ratios as referral criteria? 27
higher than median crowded acuity (p < .01). Remarkably, low vision (< 10
cycl/deg) was found in two children of group 1. One of them was known in the
Eye Hospital and wore glasses to correct mild hyperopia; we referred the other
for ophthalmological assessment. 2
Table 2. Visual acuity results of the Teller Acuity Cards (grating acuity) and the Cambridge Crowd-
ing Cards (uncrowded and crowded acuity) in typically developing children (group 1), children with
ocular disorders (group 2), children with brain damage (group 3).
Group
1 2 3
Test (n = 60) (n = 21) (n = 26)
Teller Acuity Cards
Grating acuity n 59 15 24
Median Snellen equivalent * 20/11.6 20/17.5 20/11.6
< 20/20 † (n) 2 7 5
≤ 20/30 ‡ (n) 0 0 1
Cambridge Crowding Cards
Uncrowded acuity n 60 21 24
Median Snellen equivalent 6/4 6/12 6/6
<6/6 † (n) 2 8 2
≤ 6/18 ‡ (n) 0 9 4
Crowded acuity n 60 21 21
Median Snellen equivalent 6/6 6/60 6/9
< 6/9 or 6/6 § (n) 16 4 7
≤ 6/18 ‡ (n) 2 15 6
* cycl/deg = (20/Snellen denominator) x 30. † Subnormal vision, low vision excluded. Snellen
equivalent for 30 cycl/deg is 6/6 or 20/20. ‡ Low vision ≤ 10 cycl/deg. Snellen equivalent for 10
cycl/deg is 6/18 or 20/30. § Age dependent cut-off value for subnormal vision: 20 cycl/deg (Snellen
equivalent 6/9) for age < 4y6m; < 30 cycl/deg (Snellen equivalent < 6/6) for older children. Low
vison excluded.
Acuity ratios
In Table 3, we present the observed crowding and grating/optotype ratios
within each group. Significant group differences were found for all ratios
(Kruskal-Wallis tests: p < .01).
Table 3. Observed ratios in typically developing children (group 1), children with ocular disorders
(group 2) and children with brain damage (group 3)
Group
1 2 3
Ratio (n = 60) (n = 21) (n = 26)
Uncrowded acuity/Crowded acuity
n 59 21 21
Median 1.50 1.50 2.00
Mean 1.60 1.42 1.94
SD 0.42 0.49 0.66
Ratio ≥ 2 (n) 14 3 14
Grating acuity/Uncrowded acuity
n 59 15 22
Median 1.14 2.51 1.60
Mean 1.30 2.55 2.00
SD 0.33 1.98 1.91
Ratio ≥ 2 (n) 3 10 6
Grating acuity/Crowded acuity
n 59 15 19
Median 1.71 3.35 2.57
Mean 2.04 3.75 3.96
SD 0.60 2.02 4.22
Ratio ≥ 2 (n) 23 12 13
Post-hoc analysis on the ranks indicated that the ranks of the ratios in group
1 were significantly higher than in group 2, (tw(31.7) = 2.25, p = .03), al-
though median score for the uncrowded/crowded acuity ratio of group 1 and
2 was equal. This difference cannot be explained by the different step sizes in
the Cambrigde Crowding Cards and its ratios, but is the result of the higher
proportion of participants with a crowding ratio ≥ 2 in group 1.
The difference between group 1 and 3 was nearly significant (tw(28.9) = -
2.09, p = .05) and the ratio in group 3 was significantly higher than that in
group 2 (tw(40) = 3.20, p < .01). A crowding ratio of 1.5 (crowded acuity is
a half octave or one step lower than uncrowded acuity) or lower was found in
76% of group 1, 86% of group 2, and 33% of group 3.
Visual acuity ratios as referral criteria? 29
Table 4. Mean ratio between uncrowded acuity and crowded acuity per age group in typically de-
veloping children (group 1), children with ocular disorders (group 2) and children with brain damage
(group 3)
Group
1 2 3
(n = 59) (n = 21) (n = 21)
3-4 years old
n 16 4 2
Mean 1.67 1.63 2.13
SD 0.51 0.25 0.18
5-7 years old
n 43 12 13
Mean 1.57 1.48 1.92
SD 0.39 0.56 0.44
Older than 7 years
n 5 6
Mean 1.10 1.93
SD 0.22 0.66
Table 5. Sensitivity and specificity for cut-off values evaluated for different specialist groups
Crowded acuity Ratios
Subnormal Low vision unC/C TAC/unC TAC/C
Specialist < 6/6 or 6/9 * 6/18 † ≥2 ≥2 ≥2
Youth health care physician
Sensitivity .76 .50 .40 .43 .74
(95%-CI) (.61-.87) (.36-.64) (.27-.56) (.29-.59) (.57-.85)
Specificity .70 .97 .77 .95 .61
(95%-CI) (.58-.80) (.89-.99) (.65-.86) (.86-.98) (.36-.64)
Ophthalmologist
Sensitivity .62 .29 .67 .27 .68
(95%-CI) (.41-.79) (.14-.50) (.45-.83) (.13-.48) (.46-.85)
Specificity .54 .79 .79 .82 .53
(95%-CI) (.43-.64) (.69-.87) (.69-.86) (.72-.89) (.42-.64)
Orthoptist special services
Sensitivity .62 .29 .67 .27 .68
(95%-CI) (.41-.79) (.14-.50) (.45-.83) (.13-.48) (.46-.85)
Specificity .10 .29 .86 .33 .20
(95%-CI) (.03-.29) (.14-.50) (.65-.95) (.15-.58) (.07-.45)
C = crowded acuity, unC = uncrowded acuity, TAC = grating acuity; * subnormal vision is age
dependent, 6/6 = 30 cycl/deg for children age 4y6m and older and 6/9 = 20 cycl/deg for younger
children; † 6/18 = 10 cycl/deg.
Visual acuity ratios as referral criteria? 31
Figure 1. ROC-curves for crowded visual acuity and acuity ratios from the perspective of different
groups of diagnosticians. A. Youth health care physicians (target group: children at risk of visual
problems due to ocular abnormalities or brain damage; control group: children without visual prob-
lems). B. Ophthalmologists (target group: children with cerebral visual problems; control group:
children without visual problems and children with ocular visual problems). C. Low vision centres
(target: group: children with cerebral visual problems; control group: children with ocular visual
problems)
C = crowded acuity; unC = uncrowded acuity; TAC = grating acuity
Each marker is a different cut-off point. Filled makers indicate cut-off points used in the current
study: low vision (grey diamond), subnormal acuity (black diamond) and ratios equal to 2.0 (other
black markers). Crowded acuity markers to the right of these filled markers are higher cut-off values
and markers to the left are lower cut-off values. Ratio markers to the right of the filled markers are
lower cut-off values, markers to the left are higher cut-off values.
32 Chapter 2
Within low vision services, too, the crowding ratio with a cut-off value of 2 is
currently the best option for screening for a risk of cerebral visual impairment
(AUC = 0.76, 95%-CI = 0.60-0.91, p < .01). Table 5 shows that subnormal
vision and a ratio of 2 or higher between grating acuity and crowded acuity
were relatively frequent in both patient groups 2 and 3 (high sensitivity, low
specificity). Low vision and a ratio of 2 or higher between grating acuity and
uncrowded acuity were relatively frequent in group 2, but relatively uncom-
mon in group 3 (low sensitivity and low specificity).
We conclude that the results so far indicate that in groups referred for
ophthalmological assessment or specialist evaluation in a low vision service,
the crowding ratio is sensitive to detect children at risk of cerebral visual
impairment, with and without low vision.
Discussion
Even though crowding has been extensively studied during more than 80
[22]
years and is considered clinically relevant, little is known about develop-
mental changes and normal limits in children. We were surprised to find that
14 out of 59 typically developing children had crowding ratios ≥ 2. This might 2
be explained by the relatively large number of younger children in this group:
a significant relationship between crowding ratio and age in the group without
brain damage suggests a developmental phenomenon.
Because in an earlier study applying Cambridge Crowding Cards in children
[16]
without ocular and neurological abnormalities standard deviations have
not been reported, we cannot statistically compare findings. Mean crowding
ratios found in 3-4 year olds seem comparable (1.7 vs. 1.8), whereas the
mean crowding ratio in 5-7-year olds in the present study is slightly higher
than in the earlier report (1.6 vs. 1.2).
Although the use of crowding ratio ≥ 2 may help to detect children with
unconfirmed brain damage, especially those with subnormal vision that are
otherwise not referred for or entitled to specialised diagnostics and low vi-
sion care, we did not address the question whether or not the crowding ratio
directly predicts perception problems and can be used as selection criterion
in low vision services. Studying the developmental changes of the crowding
ratio in relation to results on tasks with a high attentional load or with stimuli
that can be considered ‘crowded’ (i.e. visual search tasks and object percep-
tion tasks under suboptimal conditions), might help to answer the question
whether or not the crowding ratio can be used as selection criterion and pre-
dict higher visual impairments. If target identification in ‘crowded’ stimuli is
[5]
modulated by attention and determined by the attentional resolution, task
performance might be dependent on age and task duration. Young children
with brain damage might have a higher crowding ratio as well as weak per-
ception performances, whereas older children might perform normally on the
short acuity task but worse on perception tests, with their longer duration i.e.
with a higher attentional load.
Acknowledgements
We thank the participating children and their parents, the primary schools
(Eduard van Beinum, Openbare basisschool Charlois, De Bergse Zonnebloem,
Visio-school), Rijndam Rehabilitation Centre, and Royal Dutch Visio, all located
in Rotterdam, the Netherlands, for their participation and help.
34 Chapter 2
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Chapter
Chapter 3
3
[14, 15]
tive and stimulus characteristics, such as luminance contrast, influence
[6]
hV5+ activity.
Perception of complex motions, e.g. rotation, expansion contraction and
[16-20]
combination of these motions, is related to activity in MST. Biological
[21-23]
motion additionally activates the superior temporal sulcus (STS) region,
a ventral stream area.
Similarly, the perception of motion-defined forms does not only activate
dorsal stream motion areas, but also gives activity in ventral stream form
[24-26]
processing areas.
It is therefore clear, that visual motion perception is subserved by many
different cortical areas, and that various motion paradigms will differ in the
number and nature of the visual motion areas that they rely on for adequate
performance. Generally, it is presumed that motion perception tasks are valid
to study higher-level dorsal stream functioning and to identify motion percep-
tion problems in patients.
Figure 1. Three types of motion perception. A. Global motion. An RDK with upwards global motion
with a coherence level of 20%. Dots with an arrow move upwards, dots without an arrow move in
random direction. B. Biological motion. A point-light human walker, walking to the right. C. Motion-
defined form. Dots within the square move upwards. Dots outside the square move downwards.
Boundary of the square is only illustrative and not visible in the test condition.
background dots. The contour of the letter became clearer when the dots
moved faster. The proportion correctly named letters was used to determine
the motion sensitivity threshold in terms of motion speed and in terms of
visual acuity based on motion-defined letters.
Tasks for biological motion often consist of point-light figures (see Figure 2
right) made by placing white dots or small lights at the joints of the otherwise
[31]
invisible human or animal. In the study by Grossman et al, for instance,
observers had to discriminate a human walker from a scrambled walker and
indicate the position of the human walker. In order to make the task more
difficult, noise (extra dots) was added. A proportion correctly indicated human
walkers was used to determine the amount of additional dots the observer
could deal with.
A range of computerised motion perception tasks have been developed around
the world, but they are primarily applied in research settings. The advantage
of such tasks is, that they have a quantitative outcome measure: a perception
threshold. The use of motion perception tasks and thresholds is a way to
[31, 32]
objectify the presence and severity of a motion perception impairment,
which would be a relevant addition to clinical low vision diagnostics. Therefore,
we have dedicated a major part of this thesis to motion perception, performing
a systematic review of the literature to identify available tasks and judge their
qualities for use in clinical practice, followed by experimental research.
Introduction motion perception 43
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Chapter
Chapter 4
4
Applicability of computerised
motion perception tasks in clinical
practice for children. A systematic
review
46 Chapter 4
Abstract
Problem
A variety of computerised tasks is being used in research to assess motion
perception in children. Which can be applied in clinical diagnostics?
Methods
Published studies in children aged 2-12 years were systematically reviewed to
judge 1. types of tasks, technical specifications and quantitative outcomes; 2.
reliability of normal limits and developmental trends; 3. differences between
typically developing children and risk groups (mean performance and percent-
age abnormal performers).
Key findings
Global motion has been studied most extensively, whereas a smaller number
of studies focussed on motion-defined form and biological motion. There was a
wide variety in task characteristics, and confidence intervals for normal limits
were wide as a result of small age groups. Developmental trends were observed
for global motion and motion-defined form. Several risk groups performed
significantly worse than typically developing children, but taking confidence
intervals into account, there is only some evidence for an increased risk of
abnormal performance in children with autism, amblyopia, and prematurely
born children.
Interpretation
Computerised motion perception tasks can be used in clinical practice as ob-
servational instruments with quantifiable outcomes, but because of unreliable
normal limits, abnormal performers cannot yet be identified reliably. Interna-
tional collaboration might be needed to study larger patient groups in order to
estimate the prevalence of motion perception problems.
Systematic review motion perception 47
Introduction
Methods
Literature search
We searched for English-language articles and reviews on motion perception,
published until March, 2009, using several public databases. In ISI Web of
Knowledge we searched in all citation databases, setting the time span at
all years. In PubMed we only used a search string without additional limits.
For the search in Embase, the databases EMbase and Unique MEDLINE were
selected. A fourth and last search was done in PsycInfo. Search strings and
numbers of hits are shown in Table 1.
Eligibility of studies
Based on the abstracts, or if needed the complete article, two authors inde-
pendently judged the articles using the following inclusion criteria: original
article published in English; subgroups of participants containing at least 5
participants; children aged 2 to 12 years included in the study; typically de-
veloping children and/or patients studied; if patients were studied, at least a
typically developing control group had to be included too; motion perception,
specified as either motion coherence/global motion, motion defined form, or
biological motion was tested; biological motion tasks used stimuli express-
ing global motion of the whole human body; quantitative outcomes, other
than quality judgements of the imitation of presented motions, EEG and fMRI
Systematic review motion perception 49
results, were reported for the motion perception tasks; if typically developing
children older than 12 years of age were also studied, quantitative data for
a subgroup of children aged up to 12 years had to be extractable from the
published results. If a group of patients including children with a chronological
age above 12 years was matched by developmental age to a group of typically
developing children, results of patients with a developmental age up to 12
years had to be extractable from the article. If one of the above criteria was
not met, the article was excluded. We discussed all discrepancies in judge-
ment, until consensus was reached on the eligibility of the study.
4
Data extraction and quality assessment
The following data were extracted: date of publication, authors, recruitment
location for participants, and participant selection methods; type and number
of participants; type of task and task characteristics; type of quantitative re-
sults and formulae used; methods of statistical analysis; group results, group
differences and significance of differences.
Quality assessment, based on the Quality Assessment Tool for Quantitative
[6]
Studies, was done by two authors independently. Difficulties in data extrac-
tion and quality assessment were discussed, until consensus was reached.
For the evaluation of possible confounders, comparability of groups was as-
sessed. In comparative studies (patients vs. controls), we focussed on age,
visual acuity and social economical background (SES) or intelligence (IQ). In
developmental studies (only typically developing children of different ages)
we focussed on visual acuity and social economical background (SES) or intel-
ligence (IQ). We considered SES and IQ as one variable, because SES and IQ
are significantly related and SES seems to influence cognitive development
[7-9]
in children. In comparative studies, the confounding risk was rated ‘low’
if groups were comparable on all three variables or analysis had shown that
confounding was not likely, ‘moderate’ if confounding was not likely for two,
and ‘high’ if confounding was not likely for one variable. In developmental
studies, the confounding risk was rated ‘low’ if studies were longitudinal and
both variables were reported and controlled for; ‘moderate’ if studies were
cross-sectional and both variables were reported and controlled for; and ‘high’
if one variable was reported and controlled for.
Bias was assessed by judging the recruitment setting, selection procedure
and the level of participation (% agreement of invited persons). Because it
appeared, that such information was absent or limited in all articles, whereas
participant groups of all studies were too small to obtain reliable normal limits,
we ignored bias risk in the analyses and do not present the rating here.
50 Chapter 4
For the description of task characteristic and thresholds, all studies were
included. We examined the following task characteristics: response by partici-
pant, stimulus type, motion direction per trial, dot speed and dot size, as well
as task distance, monocular or binocular testing. For the evaluation of normal
limits and differences between risk groups and typically developing children,
we included studies with a low or moderate confounding risk.
Analysis
To study normal limits for the general population, we focussed on typically
developing children. Normal limits or cut-off values are crucial for diagnostic
use: a task performance outside the normal limits is labelled as abnormal
or deviant. Sample limits were used to estimate normal limits. To estimate
the precision of reported sample limits, we calculated the 95% confidence
intervals (95%-CI) for the intended percentage excluded participants with
[10, 11]
the exact binomial method of Clopper-Pearson. This confidence interval
indicates how many of the general population may be considered abnormal if
the reported normal limits are used.
To study and illustrate developmental trends for mean performance and
sample limits, we combined the data of typically developing children of differ-
ent studies in a graph, provided that outcome measures were identical, and
stimuli, responses and procedures were comparable, and drew a regression
th
line. To compare sample limits of different studies, we estimated p90 (90
percentile) for each sample, defined as 1.28 SD above the mean. We as-
sumed that data were distributed normally and that the reported mean and
SD were the true population values. The relation between age and outcome
was studied with the Spearman rho correlation and we drew illustrative trend
lines. Differences in performance on motion perception tasks between various
patient groups and controls were studied in two ways.
First, we evaluated group differences in mean performance. If summary
data, but no statistics were reported, group means were compared by means
of a t-test, provided that groups were comparable.
Second, we evaluated differences in the percentages of abnormal performers.
Only if the patient groups show a significantly higher frequency of abnormal
performers, it is likely that patients have a higher risk of motion perception
problems. To evaluate whether the percentage abnormal performers, observed
in patients, was significantly higher than that observed in controls, a binomial
proportion test for independent samples or Fisher’s exact test was used. These
tests were also used to evaluate whether more patients than controls would
be labelled as abnormal, under the assumption that the upper limit of the
Systematic review motion perception 51
Results
Study selection
Totally, 82 unique articles were found, of which 56 were excluded, some for
multiple reasons (Table 2). The remaining 26 articles were included in the
review, after discussion of six cases, primarily on the type of motion percep-
tion task and the extractability of data. Two tasks using global motion-like
stimuli were not included, because they were based on motion discrimination,
[12]
motion speed discrimination and motion direction discrimination, and not
[13]
on motion detection. In one article, no data were extractable for one of
two experiments on biological motion, therefore only one experiment was
[12-16]
included. For five studies also including children older than 12 years,
data of patients with a chronological age over 12 years but a younger mental
age were extracted, whereas for their control groups, only data of children
with a chronological age under 12 years were used.
Table 2. Main reason for exclusion of the articles not included in this review
Reason for exclusion # articles
Only abstract published 1
Qualitative review 7
Number of participants < 5 2
Age of participants outside range 2-12 years 18
Other task characteristics than specified for review 7
No quantitative outcome measures (fMRI, EEG, qualitative assessment motion imitation) 6
No quantitative data extractable for children in age range 2-13 years 14
Duplicate data 1
Total 56
52 Chapter 4
GM = global motion or motion coherence, MDF = motion-defined form; BM = biological motion (in-
cluding global human motion. Comp = comparative study, comparing patients with controls, Devc
= cross-sectional developmental study, comparing different age groups of typically developing chil-
dren.
Systematic review motion perception 53
Table 4a. Estimated normal limits in global motion studies, the intended percentages of persons in the general population that are excluded by use of the
estimated limit and labelled as abnormal performers, precision of sample limits (95%-CI), and percentages of abnormal performing patients according to the
sample limits.
Chapter 4
SL = sample limit, FE = fellow eye/non-amblyopic eye, Dmax_e = Dmax is elevated, Dmax_d = Dmax is depressed, p1-p2 is the difference between observed
proportions between patients and controls. The intended percentage excluded was used as observed proportion for controls, pUL-p2 is the difference between
a b
the observed proportion excluded patients and the upper limit of 95%-CI of the normal population. mean age or age range in years; 2.5% is excluded by
using lower sample limit or upper sample limit. A total of 5% will be excluded if both SLs are used.
Table 4b. Estimated normal limits in motion-defined form studies, the intended percentages of persons in the general population that are excluded by use
of the estimated limit and labelled as abnormal performers, precision of sample limits (95%-CI), and percentages of abnormal performing patients according
to the sample limits.
Controls Patients Statistical test
% intended % abnormal, p1-p2 pUL-p2
Formula for SL to exclude score outside
a
Study n Age SL-values (number) 95%- CI group n SL (number) 95%-CI p-value
Minimum dot speed
Ho et al 25 4.6 M + 1.64 SD 5% (n = 1 per 25) 0-20 amblyopia FE 21 24% (n = 5) 8-47 .01 ns
[28]
(2005) = 0.50 deg/s
25 7.5 M+ 1.64 SD
= 0.26 deg/s
25 10.6 M + 1.64 SD
= 0.23 deg/s
Wang et al 32 7.3 M + 1.64 SD 5% (n = 2) 1-21 amblyopia FE 6 67% (n = 4) 22-96 < .01 .05
[30]
(2007) = 0.26 deg/s
Giaschi et al 10 4-6 M + 2.5 SD 0.6% (n = 0) 0-31 amblyopia FE 20 90% (n = 18) 68-99 < .01 < .01
[31]
(1992) = 0.24 deg/s
10 7-9 M + 2.5 SD amblyopia AE 95% (n = 19) 75-100 < .01 < .01
= 0.10 deg/s
10 10-12 M + 2.5 SD
= 0.14 deg/s
Percentage correct
Jakobson et al 19 6.1 M - 2 SD 2.3% (n = 0) 0-18 preterm 43 47% (n = 20) 31-62 < .01 .02
[33]
(2006)
19 6.1 M - 3 SD 0.1% (n = 0) 0-18 33% (n = 14) 19-49 < .01 ns
SL = sample limit, FE = fellow eye/non-amblyopic eye, AE = amblyopic eye, p1-p2 is the difference between observed proportions between patients and con-
trols. The intended percentage excluded was used as observed proportion for controls, pUL-p2 is the difference between the observed proportion excluded in
a
patients and the upper limit of 95%-CI of the normal population. mean age or age range
Systematic review motion perception
55
4
56 Chapter 4
Developmental trends
To study possible developmental trends, we compared studies using similar
tasks, based on published results. On average, control groups consisted of 27
participants per author-defined age group (range 8-93, median 21). No stud-
ies were found for children aged 2-3 years, whereas data were very limited for
the ages 3-7 years and above 10 years.
In Figure 1A, mean results of control groups in global motion direction studies
[17, 25, 27, 28, 30]
and their estimated p90 are represented. Mean scores and the
estimated p90 seem to decrease significantly with increasing age, suggesting
that the minimum proportion of coherent moving dots, needed to identify the
motion direction correctly, becomes smaller with age. Mean coherence level
and the estimated normal limit are negatively related to age (mean ρ = -0.61;
p < .03; p90 ρ = -0.64; p < .02). This is illustrated by the linear trend lines
in the figure, because the quadratic effect was not significant. Additionally,
residual analysis of the trend line for p90 indicated the risk of overestimation of
performances in multiple age groups, with a maximum of 14% coherence. The
overestimation of performances could lead to an undesirably high number of
performers labelled as abnormal. Because of the unreliability of the estimators
and the risk of overestimation of performance, we consider the trend line not
the best way to evaluate the performance of clinically evaluated children. One
should use all information in the graph, position each clinically tested child
against the data from the presented studies.
In Figure 1B, means and estimated p90s are illustrated for two global motion
target location studies with motion coherence thresholds. No sample limits
[19, 20]
were reported in these articles. Mean coherence level and the estimated
p90 are negatively related to age (ρ = -0.71; p = .06). Again, the mean scores
and the estimated p90 seem to decrease significantly with increasing age and
visual inspection seems to indicate that there is a quadratic trend, although
the regression estimators for age are not significant, probably due to the low
number of data points. Therefore, the trend lines only illustrate the overall
mean coherence level and the overall mean of the p90’s.
Systematic review motion perception 57
Figure 1. Mean results and mean + 1.28 SD for studies with comparable motion perception stimuli
with a black background and white dots
1A. Global motion studies with a single target RDK and motion direction as response are represent-
[28] [30] [27]
ed. Symbols represent different studies: Ho et al, Wang et al, Pellicano & Gibson, Raymond
[17] [25]
& Sorensen and Chow & Ho. Dot speed, test distance varied per study. Linear regression trend
was significant.
1B. Global motion studies with two RDKs and with target location as response are represented:
[20] [19]
O’Brien et al and Gunn et al. Regression estimators, except constant, were not significant.
[30]
1C. Motion-defined form studies with naming as response are represented: Wang et al and Ho et
[28]
al. Curvilinear trend was significant, but is considered not generalisable.
Discussion
This systematic review shows that investigators around the world have in-
vested considerable energy into the development and evaluation of tests,
in order to enable quantified judgement of aspects of motion perception in
60 Chapter 4
children. It appears that global motion has been studied most extensively,
whereas a smaller number of studies focussed on motion-defined form and
biological motion. Because this field is still in a pioneering phase, there is a
wide variety of task characteristics, procedures and thresholds. Sample sizes
of age-groups are still small, so currently available estimates of normal limits
are insufficiently precise. First results suggest that developmental trends
are present for global motion and motion-defined form, whereas insufficient
data are available for biological motion. Based on comparison studies, first
potential risk groups have been identified. However, we must conclude that at
this stage, no motion perception tasks have been evaluated satisfactorily for
application as diagnostic instruments in clinical practice.
In our opinion, building further upon these pioneering activities, further
research should focus on international consensus development, test standar-
disation and collaboration of research groups, in order to include satisfactory
study samples.
Consensus is needed on: 1. tasks characteristics and task procedures;
2. (estimated) normal limits and age groups; 3. confounding risks for task
performances and group differences. We have formulated the following first
suggestions:
Ad 1. Because stimuli with a black background and white dots are most com-
mon, we suggest that at least a black and white stimulus should be included
in all studies.
Dot life-time should be limited, to prevent single dot tracking and dot speed
and motion direction should also be standardised.
The choice of dot speed might depend on the brain systems one wants
to study, and on the presence of additional disorders, like nystagmus. The
indication that the activity of V1 decreases with increasing motion speed and
that a direct route from the retina to the superior colliculus and pulvinar to the
[39, 40]
prestriate cortex might also be involved in motion perception, could be
a good reason to study multiple speeds. In this way, the integrity or develop-
mental status of multiple routes could be studied. We suggest, that at least a
slow speed (< 6 deg/s), at which V1 is activated before V5, and a high speed
task (> 15 deg/s), at which the colliculo-prestriate cortical route is assumed
to be the primary route, are studied.
The co-presence of nystagmus warrants special attention. In patients with
congenital nystagmus, adaptive perceptual processes that are considered to
prevent oscilliscopia (illusory motion of the visual world) are suggested to
[38, 41, 42]
result in a loss of sensitivity to motion of a stimulus. Elevated thresh-
olds as a result of adaptive perceptual processes seem to be more likely at low
Systematic review motion perception 61
[38, 42]
speeds, horizontal motion direction, which is often the direction of the
[38, 41] [38]
major component in congenital nystagmus, and larger stimulus size.
If the retinal image motion in patients with congenital nystagmus is simulated,
by adding continuous sinusoidal or ramp motion to stimuli for controls, motion
[41]
sensitivity of patients with nystagmus seems similar to that of controls. If
congenital nystagmus is present in the patient group, as additional disorder,
one might consider studying vertical motion with a high dot speed, or an
analysis including and excluding patients with nystagmus, for an indication of
the effect of nystagmus on the results.
4
Considering the stimuli described in this review and the above mentioned
criteria, we conclude for pragmatic reasons that the stimuli described by the
following authors may be eligible for standardisation of slow speed stimuli:
[27]
Pellicano and Gibson for global motion direction if dot speed is slightly
[26] [20]
reduced, Milne and co-authors or O’brien and co-authors, for global
motion target location if limited dot life-time is guaranteed, and Reiss and
[14]
co-authors for biological motion.
Target location stimuli for global motion and biological motion are preferable
in young children, because target detection tasks appear to be easier to ac-
complish than motion direction tasks at that age.
Although no limited dot life-time seems to be used in motion-defined form
[28]
stimuli, the stimuli described by Ho et al are studied most extensively and
therefore may be eligible for standardisation.
At this moment, we have no suggestions for high-speed stimuli with a black
background and white dots, because this has infrequently been studied and
only was used in motion direction tasks.
Ad 2. Current sample sizes are too small to set reliable sample limits and to es-
timate the prevalence of motion perception problems. Reliable percentile norms
[43]
would require groups of at least 120 participants per age category. Which
age groups should be studied, could be determined by studying the develop-
mental trend more extensively, ideally by doing a longitudinal study. However,
this would take many years and participants’ performances might improve over
time, due to growing task experience. The alternative is to cross-sectionally
study large study populations and identify relevant age groups in the analysis.
We realise that large samples, specifically of patients, are difficult to recruit and
therefore might require international collaboration of research groups.
Other normal limits than sample-based limits, such as a deficit ratio, seem
to be unsuitable for diagnostic purposes, because if a patient is matched to a
single control, normal variation in controls is disregarded and there is a risk of
erroneous judgements.
62 Chapter 4
Acknowledgements
We thank Paul Looijestein for his expert contribution to the discussion of the
results.
Systematic review motion perception 63
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order: Relationship to motor control and 2 : 4 digit ratio. Journal of Autism and
Developmental Disorders, 2006. 36(2): p. 225-237.
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visual pathway in autism and dyslexia. Neuropsychologia, 2008. 46(10): p. 2593-
2596.
28. Ho, C.S., et al., Deficient motion perception in the fellow eye of amblyopic chil-
dren. Vision Research, 2005. 45(12): p. 1615-1627.
29. Parrish, E., et al., The maturation of form and motion perception in school age
children. Vision Research, 2005. 45(7): p. 827-837.
30. Wang, J., C.S. Ho, and D.E. Giaschi, Deficient motion-defined and texture-defined
figure-ground segregation in amblyopic children. Journal of Pediatric Ophthalmol-
ogy & Strabismus, 2007. 44(6): p. 363-371.
31. Giaschi, D.E., et al., Defective Processing of Motion-Defined Form in the Fellow
Eye of Patients with Unilateral Amblyopia. Investigative Ophthalmology & Visual
Science, 1992. 33(8): p. 2483-2489.
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based on motion contrast. Exp Brain Res, 1999. 124(4): p. 469-73.
33. Jakobson, L., V. Frisk, and A. Downie, Motion-defined form processing in ex-
tremely premature children. Neuropsychologia, 2006. 44(10): p. 1777-1786.
34. Pavlova, M., et al., Recognition of point-light biological motion displays by young
children. Perception, 2001. 30(8): p. 925-933.
35. Blake, R., et al., Visual recognition of biological motion is impaired in children with
autism. Psychological Science, 2003. 14(2): p. 151-157.
36. Freire, A., et al., The development of sensitivity to biological motion in noise.
Perception, 2006. 35(5): p. 647-57.
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cal motion perception. Neuroreport, 2008. 19(18): p. 1763-1767.
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Systematic review motion perception 65
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Chapter
Chapter 4:
4: Appendix
Appendix 1
1
4A1
70
Table 2. Characteristics of motion-defined form studies: thresholds, responses, stimulus characteristics (stimulus type, motion direction, speed, dot size)
and test distance.
Test
Motion direction per Dot size distance
Threshold Response Stimulus type trial Speed (deg/s) (arcmin) (cm)
[4-6] [2]
1. Minimum dots speed 1. Identification 1. RDK, black background, white dots 1. motion in form opposite Slow (< 6 deg/s) - 3.8 - 61
[4-6, 18] [4-6] [20] [18] [19]
- Form - With 1 of 5 forms (circle, duck, to background motion - 0.021 - 0.68, - 15.6 - 100
[18] [2, 18, 20] [4-6] [2] [20]
2. Accuracy - Letter fish, heart, gingerbread man) - left or right - 0.039 - 1.26 - 22.8 - 200
Chapter 4: Appendix 1
1 arcmin = 1/60 degree. For a visual acuity of 1.0 one has to be able to discriminate an element 1 arcmin in size, a Snellen-E of 5 arcmin.
d’ , unbiased measure of sensitivity, is based on hits (target indicated as target) and false alarms (non-target indicated as target). A higher positive value
indicates a higher sensitivity to the target.
Appendix 1 Characteristics of motion perception studies
71
4A1
72 Chapter 4: Appendix 1
References
1. Raymond, J.E. and R.E. Sorensen, Visual motion perception in children with dys-
lexia: Normal detection but abnormal integration. Visual Cognition, 1998. 5(3):
p. 389-404.
2. Reiss, J.E., J.E. Hoffman, and B. Landau, Motion processing specialization in Wil-
liams syndrome. Vision Research, 2005. 45(27): p. 3379-3390.
3. Pellicano, E. and L.Y. Gibson, Investigating the functional integrity of the dorsal
visual pathway in autism and dyslexia. Neuropsychologia, 2008. 46(10): p. 2593-
2596.
4. Ho, C.S., et al., Deficient motion perception in the fellow eye of amblyopic chil-
dren. Vision Research, 2005. 45(12): p. 1615-1627.
5. Wang, J., C.S. Ho, and D.E. Giaschi, Deficient motion-defined and texture-defined
figure-ground segregation in amblyopic children. Journal of Pediatric Ophthalmol-
ogy & Strabismus, 2007. 44(6): p. 363-371.
6. Parrish, E., et al., The maturation of form and motion perception in school age
children. Vision Research, 2005. 45(7): p. 827-837.
7. Spencer, J., et al., Motion processing in autism: evidence for a dorsal stream
deficiency. Neuroreport, 2000. 11(12): p. 2765-2767.
8. O’Brien, J., et al., Form and motion coherence processing in dyspraxia: evidence
of a global spatial processing deficit. Neuroreport, 2002. 13(11): p. 1399-1402.
9. Gunn, A., et al., Dorsal and ventral stream sensitivity in normal development and
hemiplegia. Neuroreport, 2002. 13(6): p. 843-847.
10. Atkinson, J., et al., Neurobiological models of visuospatial cognition in children
with Williams syndrome: measures of dorsal-stream and frontal function. Dev
Neuropsychol, 2003. 23(1-2): p. 139-72.
11. Ellemberg, D., et al., Putting order into the development of sensitivity to global
motion. Vision Research, 2004. 44(20): p. 2403-2411.
12. MacKay, T.L., et al., Deficits in the processing of local and global motion in very
low birthweight children. Neuropsychologia, 2005. 43(12): p. 1738-48.
13. Chow, E.M.-C. and C.S.-H. Ho, Visual motion perception in Chinese dyslexic chil-
dren. Journal of Psychology in Chinese Societies, 2005. 6(2): p. 161-178.
14. Ellemberg, D., et al., Better perception of global motion after monocular than
after binocular deprivation. Vision Res, 2002. 42(2): p. 169-79.
15. Milne, E., et al., Motion and form coherence detection in autistic spectrum dis-
order: Relationship to motor control and 2 : 4 digit ratio. Journal of Autism and
Developmental Disorders, 2006. 36(2): p. 225-237.
16. Del Viva, M.M., et al., Spatial and motion integration in children with autism.
Vision Research, 2006. 46(8-9): p. 1242-1252.
17. Mendes, M., et al., Visual magnocellular and structure from motion perceptual
deficits in a neurodevelopmental model of dorsal stream function. Brain Res Cogn
Brain Res, 2005. 25(3): p. 788-98.
18. Giaschi, D.E., et al., Defective Processing of Motion-Defined Form in the Fellow
Eye of Patients with Unilateral Amblyopia. Investigative Ophthalmology & Visual
Science, 1992. 33(8): p. 2483-2489.
Appendix 1 Characteristics of motion perception studies 73
19. Schrauf, M., E.R. Wist, and W.H. Ehrenstein, Development of dynamic vision
based on motion contrast. Exp Brain Res, 1999. 124(4): p. 469-73.
20. Jakobson, L., V. Frisk, and A. Downie, Motion-defined form processing in ex-
tremely premature children. Neuropsychologia, 2006. 44(10): p. 1777-1786.
21. Blake, R., et al., Visual recognition of biological motion is impaired in children with
autism. Psychological Science, 2003. 14(2): p. 151-157.
22. Jordan, H., et al., Intact perception of biological motion in the face of profound
spatial deficits: Williams syndrome. Psychological Science, 2002. 13(2): p. 162-
167.
23. Lichtensteiger, J., et al., Role of dorsal and ventral stream development in biologi-
cal motion perception. Neuroreport, 2008. 19(18): p. 1763-1767. 4A1
24. Pavlova, M., et al., Recognition of point-light biological motion displays by young
children. Perception, 2001. 30(8): p. 925-933.
25. Freire, A., et al., The development of sensitivity to biological motion in noise.
Perception, 2006. 35(5): p. 647-57.
26. Moore, D.G., R.P. Hobson, and M. Anderson, Person Perception - Does It Involve
Iq-Independent Perceptual Processing. Intelligence, 1995. 20(1): p. 65-86.
Chapter
Chapter 4:
4: Appendix
Appendix 2
2
1. Amblyopia
[1]
Ho et al (2005)
Amblyopia,
non-amblyopic eye Controls Statistics
n 21 21
4A2
Gender (% male) - -
Age range in years 4.4-11.0 4.3-11.2
(mean; SD) (6.9; 1.7) (7.0; 1.9)
IQ information - -
Motion perception MANOVA
Group: F(3, 38) = 4.71, p < .01
Global motion
a b
Mean motion coherence % 26 25 F(1, 40) = 0.01,
(SD; range) (22; 3-81) (18) p = .91, f = 0.00
a b
Dmax deg 1.24 1.04 F(1, 40) = 0.23,
(SD; range) (0.79; 0.49-3.70) (0.26) p = .63; f = 0.08
Motion-defined form
a b
Minimum dots speed deg/s 0.20 0.10 F(1, 40) = 13.55,
(SD; range) (0.13; 0.07-0.61) (0,04) p < .01; f = 0.58
a b
Data was extracted from table with individual data and figure with group results; Results if abnor-
mal performers are excluded: Motion coherence %: 19 (14; 3-47); Dmax : 0.99 (0.24; 0.55-1.37);
deg/s: 0.16 (0.08; 0.07-0.34).
[2]
Wang et al (2007)
Amblyopia,
a
non-amblyopic eye Controls Statistics
n 6 32
Gender (% male) -
Age range in years 5.81-8.66 5-8
(mean; SD) (6.8; 1.1) (7.3; 1.1)
IQ information - -
Motion perception MANOVA
Group: F(2, 9) = 4.50, p < .04
Global motion
Mean motion coherence % 20 20 F(1, 10) = 4.133,
(SD; range) (16; 9-47) (15) p < .07, ns
Motion defined form
Mean minimum dot speed deg/sec 0.39 0.14 ns
(SD; range) (0.32; 0.07-0.91) (0.08)
a
an age matched control group (n = 6) was used for analysis (mean age 6.8 years, SD = 1.1),
post-hoc univariate F-test was controlled for multiple comparisons with Bonferroni adjustment set at
0.025 for each task. Also a texture defined task was used.
78 Chapter 4: Appendix 2
2. Autism
Global motion
Global motion study with target location as response and motion coherence level
(%;(Signal dots/(Signal dots + Noise dots)*100) as outcome.
[3]
Milne et al (2006)
Autism spectrum
disorder Controls Statistics
n 23 23
Gender (% male) 96 43
Age range in years 8.0-12.92 8.83-12.33
(mean; SD) (10.08; 1.67) (10.25; 1.08)
a
Mean non-verbal IQ 95 102
(SD; range) (14.2; 70-122) (14.1; 84-130)
Global motion
Mean motion coherence level % 17.09 10.26 Mann-Witney: ns
(SD; range) (15.22; 6.24-55.14) (4.13; 3.55-19.65)
a
Outcomes of Raven’s (standard) progressive matrices were used to calculate non-verbal IQ.
Global motion
Global motion studies with motion direction as response and motion sensitivity ((Signal dots +Noise
dots)/Signal dots) or motion coherence level (%;(Signal dots/Noise dots)*100) as outcome.
[4]
Del Viva et al (2006)
Verbal mental
Age matched age matched
Autism controls controls Statistics
n 10 14 12
Gender (% male) - - -
Age range in years 6.0-14.1 8.0-11.9 6.1-7.2
(mean; SD) (8.8; 3.0) (9.7;0.8) (6.6; 0.3)
Mean verbal 6.7 - matched
a
mental age years (2.5;4.4-12.3)
Global motion ANOVA
Mean motion Group: F = 5.8, p < .01
sensitivity (%) per Control groups: p < .05
test condition Patients vs. age-matched
controls: ns
Patients vs. verbal mental age
matched controls: ns
Rotation 14.4 23.1 18.2 Student t-test
(SD; range) (3.7; 7.9-21.2) (5.2;12.7-30.4) (6.0; 9.0-27.2) Patients vs. Age-matched
Horizontal 20.3 18.1 14.4 controls:
(SD; range) (7.8;12.0-36.8) (2.7;13.1-21.9) (2.8; 11.7-19.2) Rotation: p < .01
Expansion & horizontal: ns
Contraction/ 15.1 16.1 13.3
Patients vs. Verbal mental age
Expansion (3.0; 11.1-22.3) (3.8;11.7-26) (2.1; 9.1-16.5)
matched controls:
(SD; range)
Horizontal: p = .02
Expansion
(p = .1) & rotation (p = .05):
ns
a
Data of the WISC-R was used to estimate the verbal mental age ((chronological age*VIQ)/100).
The reported mean verbal age is that of the total patient group (n = 13, mean chronological age in
years = 10.9, SD = 4.2).
Appendix 2 Outcomes of motion perception studies 79
[5]
Pellicano & Gibson (2008)
ab
Autism Controls Statistics
n 20 61
Gender (% male) 90 77
Age range in years 8.08-12.33 8.00-12.58
(mean; SD) (9.59; 1.38) (9.88; 1.01)
c
Mean non-verbal IQ 107.10 106.82
(SD) (8.95) (12.90)
c
Verbal IQ 97.00 104.28
(SD) (15.25) (11.60)
Global motion 4A2
Mean motion coherence 22.40 14.02 ANOVA
level % (13.78; 5.31-54.44) (6.70; 4.41-40.53) Group: F(2, 119) =
(SD; range) 10.82, p < .001
t(119) = 2.41, p < .01,
d = 1.01
a
Effect of outliers was reduced by scores more than 3 SD above/below the group mean were re-
b
placed by a score at 2.5 SD before calculation of standard scores and analysis took place; Also a
c
group with dyslexia was included. Autism vs. dyslexia: t(119) = 1.08, ns; Outcomes of Raven’s
(standard) progressive matrices or Wechsler Abbreviated Scale of Intelligence (WASI) were used
to assess non-verbal IQ, outcomes of the Peabody Picture Vocabulary Test or Wechsler Abbreviated
Scale of Intelligence were used to assess verbal IQ.
80 Chapter 4: Appendix 2
3. Dyslexia
Global motion
Global motion studies with motion direction as response and motion coherence level (%;(Signal
dots/(Signal dots + Noise dots)*100) as outcome.
[6]
Raymond & Sorensen (1998)
a
Experiment 1a Dyslexia Controls Statistics
n 10 10
Gender (% male) 50 50
Age range in years 7.3-11.3 7.3-11.3
(Mean; SD) (9.9; 1.2) (9.9; 1.2)
Mean IQ 98 At least average
(SD) (9.8)
Reading level At least 1.5 years Assumed at age
below age level level
Global motion
Mean motion coherence level (%) per
stimulus condition
Noise and no-noise, 60 ms 39.8 19.9 p < .01
b
(SD; range ) (17.2; 18-70) (2.9; 17-26)
Experiment 2 Dyslexia Controls Controls Statistics
n 12 12 8
Gender (% male) 50 41 38
Age range in years - - -
(mean; SD) (11.6) (9.3) (8.0)
IQ Mean (SD) - -
Reading level At least 1.5 years Assumed at age
below age level level
Global motion
Mean motion coherence level (%) per
stimulus condition
2 short frames, 64 ms 26.3 25.4 - ns
b
(SD; range) (15; 14-56) (14; 9-48)
7 short-frames, 224 ms 19.9 10.5 - p < .01
b
(SD; range) (8; 8-34) (4; 4-16)
2 long-frames, 224 ms - - 25
b
(SD; range) (10; 11-41)
a b
Experiment 1b is excluded, because the sample size of the control group was too small; Data was
partially extracted from a figure with individual results.
Appendix 2 Outcomes of motion perception studies 81
[7]
Chow & Ho (2005)
Dyslexia Controls Statistics
n 24 24
Gender (% male) - -
Age range in years - -
(mean; SD) (9.16; 1.38) (9.12; 1.29)
a
Mean non-verbal IQ 106.21 106.00
(SD) (8.28) (7.10)
Global motion
Mean motion coherence level
(%) per test condition
White dots 36.59 24.73 Two-way mixed design
4A2
(SD) (8.63) (2.26) ANOVA:
Group x Colour:
Blue dots 31.97 23.30
F(2,41) = 5.83,
(SD) (7.91) (0.87)
p < .01
Red dots 35.83 24.81 Group: F(1,47) =
(SD) (10.62) (1.93) 37.58, p < .01
Total 34.80 24.28
(SD) (9.23) (1.90)
a
Outcomes of Raven’s (standard) progressive matrices were used to calculate non-verbal IQ.
[5]
Pellicano & Gibson (2008)
ab
Dyslexia Controls Statistics
n 41 61
Gender (% male) 63 77
Age range in years 8.08-12.33 8.00-12.58
(mean; SD) (9.97; 1.10) (9.88; 1.01)
c
Mean non-verbal IQ 106.76 106.82
(11.38) (12.90)
c
Verbal IQ 110.15 104.28
(SD) (10.05) (11.60)
Global motion
Mean motion coherence 26.38 14.02 ANOVA
level % (19.60; 5.19-75.50) (6.70; 4.41-40.53) Group: F(2, 119) =
(SD; range) 10.82, p < .001
t(119) = 4.54,
p < .001, d = 1.32
a
Effect of outliers was reduced by scores more than 3 SD above/below the group mean were re-
b
placed by a score at 2.5 SD before calculation of standard scores and analysis took place; Also a
c
group with dyslexia was included. Autism vs. dyslexia: t(119) = 1.08, ns; Outcomes of Raven’s
(standard) progressive matrices or Wechsler Abbreviated Scale of Intelligence (WASI) were used
to assess non-verbal IQ, outcomes of the Peabody Picture Vocabulary Test or Wechsler Abbreviated
Scale of Intelligence were used to assess verbal IQ.
82 Chapter 4: Appendix 2
4. Dyspraxia
Global motion
Global motion study with target location as response and motion coherence level
(%;(Signal dots/Noise dots)*100) as outcome.
[8]
O’Brien et al (2002)
Chronological age
and verbal mental
Pure dyspraxia age matched controls Statistics
n 8 50 F(1,56) = 1.2; ns
Gender (% male) 75 -
Age range in years 7-11 matched
(mean; SD) (8.2; 1.5) (8.4)
a
Verbal mental age matched matched
Global motion
Mean motion coherence level 14.9 17.5
% (SD) (7.9) (6.1)
a
Outcomes of the British Picture Vocabulary Scale were used to estimate mental age.
5. Hemiplegia
Global motion
Global motion study with target location as response and motion coherence level as
outcome.
[9]
Gunn et al (2002) Threshold: Motion coherence level (%); Response: target Location
a
Hemiplegia Controls Statistics
n 22 295 repeated measure
ANOVA with age as
Gender (% male)
covariate: interaction
b
Age range in years 3.2-12.4 4.10 –11.99 task*group :
(mean; SD) (-) (-) F(1,381) = 5.6;
p < .02
IQ information - -
t-test done by
Global motion reviewers for threshold
Mean coherence level % 36.8 28.8 difference
(SD; range) (10.4; 26.4-61.4) (8.4) p < .01
a
Two patients were excluded because of the age criterion, data was therefore estimated from figures
b
with individual data; also a global form task was done.
Appendix 2 Outcomes of motion perception studies 83
6. Intellectual disability
Biological motion
Biological motion study with identification as response and minimum exposure duration
as outcome.
[10]
Moore et al (1995) Threshold:Minimum exposure duration (ms), response naming
Intellectually Verbal mental age
disabled matched controls Statistics
n 15 15
Gender (% male) - -
Age range in years 9.75 -16.42 11.92-10.58
(mean; SD) (14.17; 1.67) (8.42;1.17) 4A2
a
Verbal mental age 6.00-10.33 6.25-10.33
(mean, SD) (8.08; 1.33) (8.33; 1.25)
a
Verbal IQ 61.5 100.4
(mean, SD) (7.3; 49-71) (4.3; 91-106)
Biological motion
Mean exposure duration in ms
b
per test condition
c
First presentation: 5PLW 203 309 Sign test: ns
(SD; range) - -
c
Second presentation: 10PLW 123 149 Sign test: ns
(SD; range) - -
Total 163 229 Sign test: p = .09, ns
(SD; range) - -
a
Outcomes of the British Picture Vocabulary Scale were used to match subjects pair wise and assess
b c
verbal IQ; Data was partially extracted from a figure with individual results; 5PLW = point-light
walker made of 5 dots, 10PLW is point-light walker made of 10 dots.
84 Chapter 4: Appendix 2
Motion-defined form
Motion-defined form study with gap position location as response and percentage correct responses
as outcome.
[11]
Jakobson et al (2006) Threshold: Percentage correct response &, response: gap position
Preterm Age
and SES
matched
No ROP PVBI ROP and full-term
and PVBI ROP only only PVBI Total controls Statistics
n 11 12 10 10 43 19
Gender (% male) - - - - 34 47
Age range in - - - - 5.25-6.83 5.25-6.83
years (6.08; (6.08;
(mean; SD) 0.52) 0.52)
IQ information - - - -
Performance IQ - - - - 90.5 109.3
(SD) (10.6) (13.0)
Verbal IQ - - - - 91.0 114.3
(SD) (10.8) (16.0)
Motion-defined
letter
a
correct % 61 47 46 37 48 71 ANOVA
(SD) (14) (11) (13) (13) (16) (19) Group:
F(4, 57) =
10.16,
p < .01,
2
η = .42
ROP vs.
control
PVBI vs.
control
ROP and
PVBI vs.
control: p
< .05
a
PVBI = periventricular brain injury; ROP = retinopathy of prematurity; Data partially extracted
from a figure with group results.
Appendix 2 Outcomes of motion perception studies 85
Global motion
Global motion study with motion direction as response and motion coherence level
(%;(Signal dots/(Signal dots + Noise dots)*100) as outcome.
[12]
MacKay et al (2005)
VLBW, without
major neurological
a
abnormalities A term controls Statistics
n 19 19
Gender (% male) 47 53
Age range in years 5.17-8.42 4.92-8.92 4A2
(mean; SD) (6.83; 0.98) (6.83; 1.28)
Mean Verbal IQ 103.8 110.9
(SD) (9.8) (6.9)
Global motion
Mean coherence level % 29.81 9.80 MANCOVA, controlling
(SD) (29.20) (11.72) for age
F(5,29) = 4.12,
p < .01
Group: p < .01
t(22) =−2.70, p < .05
a b
Number of participants for analysis is 18, 1 control and 1 patient were not tested on global motion;
Peabody Picture Vocabulary Test- Third Edition was used to assess Verbal IQ.
86 Chapter 4: Appendix 2
9. Williams syndrome
[13]
Reiss et al (2005)
Mental age matched
c
Williams Syndrome controls Statistics
n 10 10
Gender (% male) - -
Age range in years 9.25-18.3 4.92-7.58
(mean; SD) (14.25; -) (6.08; -)
a
IQ test information
Composite IQ-score 63.7 119.50
(SD) (15.97) (9.04)
Mean verbal score 38.30 34.40
(SD) (7.72) (5.22)
Mean matrices score 20.80 20.10
(SD) (4.21) (3.35)
Mean coherence level (%) Mixed-model repeated
b
per test condition measure ANOVA
Group: F(3, 36) =
3.10, p < .04
Global motion 8 8 t(18) < 1.54, ns
(SD; range) (5) (-)
Motion defined form 56 32 t(18) = 4.01,
(SD; range) (11) (7) p < .001
Biological motion 23 36 t(18) = 2.38,
(SD; range) (16) (13) p < .04
a
Outcomes of the Kaufman Brief Intelligence Test were used to match patients to controls on mental
b c
age; Data was extracted from a figure with group results; Study also included adult groups
Appendix 2 Outcomes of motion perception studies 87
Biological motion
Biological motion study with walking direction as response and percentage correct
responses as outcome.
[14]
Jordan et al (2002) Percentage correct & walking direction
Mental age matched
b
Williams Syndrome controls Statistics
n 10 10
Gender (% male) - -
Age range in years 9.33-15.58 4.25-7.25
(mean; SD) (11.58;-) (6.0;-)
a
IQ test information
4A2
Composite IQ-score 62.60 116.40
(SD) (15.72) (9.83)
Mean verbal score 33.15 31.60
(SD) (6.10) (4.59)
Mean matrices score 18.50 19.16
(SD) (2.56) (3.35)
Biological motion
Mean percentage correct per Mixed-model repeated
test condition measures ANOVA
Group x S/N ratio x
Noise Type
c
S/N ratio 1:1 97.54 89.20 Groups: F(2, 25) =
(SD; range) - - 9.11, p < .01
Post hoc comparison:
p < .01
c
S/N ratio 1:3 84.26 77.78 Groups: F(2, 25) =
(SD; range) - - 9.45, p < .01
Post hoc comparison:
p = .18, ns
total 90.90 83.49 Groups: F(2, 25) =
(SD; range) - - 11.33, p < .01
Post hoc comparison:
p < .05
a
Outcomes of the Kaufman Brief Intelligence Test was used to match patients to controls on mental
b
age; Study also included a group with adult controls, only group effect and post hoc comparison
c
for the patients vs. mental-age matched controls are reported; S/N = number of signal dots (S)/
number of noise dots (N)
88 Chapter 4: Appendix 2
Global motion
Global motion study with target or non-target as response and motion coherence level as outcome.
[15]
Mendes et al (2005)
c
Williams Syndrome Mental age matched Statistics
n 6 11
Gender (% male) 33 64
Age range in years 11-20 5-14
(mean; SD) (16.00;3.52) (9.09;3.08)
Mental age 6.5-10
(8.67;1.44)
a
IQ information
Performance IQ 44.3 -
(SD) (2.58)
Verbal IQ 52 -
(SD) (6.98)
Global motion
b
Mean coherence level (%) per test condition Mann-Whitney
Global motion or noise (SD) 36 28 ns
(12) (7)
3D global motion or 2D noise 35 12 p < .01
no time pressure (SD) (12) (2)
3D global motion or 2D noise 31 26 p = .02
200 ms per trial (SD) (16) (9)
a b c
WISC-3 or WAIS was used to assess IQ; Data was extracted from a figure with group results;
Control group consisted of 8, 9, 8 age matched controls for consecutive test conditions. The patient
group consisted of 5 patients in the 3D time constraint condition.
Appendix 2 Outcomes of motion perception studies 89
Global motion
Global motion study with letter identification as response and Minimum dots speed
(deg/s) as outcome.
[16]
Giaschi et al (1992)
Controls
4-6 year olds 7-9 year olds 10-12 year olds Total
n 10 10 10 30
Gender (% male) - - - -
4A2
Age range in years - - - 3.67 -13.5
(mean; SD) (8.42-2.75)
IQ information - - - -
Motion-defined letter
Mean minimum dot 0.14 0.05 0.06 -
speed deg/s (0.04) (0.02) (0.03)
(SD; range)
Global motion
Global motion study with target location as response and motion coherence level as outcome.
[9]
Gunn et al (2002)
a
Controls
4 year 5 year 6-7 year 8-9 year 10-11 year
olds olds olds olds olds Statistics
n 37 93 60 50 55
Gender (% male) - - - - -
Age range in years 4.10-5.29 5.30-5.99 6.00-7.99 8.00-9.99 10.00-11.99
(mean; SD) (-) (-) (-) (-) (-)
IQ information - - - - -
Global motion
Mean motion coherence 34.2 29.5 28.0 28.8 24.9 F(5,354) =
level % (11.3) (8.2) (7.0) (7.7) (6.2) 15.6;
(SD; range) p < .001
a
data of adults is excluded
90 Chapter 4: Appendix 2
[1]
Ho et al (2005)
Controls
3-5 year olds 6-8 year olds 9-11 year olds
n 25 25 25
Gender (% male) - - -
Age range in years - - -
(mean; SD) (4.63; 0.65) (7.46;0.88) (10.65; 0.93)
IQ information - - -
Motion tests
Global motion
Mean motion coherence level % 30 22 19
(SD; range) (25) (16) (10)
Mean Dmax deg 0.90 1.03 1.00
(SD; range) (0.28) (0.27) (0.22)
Motion-defined form
Mean Minimum dots speed 0.24 0.13 0.12
deg/s (0.16) (0.08) (0.07)
(SD; range)
Appendix 2 Outcomes of motion perception studies 91
Global motion
Global motion study with motion direction as response and coherence level as outcome.
[17]_1
Ellemberg et al (2002)
Congenital bilateral Congenital unilateral
a a
(CB) cataract (CU) cataract
Non-
deprived Deprived
Best eye Worst eye eye eye Controls Statistics
4A2
n 6 6 9 9 12
Gender (% male)
Age range in 5.0-11.7 5.0-11.7 4.1-12.1 4.1-12.1 -
years (7.15; 2.42) (7.15; 2.42) (6.68; 2.24) (6.68; 2.24) (6.0; 0.17)
(mean; SD)
IQ information - - - - -
Global motion ANOVA
Group: F(4,
54) = 4.40,
p < .01
b
Mean motion 42.7 45.5 16.8 15.6 9.0 CB and CU
coherence level % (16.5; 19-63) (19.6; 26-75) (4.2; 7-22) (3.9; 7-19) both eyes
worse than
controls: p
c
<.01.
[17]_2
Ellemberg et al (2002)
Developmental unilateral
a
(DU) cataract
Non-deprived
eye Deprived eye Controls Statistics
n 7 7 12
Gender (% male)
Age range in years 6.0-12.5 6.0-12.5 -
(mean; SD) (9.63; 2.09) (9.63; 2.09) (6.0; 0.17)
IQ information - - -
Global motion
Mean motion 10.1 11.1 9.0 ns
coherence level % (2.0; 8-14) (1.6; 9-14) (-) j
a
2 patients with bilateral congenital cataract, 5 patients with unilateral congenital cataract and 2
patients with developmental cataract were excluded because they were older than 12.99 years of
age. Bilateral developmental cataract was excluded because of the low number of remaining patients
b c
within the age criterion; Data extracted from a figure with group results; Patients with congenital
unilateral cataract performed better with the deprived eye than patients with congenital bilateral
cataract with either eye (p < .01). The performance with the deprived and the non-deprived eye of
the patients with congenital unilateral cataract did not differ significantly.
92 Chapter 4: Appendix 2
Global motion
Global motion studies with target location as response and motion coherence level
(%;(Signal dots/Noise dots)*100) as outcome.
[18]
Spencer et al (2000)
Autism Controls Statistics
n 23 50
Gender (% male) - -
Age range in years - -
(mean; SD)
a
Verbal mental age in years 7-11 7-11
Global motion
Mean motion coherence 25.5 17.5 F(1,72) = 10.98,
level % p < .01
(SD)
a
Test used to assess verbal mental age is not reported
Global motion
Global motion study with target location as response and motion coherence level as
outcome.
[19]
Atkinson et al (2003)
Williams
a d
Syndrome Statistics
n - - - - 41
Gender (% male) -
Age range in years 4-5.5 5.5-6.9 7-8 10-11 4.75-12.99
(mean; SD) (-)
b
Mental age years ≥4
Global motion
Mean motion 32 -
c
coherence level % (12)
(SD)
Median motion 31 30 24 20 29
c
coherence level %
(SD)
P90 motion coherence 54 37 30 26 -
c
level%
a b
4 patients were excluded because of the age the criterion; Outcomes of the British Picture Vo-
c
cabulary Scale were used to assess mental age in patients; Data was extracted from a figure with
d
group results for controls and individual results for patients; Patients results were only compared
to p90 of controls (percentile 90) of controls: 45% of patients performed worse than p90 percentile, if
mental age was used for performance evaluations 18% of patients performed worse than p90
Appendix 2 Outcomes of motion perception studies 93
Biological motion
Biological motion study with target or non-target as unbiased measure of sensitivity (d’)
as outcome.
[20]
Blake et al (2003)
Autism Controls Statistics
n 12 9
Gender (% male)
Age range in years 8-10 5-10
(SD) (-) (8.42; 1.89)
IQ information - -
Biological motion 4A2
unbiased measure of sensitivity d’ 2.52 1.17 t(19) = 2.68,
a
(SD) (0.5) (0.7) p = .02
a
Data was extracted from a figure with group results.
Motion-defined form
Motion-defined form study with gap position as response and (weighted) percentage
Correct response as outcome.
[21]
Schrauf et al (1999)
Controls
4 5 6 7 8 9 10 11 12
year year year year year year year year year
olds olds olds olds olds olds olds olds olds
n - - - - - - - - -
Age range in years - - - - - - - - -
IQ information - - - - - - - - -
Motion-defined form
Males
Mean percentage correct 67 67 67 69 72 75 78 80 81
ab
% (7) (7) (8) (9) (3) (2) (3) (3) (4)
(SEM)
Females
Mean percentage correct 74 (7) 74 (6) 74 (7) 74 (7) 74 (3) 74 (4) 75 (5) 76 (5) 77 (5)
a
%
a b
Data was extracted from a figure with group results; In the age group 4-6 year olds also mean
percentage correct % per coherence level was illustrated: 100% coherence 94% (SEM = 1); 50%
coherence 90% (SEM = 3); 30% coherence 79% (SEM = 4); 20% coherence 63% (SEM = 5).
94 Chapter 4: Appendix 2
Biological motion
Biological motion study with naming and facing direction as response and percentage
correct as outcome.
[22]
Pavlova et al (2001)
Controls
3 year olds 4 year olds 5 year olds
n 16 16 16
Gender (% male) 63 56 50
Age range in years - - -
(SD) (3.58; 0.17) (4.42; 0.25) (5.42; 0.33)
IQ information - -
Biological motion
Naming PLW
Mean percentage correct % 23 42 100
Global motion
Global motion study with motion direction as response and coherence level (%;(Signal
gabors/(Signal gabors + Noise gabors)*100)as outcome.
[23]
Ellemberg et al (2004)
a
Controls Statistics
n 24
Gender (% male)
Age range in years 4.75-5.25 (5.0; -)
(mean; SD)
IQ information -
Global motion
Mean motion coherence level % per test
condition
a
Luminance defined Age : F(1, 46) = 24.03, p < .01
speed 1.5 deg/s 24 Speed: F(2, 46) = 26.80,
(SD) (20) p < .01
speed 6 deg/s 7
speed 9 deg/s 6
a
Contrast defined Age : F(1, 46) = 27.51, p < .01
speed 1.5 deg/s 36 Speed: F(2, 46) = 40.53,
(SD) (29) p < .01
speed 6 deg/s 8
speed 9 deg/s 7
a
An adult group was included in the original study.
Appendix 2 Outcomes of motion perception studies 95
Motion-defined form
Global motion study with motion direction as response and coherence level as outcome.
Motion-defined form study with identification as response and minimum dots speed
(deg/s) as outcome.
[24]
Parrish et al (2005)
Controls
3-4 5-6 7-8 9-10 11-12
a
year olds year olds year olds year olds year olds Statistics
n 11-33 11-33 11-33 11-33 11-33
Gender (% male) - - - - -
Age range in
years
- - - - -
4A2
IQ information - - - - -
Motion perception
Global motion MANOVA
Age group:
n 23 23 23 23 23
F(10, 130) =
Mean coherence 33 30 23 24 30 1.37, ns
level %
n 11 11 11 11 11 MANOVA
Age group:
Mean Dmax deg 0.86 0.97 1.05 1.05 1.06
F(10, 118) =
2.39,
c
p < .05
ANCOVA with
covariate visual
acuity (LogMAR)
Age group: F(5,
61) = 3.85, p
< .05
Motion-defined MANOVA
form Age group: F(8,
188) = 2.95, p
n 13 13 13 13 13 b
< .01.
Mean minimum 0.28 0.18 0.14 0.09 0.14 ANCOVA with
dot speed deg/s (0.06) (0.03) (0.02) (0.02) (0.04) covariate visual
(SD) acuity (LogMAR)
Age group: F(4,
59) = 1.89, ns
a
Global motion studies included an adult group. Each age group for the mean coherence level analy-
b
sis consisted of 12 subjects; Performance of 3-4 year olds was significantly different from other
c
groups (p-value not available); Performance of 3-4 and 5-6 year olds was significantly different
from adults (p-value not available).
96 Chapter 4: Appendix 2
Biological motion
Biological motion study with target or non-target as response and percentage correct and
number of tolerated noise dots as outcome.
[25]
Freire et al (2006)
Controls
a
6 year olds 9 year olds Statistics
n 24 24
Gender (% male) 50 62
Age range in years - -
(SD) (6.0; 0.25) (9.0; 0.25)
IQ information -
Biological motion
Correct identification
Mean percentage correct % 95 94
(SD; range) (-; 90-100) (-; 86-100)
b
Mean number of noise dots 69.26 77.76 Age group: F(2, 69) =
c c
tolerated (12) (12) 6.00, p < .01
(SD) 6 year olds vs. adults:
p <.01
9 year olds vs. adults:
ns
a b c
Also an adult group was included in the study; One outliers was replaced by the group mean;
Data was extracted from a figure with group results.
Biological motion
Biological motion study with target or non-target as response and reaction time as
outcome.
[26]
Lichtensteiger et al (2008)
a
Controls Statistics
n 13
Gender (% male) 62
Age range in years -
(SD) (6.59; 1.2)
IQ information -
Biological motion Age group: F(1, 29) = 57.36,
p < .01. Children are slower
Target
than adults
Mean reaction time sec 1.36 (0.22)
(SD; range)
Non-target
Mean reaction time sec 1.50 (0.25)
(SD; range)
a
Also an adult group was included in the study.
Appendix 2 Outcomes of motion perception studies 97
References
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98 Chapter 4: Appendix 2
van der Zee, Y., Stiers, P., Lagae, L., Pel, J., & Evenhuis, H. (2018).
Chronological age versus developmental age in evaluating patients’
performances on motion perception tests. Accepted for publication
in Neuropsychological Trends.
100 Chapter 5
Abstract
Introduction
level of functioning might not be the best predictor or control factor for their
performance level on a given task.
It might be a crucial factor to select the appropriate cognitive level, verbal
or non-verbal, when evaluating the performances of specific neuropsycho-
[12]
logical tests in multiply disabled patients. A study in Fragile X Syndrome
suggests that specific verbal and non-verbal working memory problems can
be detected if the verbal and non-verbal age equivalents, based on Verbal
IQ and Performance IQ results, are used as input for norm tables of verbal
tests and non-verbal tests, respectively. Specific impairments in dorsal stream
[13, 14]
functions, such as object recognition in suboptimal conditions can be
found in children with early brain damage by using the non-verbal mental age
as entry of the present norm tables. The use of chronological age masks these
specific neuropsychological deficits by a profile of weaknesses in several func-
[12, 14]
tions and thereby dramatically increases the number of impairments
[14]
in patients. This suggests that outcomes of dorsal stream function tests,
like motion perception test results obtained in children with congenital brain
damage could be either judged against chronological or non-verbal develop-
mental age. The aim of this study was to contribute to the discussion what age
parameter should be considered as entry of the norm tables when assessing
individual patients in clinical practice.
We examined four aspects of visual motion perception in a group of typically
developing children and children with brain damage: global motion, motion
speed, biological motion, motion-defined form. In this article, we focused on
the relation between age parameters (chronological age and developmental
age, i.e. the median age equivalent based on raw scores of nonverbal intel-
ligence subtests) and motion perception outcomes. We hypothesized that
motion perception scores are closely related to the non-verbal cognitive
level. In typically developing children, both measures are reflected in their
chronological age, suggesting that a clinician would be free to choose between
chronological age and performance age in the construction of norm values.
In children with brain damage, on the other hand, non-verbal cognitive level
and chronological age are dissociated. For the children with brain damage, we
hypothesized that motion perception performance is related to developmental
age rather than to chronological age. Here, we set and evaluated preliminary
norm values and considered the possible impact of the choice between the use
of chronological age or performance age as the entry of the norm table in the
evaluation of the performance of individual patients.
Assessing visual motion perception problems 103
Methods
Participants
The patient group consisted of 49 children (24 boys, 25 girls). The patients
were recruited through rehabilitation centers in the Rotterdam area (Rijn-
dam Rehabilitation Centre and Royal Dutch Visio, n = 19) and the Leuven
University Hospital, Belgium (n = 30). Forty patients had abnormal imaging
results and nine had normal or no imaging results but had indications of brain
damage/dysfunction. The aetiology of brain damage was brain malformations
in three children, hypoxic-ischemic encephalopathy in twenty-three cases (19
periventricular leukomalacia (PVL), 3 intraventricular haemorrhage (IVH),
1 PVL + IVH), perinatal asphyxia in five, intracranial haemorrhage in two, 5
hydrocephalus in one and acquired brain injury in six (4 trauma, 1 meningitis,
1 tumour). Of the nine patients in whom no or normal imaging results were
present, three had a genetic disorder (Velo-Cardio-Facial syndrome; Beckwith
Wiedemann syndrome; 46XY + m), four had neurological signs such as cere-
bral palsy, one had visual problems not explained by ocular abnormalities and
one was dysmature probably due to prenatal drug exposure. Five patients had
ocular abnormalities other than refractive errors or oculomotor dysfunctions.
No patient had ophthalmological abnormalities to such a degree that it would
[15]
interfere with perceiving details of the motion stimuli. At the moment of
motion perception testing, chronological age ranged from 4.11 to 14.58 (M =
7.35, SD = 2.26 years).
The control group consisted of 119 typically developing children (54 boys,
65 girls) with no indication of neurological or visual impairments and normal
or corrected to normal visual acuity. Controls were recruited through primary
schools in the Netherlands (n = 79) and Belgium (n = 40). At the moment of
motion perception testing, their chronological age ranged from 3.50 to 7.86
years (M = 5.47, SD = 1.05 years), which was significantly lower than that of
the control group (U(166) = 1141.5, Z = -6.19, p < .01).
Studies were approved by the Ethics Committees of the Erasmus Medical
Center and the Leuven University Hospital. For all participants informed con-
sent was obtained from their parents or guardians.
Procedures
All Dutch and Belgian controls (n = 119), and the Dutch patients (n = 19)
were tested at the children’s primary schools. The Belgian patient group (n
= 30) was studied at the Leuven University Hospital. In the Dutch groups,
motion perception tasks were presented in a fixed order: biological motion,
104 Chapter 5
dots (starting level 1 dot added, scaling factor 0.075 and 0.150 from second
reversal), and the threshold was the critical number of noise dots added.
The motion speed stimulus consisted of two identical contours of a car (car
length approx. 17 deg) filled with leftwards moving dots (dot density 11 dots/
2
deg , dot size 0.07 deg, lifetime 120 ms). Participants were asked to indicate
the location of the fastest car (presentation time 10 s). A decrease in the
speed difference of the dots in the cars made the task more difficult (starting
speed difference 17.0 deg/s, scaling factor 0.33, 0.25 from fifth reversal) and
the critical speed difference was the score for this task.
Before each task, example stimuli were used to familiarize participants with
task elements and verify that they understood the task.
Developmental age
Because previous studies suggest that non-verbal cognitive ability, and not
[16-20]
verbal cognitive skill, is predictive of perceptual performance we only
studied non-verbal intelligence in addition to visual perception in patients and
in a subset of controls. The data collection of IQ data in the control group was
limited due to time constraints. Although the use of a single intelligence test
is preferable, the broad age range in the patient group and the cognitive con-
sequences of the brain damage made this impossible. In addition, we decided
to use recent intelligence results when available to keep the required effort of
the patients as low as possible.
Non-verbal intelligence data were collected in 60 Dutch controls, using the
Snijders-Oomen non-verbal intelligence test (SON-R 2½ - 7). In the patient
group, data were available for SON-R in 19, Wechsler preschool and primary
scales of intelligence (WPPSI-R) in 24, Wechsler Intelligence Scale for Chil-
dren III (WISC-III) in 5 and Wechsler Intelligence Scale for Children-revised
(WISC-R) in 1 patient. All these tests have normative data for the Dutch
speaking population of Belgium and The Netherlands.
The SON-R differs from the Wechsler tests in that the SON-R can be ad-
ministered without using verbal instructions, which makes the assessment in
children with hearing or language problems possible, and feedback is provided
after each item, which gives the child the possibility to learn. The effect of
these differences on the outcomes is unknown, but because the correlation
[21] [22]
between SON-R IQ and WPSSI-R PIQ is 0.93 and WISC-R PIQ is 0.79,
we considered these tests interchangeable for the developmental age estima-
tion.
The developmental age was defined as the median age equivalent based
on the raw subtest scores of the non-verbal intelligence scale. We used age
Assessing visual motion perception problems 107
Statistical analysis
We used IBM SPSS Statistics version 20, the data of the 60 Dutch controls and 5
all patients and the Mann-Whitney test to study group performances. Because
we assumed that patients performed equally well or worse than controls we
used the one-tailed significance and a p-value of .05.
To study the relation between the outcomes of the motion perception tasks
and the age parameters chronological age and developmental age we calculated
the Spearman correlation and partial correlation. Outcomes of these analysis
in controls were used to decide whether chronological age or developmental
age should be used to set the normal limits. We ordered the performances of
the controls from worst to best and computed the weighted average of the
th th th th th th
5 , 10 , 25 , 50 and 75 percentile. We set the 5 percentile score as the
th
cut-off value for abnormal performance and the 10 percentile score as the
cut-off value for weak performance.
We then calculated the 95%-confidence interval for the found cut-off values
based on 1000 bootstrap samples, with replacement from the original data-
set. In addition we calculated the 95%-confidence interval for the percentage
[23]
excluded participants with the exact binomial method of Clopper-Pearson.
Results
.72, p < .01, df = 59) and absent between chronological age and PIQ (rs =
- .01, ns, df = 59), showing that mean PIQ is similar across age. In eight con-
trols one or two motion perception tasks were not completed due to reduced
compliance. With respect to the biological motion task it was remarkable that
several children mentioned that the phase-scrambled point-light figure looked
like a dancing person when it was introduced.
Table 1. Calculating developmental age in months from non-verbal IQ subtest age equivalents of
the WPPSI-R in 4 different Belgian patients (BE04; BE02; BE11; BE07). * middle two values, values
around the median.
BE04 BE02 BE11 BE07
(Raw test scores)
WPPSI-R subtests Age equivalents in months according manual
Object Assembly (28) 88* (24) 66* (20) 54* (10) 33
Geometric designs (47) 68 (48) 69 (34) 57* (15) 41
Block design (20) 57 (18) 54 (10) 43 (8) 39*
Mazes (19) 75* (17) 67* (8) 42 (9) 41
Picture completion (23) 92 (18) 58 (22) 83 (10) 40*
Animal Pegs (58) 96 (56) 84 (58) 96 (50) 67
Median age equivalent 81 66 56 40
Age IQ test 73.13 73.86 93.96 91.73
Age motion tests 73.13 73.86 96.89 103.72
a
Developmental age 81 66 57.74 45.23
PIQ 102 83 62 -
VIQ 106 83 102 -
a
Developmental age = (Median age equivalent/Age IQ test)*Age motion test.
In the patient group one girl and one boy did not complete any of the motion
perception tasks. The girl complained that she did not see anything moving.
Ten patients completed all four tasks, 24 three, 7 two, and 6 one. Chronologi-
cal age of these remaining 47 patients was 7.32 years (SD = 2.28), mean PIQ
78 (SD = 20, n = 40), and mean developmental age 5.38 years (SD = 1.42).
The correlation between chronological and developmental age was modest (rs
= .41, p < .01), but significantly lower than in the control group (.41 versus
.72, p < .01). The relation between chronological age and PIQ was absent (rs
= - .07, ns).
In Figure 2 the distribution of scores on the motion perception tasks in
patients and controls are plotted. The boxplots and measures for skewness
and kurtosis show that the data of most tasks are not normally distributed,
except for the data of the patient group for the global motion and biological
motion tasks. The distribution for the global motion task in the controls is near-
normal. The non-normal distributions are skewed and sometimes leptokurtic
Assessing visual motion perception problems 109
(clustered about the center and thinner tails, except at the end points where
the tails are thicker than in the normal distribution). The motion coherence
level in patients (Mdn = .45) did not differ significantly from controls (Mdn
= .40; U = 1416.50, z = 1.56, p = .06, effect size r = 0.16). However, the
patients (Mdn = .72) performed significantly worse than the controls (Mdn =
.84) on the motion-defined form task (U = 861.50, z= -1.91, p = .03, effect
size r = -0.19). The performance on the biological motion task did not differ
significantly (Mdnpatients = 8.12, Mdncontrols = 7.87; U = 813.50, z = -0.24,
ns, effect size r = 0.03). Unexpectedly patients performed significantly better
on the motion speed task (Mdnpatients = 4.28 deg/s, Mdncontrols = 5.78; U =
507.50, z = -1.66, p = .05, effect size r = 0.19). The data of the patient group
is more clustered and shows 1 outlier. 5
Figure 2. Motion perception performances in controls and patients. Boxplots: horizontal line is the
median, the box represents the interquartile range (range between 25th and 75th percentile), the
wishers represent the 95%-confidence interval, the circles are data points outside the confidence
interval and the asterisk is an outlier in that group A. Motion coherence task; B. Motion-defined form
task; C. Biological motion; D. Motion speed.
Table 2. Controls: relation between motion perception task outcomes, chronological age and de-
velopmental age, as well as unique contribution of chronological age and developmental age to task
outcomes. * p ≤ .05 ** p ≤ .01
Spearman correlation Spearman partial correlation
Chronological Developmental Chronological Developmental
a b
n age age age age
Global motion 57 - .43 ** - .35 ** - .27 * - .07
Motion-defined form 59 .39 * .40 * .16 .19
Biological motion 60 .31 * .27 * .17 .08
Motion Speed 53 - .34 * - .42 ** - .07 - .27 *
a b
controlled for developmental age; controlled for developmental age
Table 3. Patients: relation between motion perception task outcomes, chronological age and devel-
opmental age, as well as unique contribution of chronological age and developmental age to task
outcomes. * p ≤ .05 ** p ≤ .01
Spearman correlation Spearman partial correlation
Chronological Developmental Chronological Developmental
a b
n age age age age
Global motion 42 - .17 - .42 ** .00 - .39 **
Motion-defined form 38 .01 .32 * - .14 .34 *
Biological motion 28 - .12 .48 ** - .39 * .59 **
Motion Speed 25 - .18 - .33 * - .05 - .29
a b
controlled for developmental age; controlled for developmental age
Assessing visual motion perception problems 111
Normal limits
The results above show that in typically developing children the unique contri-
bution of performance age over chronological age in visual motion perception
performance is limited. Therefore, we had no reasons to deviate from common
practice and calculated the normal limits based on controls’ chronological age.
As a result, we could use data of the entire control group (N = 119), including
the controls without IQ data.
The control groups performed equally on the global motion task (Mdn = .40
vs .37) and the biological motion task (Mdn = 7.87 vs 9.42, effect size r =
0.14). The control group with IQ data (Mdn = .84) performed significantly bet-
ter than the control group without IQ data (Mdn = .77) on the motion-defined
task (U = 2222.50, z = 2.79, p < .01, effect size r = 0.26) and on the motion 5
speed task (Mdn = 5.78 vs. 9.40 deg/s; U = 635.50, z = -2.83, p < .01, effect
size r = 0.30).
In Figure 3 the motion perception scores obtained in the group with and
without IQ information are plotted relative to age. As the chronological age in
the group without IQ data was slightly but significantly lower than in the group
with IQ data (5.29 ± 1.21 years vs. 5.66 ± 0.81 years; t(101.5) = 1.99, p =
.05), there is a slight shift of the groups relative to the X-axis. This explains
the differences in performance between the control groups.
To construct age-specific cut-off criteria, the entire sample was optimally
divided in three age groups with a minimum of 30 participants per group. The
youngest group, group 1, consisted of 19 boys and 12 girls younger than 4.75
years with a mean age of 4.20 years (SD = 0.39; range = 3.50 - 4.67). Group
2 consisted of 17 boys and 26 girls with an age between 4.75 and 5.75 years
with a mean age of 5.26 years (SD = 0.27; range = 4.75 - 5.74). Group 3, the
oldest group, consisted of 18 boys and 27 girls aged 5.75 years and older with
a mean age of 6.56 years (SD = 0.60; range 5.75 - 7.86).
The data of the global motion task was normally distributed in group 1 and
2. Skewness and kurtosis were within normality ranges in group 3, but the
Shapiro-Wilks was significant (p = .05), suggesting a non-normal distribution.
The data of the motion-defined form task was normally distributed for group
1 and 3. The data of the group 2 was skewed and the Shapiro-Wilks was near
significant (p = .06). The data of the motion speed task had a non-normal
distribution in all groups (Shapiro-Wilks ps < .01). In group 1 skewness and
kurtosis were within normality ranges, the data in group 2 was skewed and the
data of group 3 was more skewed, looked more like a lognormal distribution,
but was also leptokurtic. Because of the different shapes of the distributions
we decided not to transform and normalize the data.
112 Chapter 5
Figure 3. Performance of the control group with IQ (n = 60) information and the control group
without IQ information (n = 59) on A. global motion, B. motion-defined form, C. Biological motion,
D. motion speed
For the global motion and motion speed task the 10th and 5th percentile
cut-off values decreased by age. In the youngest group (n1 = 31) the global
motion cut-off coherence levels were 0.78 and 0.80, in the second group (n2
= 39) 0.69 and 0.74, and in the oldest group (n3 = 45) 0.46 and 0.56. 10th
percentile cut-off values for the motion speed differences were 23.80, 20.00
and 12.49 deg/s and 5th percentiles cut-off values were 23.80, 21.53 and
19.87 (n1 = 25; n2 = 34; n3 = 31). For the motion-defined form task the
proportion correct cut-off values increased by age from 0.45 in group 1 (n1
= 31), 0.63 in group 2 (n2 = 43) to 0.74 in group 3 (n3 = 43) for the 10th
th th
percentile and from 0.33, 0.59 to 0.70 for the 5 percentile. The 5 percentile
of the biological motion task coincided with the lowest score obtainable in all
age groups, implying a bottom effect for this task. Therefore, presentation of
cut-off values and clinical evaluation on this task is not useful.
Assessing visual motion perception problems 113
Figure 4. Confidence intervals for cut-off values for percentile 5 (left) and percentile 10 (right).
Filled circle: median score; filled black triangle: cut-off value; grey triangles: confidence limits. The
lines are fitted to illustrate possible trends. A. global motion, B. motion-defined form, C. motion
speed.
age, most notable for the motion speed task, are reflected in our plots: the
increasing variance and skewness in the motion speed task resulted in a wider
confidence interval, although group size changed from 25 to 34 and 31.
The exact binomial method of Clopper-Pearson showed that we might label
th
1% to 17-21% of the population as abnormal when using the 5 percentile
cut-off values of the global motion task and 2-4% to 24-26% as weak when
th
using the 10 percentile cut-off values. The results for the motion-defined
form are comparable. For the motion speed task, we might label 1% to 20-
26% as abnormal and 2-3% to 26-31% as weak when using the cut-off values
th th
for the 5 and 10 percentile.
Discussion
This study shows that a child’s level of non-verbal cognitive ability is indicative
of the level of performance on a visual motion perception task. This non-
verbal cognitive level is not the relative level in comparison to peers, but the
absolute level of ability as reflected in the non-verbal cognitive complexity of
the tasks that the child is able to perform. In typically developing children this
absolute level of non-verbal cognitive ability is directly related to the child’s
chronological age, which is a good proxy for it. In children with early brain
damage, on the other hand, the level of non-verbal ability is often dissociated
[16, 24-27]
from chronological age. Our results show that in that case the non-
verbal cognitive level is predictive of visual motion perception performance.
This is in line with previous studies on object and form perception abilities in
[16, 18, 28]
neuropediatric populations, such as cerebral palsy, hypoxic-ischemic
[16]
encephalopathy in premature infants and in birth asphyxia and spina
[19]
bifida. The high correlations between PIQ and object or form perception
scores reported, ranging from 0.33 to 0.85, imply that a lower perception
score than expected from a child’s chronological age is not as such an indica-
tion of a perceptual disability. This implies that, in general, the scores on visual
motion perception tasks reflect a patient’s global non-verbal cognitive level,
in addition to a possible specific visual motion perception disability. Therefore,
to evaluate perceptual ability in these children it is important to use their
global non-verbal cognitive level, as expressed by the developmental age, as
a baseline. Only in this way, it can be avoided to erroneously interpret non-
verbal cognitive impairment manifested in the motion task performance as a
[16]
motion perception impairment. Stiers, De Cock and Vandenbussche (see
[14] [15]
also Stiers et al. , Stiers & Fazzi ) suggest a simple and clinically feasible
Assessing visual motion perception problems 115
Acknowledgements
We thank the participating children and their parents, the schools (Eduard
van Beinum, Openbare basisschool Charlois, De Bergse Zonnebloem, Visio-
school); Rijndam Revalidatiecentrum, Rijndam Rehabilitation Centre; Royal
Dutch Visio, Centre of expertise for blind and partially sighted people, all
located in Rotterdam, the Netherlands for their cooperation in the data col-
lection.
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Chapter
Chapter 6
6
van der Zee Y., Stiers P., Lagae L., et al. Clinical assessment of
visual motion perception in children with brain damage and the risk
of overdiagnosis. Submitted.
122 Chapter 6
Abstract
Aim
In this study, we examined 1) the presence of weaknesses in various visual
motion perception aspects in children with brain damage; 2) the clinical im-
pact of chronological age and developmental age as reference level when
interpreting motion perception performances.
Method
Performances of 46 children with indications of brain damage (Mage = 7y4m,
SD = 2y4m) on three visual motion perception aspects (global motion, motion
speed, motion-defined form) were evaluated. We used developmental and
chronological age as entry of a preliminary reference table, and compared
the proportions of weak performers with probabilities expected in the general
population.
Results
When using developmental age as reference level, the proportion of weak
performers on at least one of the three tasks was significantly higher than
expected in the general population (19/46, p = .02). In 15/19 patients only
one aspect of motion perception was affected. When using chronological age
as reference level, the proportion of patients that performed weak on at least
one task increased significantly from 19/46 to 24/46 (p = .03).
Interpretation
There is an increased risk of isolated motion perception problems in children
with brain damage, independent of their performance IQ. The use of chrono-
logical age as reference level increases the risk of overdiagnosis significantly.
Introduction
Method
Participants
The patient group consisted of 46 children with indications of brain damage,
brain malformation, or clinical indication of visual perceptual impairment.
They were recruited through rehabilitation centres in the Rotterdam area (Ri-
jndam Rehabilitation Centre and Royal Dutch Visio) and the Leuven University
Hospital, Belgium. The chronological age ranged from 4y1m to 14y7m (M =
7y4m, SD = 2y4m). Performance IQ ranged from 45 to 119 (M =75, SD =
21), developmental age, the extrapolated median age equivalent on nonverbal
[14]
intelligence subtests, ranged from 2y5m to 8y2m (M = 5y4m, SD = 1y5m).
Twenty children had been born prematurely (gestational age <37 weeks). The
aetiology of brain damage was brain malformations in three children, hypoxic-
ischemic encephalopathy in twenty-one cases (18 periventricular leukomala-
cia, 3 intraventricular haemorrhage), perinatal asphyxia in five, intracranial
haemorrhage in one, hydrocephalus in one and acquired brain injury in six (4
trauma, 1 meningitis, 1 tumour). Of the nine patients in whom no or normal
imaging results were present, three had a genetic disorder (Velo-Cardio-Facial
syndrome; Beckwith Wiedemann syndrome; 46XY + m), five had neurological
signs such as cerebral palsy, one had visual problems not explained by ocular
abnormalities and one was dysmature probably due to prenatal drug expo-
sure. Five patients had ocular abnormalities other than refractive errors or
oculomotor dysfunctions, like nystagmus, saccadic dysfunction, convergence
abnormality and horizontal oculomotor apraxia. In twenty-two children, visual
acuity and/or visual field abnormalities were found. Eight had low vision (vi-
sual acuity between 0.1 and 0.3) and could therefore be considered visually
impaired and eight children had a subnormal visual acuity for their age (0.5
- 0.8). In seven children a slow or late response was found in one side of the
visual field, in one child a late response was found in the lower visual field,
two children had a concentric visual field loss, but one side was more affected
then the other and one child had a scotoma in the right visual field. None of
the patients had abnormalities to such a degree that it would interfere with
perceiving details of the motion stimuli.
Assessing visual motion perception problems 125
Procedures
The Dutch patient group (n = 17) was tested at the children’s primary schools.
The Belgian patient group (n = 29) was studied at the Leuven University
Hospital. In the order.
random Dutch group, motion perception tasks were presented in the
order: motion-defined form, global motion and motion speed. In the Belgian
Task administration was done by trained senior psychology students or
group tasks were administered in random order.
Task administration was done by trained senior psychology students or neu-
ropsychologists. Tasks
Participants were
were presented
placed on aof15-inch
in front CRT monitor
the screen attached a 40 cm.
at approximately
laptop. Participants were placed in front of the screen at approximately 40 cm.
Figure
Figure 1. 1. Illustration
Illustration of motion
of motion perception
perception tasks. In thetasks.
real taskIn the real
borders are not
A. global
defined motion
by lines. task motion
A. global with target area
task with onarea
target theon the B.
left; left; B. motion-
square;
defined C.task,
form motion speed:
example dots inC.right
item square; motioncar move
speed: dotsfaster.
in right car move
faster.
Motion Perception
Motion tasks
Perception tasks
All stimuli (see Figure 1 for examples of the stimuli) consisted of white dots
on a black background, with a resolution of 640 x 480 and refresh rate 25
frames/s. In the global motion task and the motion speed task psychophysical
thresholds were estimated by calculating the mean of the values of the last
4 of 8 reversals, using a 2up-1down staircase procedure. In these tasks, a
correct answer was followed by a beep.
126 Chapter 6
* 95%-CI indicates the precision of the percentiles (range of general population that could be ex-
cluded using the cut-off values). For this sample, it was calculated for the nearest percentile above
p10 giving a whole number of participants excluded.
Statistical analysis
The binomial test was used to establish whether the proportion weak per-
formers was significantly higher than the probability in the general population
th
given the use of the 10 percentile cut-off in each task and the number of
tasks evaluated: i.e. higher than .27 (change at no weaknesses is .73) for
three tasks and .10 for a single task.
The McNemar test was used to study the developmental-chronological age
effect. A one-sided alpha ≤ .05 was considered significant.
128 Chapter 6
Results
Figure 2. Patients’ performances in relation to the trendlines for p05, p10 and p50 of the reference
Figure 2. Patients' performances in relation to the trendlines for p motion
group using developmental age as entry for reference table. A. global motion task; B. 05
, p10 speed
and p50
task; C.group
motionusing developmental
defined form task. age as entry for reference table. A. global motion task; B.
speed task; C. motion defined form task.
A
130 Chapter 6
Discussion
preterm and with mild periventricular brain damage scored below 2 standard
deviations from the mean in age-matched controls. However, their average
performance IQ was almost 20 points lower than that of the controls. It is
likely that these incidences, at least in part, also reflect reduced non-verbal
cognitive ability.
The use of developmental age as reference level not only reduced the num-
ber of diagnosed problems in groups and individual children, but it will also
help neuropsychologists to uncover specific problems and weighing the effect
of different neuropsychological factors on the child’s (dis)abilities. Determin-
ing and knowing a child’s relative strengths is very important, especially in
case of training or support.
It should be noted that the reliability of the preliminary reference cut-offs
is still limited. To set normal limits more precisely, larger samples of typically
developing children are needed. Another limitation of our study is that the
heterogeneity of the patient population does not allow to delineate specific
6
aetiological conditions of risk for visual motion perception disability. Also, evi-
dence for the clinical relevance, i.e. the relation between outcomes of these
motion perception tasks and problems in daily life, is still missing. Currently,
clinical relevance is based on publication of a single case study, that of pa-
[16]
tient LM. More extensive research on carefully selected patient samples is
needed. At this moment, motion perception tasks should only be applied as
additional observational tools in children with brain damage that have typical
problems, for example difficulties in traffic participation.
It is not clear why no weaknesses were observed on the motion speed task.
It might be a result of a bias in compliance due to the fixed order of presenta-
tion in the Dutch patient group, with motion speed last: only one patient
completed the motion speed task. To avoid this bias in future studies, tasks
should be administered in random order. Another possible explanation might
be that this was the only task that allows for a low-level comparison of stimu-
lus features, whereas the other tasks all require a higher level of integration
of the moving dots to find the correct answer. Unlike speed discrimination,
motion-defined form and global motion require the child to find or identify an
object from a limited amount of visual information. This relies on the function-
ing of more complex networks, the engagement of attention, search and hy-
pothesis testing operations that are associated with frontal-parietal networks.
[17, 18]
The integrated functioning of posterior visual and anterior executive
areas thrives on long-range connection fibres, which may be affected by early
[19]
brain damage or brain malformation. Additionally, performances on the
motion speed task might be less dependent on the integrity of primary visual
132 Chapter 6
cortex (V1) due to the higher dot speeds used, and might mainly depend on
the direct route from the retina to the superior colliculus and pulvinar to the
[20]
prestriate cortex. The common involvement of V1 in visual acuity, visual
[21] [20]
field and motion processing of the global motion and motion-defined
form task, might also explain why we find significant correlations between
these measures. We suggest, that at least a low-speed task (< 6 deg/s) which
activates V1 before V5, and a high-speed task (> 15 deg/s) which activates
the colliculo-prestriate cortical route, should be developed and studied for
[20]
different motion aspects, in order to study the integrity of different neural
networks and the relation with visual acuity and visual field outcomes.
Acknowledgements
References
1. Jakobson, L., V. Frisk, and A. Downie, Motion-defined form processing in ex-
tremely premature children. Neuropsychologia, 2006. 44(10): p. 1777-1786.
2. Gunn, A., et al., Dorsal and ventral stream sensitivity in normal development and
hemiplegia. Neuroreport, 2002. 13(6): p. 843-847.
3. Guzzetta, A., et al., Motion perception in preterm children: role of prematurity and
brain damage. Neuroreport, 2009.
4. Stiers, P., et al., Mapping multiple visual areas in the human brain with a short
fMRI sequence. Neuroimage, 2006. 29(1): p. 74-89.
5. Braddick, O.J., et al., Brain areas sensitive to coherent visual motion. Perception,
2001. 30(1): p. 61-72.
6. Sunaert, S., et al., Attention to speed of motion, speed discrimination, and task
difficulty: an fMRI study. Neuroimage, 2000. 11(6 Pt 1): p. 612-23.
7. Marcar, V.L., et al., An fMRI study of the cerebral macro network involved in
‘cue invariant’ form perception and how it is influenced by stimulus complexity.
Neuroimage, 2004. 23(3): p. 947-55.
8. Klaver, P., et al., Dorsal stream development in motion and structure-from-motion
6
perception. Neuroimage, 2008. 39(4): p. 1815-23.
9. Bava, S., A.O. Ballantyne, and D.A. Trauner, Disparity of verbal and performance
IQ following early bilateral brain damage. Cognitive and Behavioral Neurology,
2005. 18(3): p. 163-70.
10. van der Zee, Y., et al., Chronological age versus developmental age in evaluating
patients’ performances on motion perception tests. Accepted for publication in
Neuropsychological Trends, 2018.
11. Reiss, J.E., J.E. Hoffman, and B. Landau, Motion processing specialization in Wil-
liams syndrome. Vision Research, 2005. 45(27): p. 3379-3390.
12. Del Viva, M.M., et al., Spatial and motion integration in children with autism.
Vision Research, 2006. 46(8-9): p. 1242-1252.
13. Atkinson, J., et al., Neurobiological models of visuospatial cognition in children
with Williams syndrome: measures of dorsal-stream and frontal function. Devel-
opmental Neuropsychology, 2003. 23(1-2): p. 139-72.
14. Stiers, P., et al., The variety of visual perceptual impairments in pre-school
children with perinatal brain damage. Brain and Development, 2001. 23(5): p.
333-48.
15. MacKay, T.L., et al., Deficits in the processing of local and global motion in very
low birthweight children. Neuropsychologia, 2005. 43(12): p. 1738-48.
16. Zihl, J., D. Von Cramon, and N. Mai, Selective disturbance of movement vision
after bilateral brain damage. Brain, 1983. 106: p. 313-340.
17. Pollmann, S., et al., A fronto-posterior network involved in visual dimension
changes. Journal of Cognitive Neuroscience, 2000. 12(3): p. 480-94.
18. Corbetta, M. and G.L. Shulman, Control of goal-directed and stimulus-driven at-
tention in the brain. Nature Reviews Neuroscience, 2002. 3(3): p. 201-215.
19. Ortibus, E., et al., Integrity of the inferior longitudinal fasciculus and impaired
object recognition in children: a diffusion tensor imaging study. Developmental
Medicine & Child Neurology, 2012. 54(1): p. 38-43.
134 Chapter 6
20. Ffytche, D.H., C.N. Guy, and S. Zeki, The parallel visual motion inputs into areas
V1 and V5 of human cerebral cortex. Brain, 1995. 118 ( Pt 6): p. 1375-94.
21. Duncan, R.O. and G.M. Boynton, Cortical magnification within human primary
visual cortex correlates with acuity thresholds. Neuron, 2003. 38(4): p. 659-71.
Chapter
Chapter 7
7
van der Zee, Y., Stiers, P., & Evenhuis, H. Object recognition and
dorsal stream vulnerabilities in children with early brain damage.
Submitted.
136 Chapter 7
Abstract
Aim
Dorsal stream functions are considered vulnerable in children with early brain
damage. Considering the recognition of objects in suboptimal representations
a dorsal stream dysfunction, we examined whether children with early brain
damage and impaired recognition have either general or selective dorsal
stream dysfunctions.
Method
Performances on motion perception, visual attention and visuoconstruction
were evaluated in patients with (n = 18) and without (n = 11) object recogni-
tion abnormalities. Increased risk of dorsal stream dysfunctions was deter-
mined by the comparison of the proportions of abnormal/weak performers
with the probabilities expected in the general population, given the cut-offs
and number of tasks used.
Results
Compared to patients with normal object recognition, patients with object
recognition problems performed significantly more often weak on motion per-
ception and visual attention (ps = .03) but did not differ on visuoconstructive
skills. Six of the eighteen patients with object recognition problems performed
weak on at least two additional dorsal stream functions, which we considered
a general dorsal stream dysfunction.
Interpretation
Children with object recognition problems are at risk for other dorsal stream
dysfunctions, but dysfunctions seem rather specific than general. Multiple
functions/aspects should be assessed in neuropsychological assessment of
children at risk.
Dorsal stream functioning in at-risk children 137
Introduction
[1]
Studies on visual perception in children with developmental disorders and
[2, 3]
early brain damage suggest that the dorsal stream of the cerebral vi-
sual system is more vulnerable than the ventral stream. The dorsal stream
[4, 5] [6]
is associated with motion perception, visuomotor integration, and
[7]
visual attention. Different brain areas are thought to be crucial for these
functions: V5/MT+ for global motion, motion speed and motion-defined form
[8-10]
perception; the superior temporal sulcus (STS) area for biological motion
[11] [12]
perception and target detection; the temporoparietal junction (TPJ) for
[13] [13]
attention shift, the intraparietal sulcus (IPS) for visuospatial attention
[12]
and response prepartion; the inferior parietal lobule (IPL) for visuomo-
[14] [7]
tor planning, and the superior parietal lobule (SPL) for attentional bias,
[14]
action, visuomotor control. The ventral stream, which projects into the
inferotemporal cortex, is associated with form perception, object recogni-
[1, 6] [1]
tion and face recognition. Although object recognition is primarily
considered a ventral stream function, existing evidence indicates that it is not 7
[15] [15, 16] [16]
a ventral stream function alone: IPS, IPL and SPL play a role in
object recognition in suboptimal representations. Damage in the parietal lobe
is associated with impaired recognition in the following suboptimal representa-
[3, 17] [18]
tions: incomplete drawings, overlapping drawings, objects presented
[18] [18]
from an unconventional view, and drawings degraded by noise.
Studies on dorsal stream functions in children with early brain damage or
developmental disorders indicate that different aspects of object recogni-
[19] [8-10]
tion and motion perception can be selectively impaired. Because in
most studies single functions or aspects were studied, it is unknown how often
multiple dorsal stream functions are affected. One study in prematurely born
children with complications such as periventricular white matter disease and
retinopathy of prematurity, showed that 20-55% of the patients had clinically
[20]
significant impairments in different dorsal stream functions. However, it
was not reported whether individual patients were impaired on multiple tasks,
and object recognition in suboptimal representations was not addressed in this
study.
The aim of the present study was to determine whether other dorsal stream
dysfunctions are commonly present in children with an identified dorsal stream
dysfunction. In this study, the L94 was used to detect children with a dorsal
stream dysfunction in a group of children with (indications of) early brain
damage. The L94 is a valid diagnostic test battery for object recognition in
suboptimal representations. Abnormal performances on the L94 are associated
138 Chapter 7
[21]
with parietal lobe damage. We hypothesized that patients with object rec-
ognition abnormalities perform significantly more often weak on other dorsal
stream aspects, i.e. motion perception, visual attention, and visuoconstructive
skills, than children with normal object recognition. We also examined how
often a general dorsal stream dysfunction was present, i.e. how often at least
2 out of three additional dorsal stream functions were weak.
Methods
Participants
The patient group consisted of 48 children at risk for object recognition prob-
lems, because of brain damage, indications of brain damage and/or reports of
suspicion of visual perceptual impairments in the medical file. Patients were
recruited through rehabilitation centres in the Rotterdam area (Rijndam Reha-
bilitation Centre and Royal Dutch Visio, Centre of Expertise for blind and par-
tially sighted people, n = 19) and through the Laboratory of Neuropsychology
at the University Hospital in Leuven, Belgium (n = 29). Their chronological age
ranged from 4y1m to 14y7m (M = 7y3m, SD = 2y4m). Their developmental
[22]
age, the median age equivalent of nonverbal intelligence subtests, ranged
from 2y5m to 7y8m (M = 5y3m, SD = 1y5m). Patient characteristics are
presented in Table 1. Eight patients had low vision, a visual acuity between
0.1 and 0.3, but all patients should be able to perceive the detailed stimuli.
Studies were approved by the Ethics Committees of the Erasmus Medical
Centre MEC-2006-056) and the Catholic University of Leuven. Informed con-
sent was obtained for all participants through their parents or guardians.
Procedures
The following dorsal stream functions were studied in arbitrary order: object
recognition in suboptimal representations; motion perception; visual atten-
tion; visuoconstructive abilities.
To assess object recognition in suboptimal representations we used five
[19]
computerised subtasks of the L94 that require recognition of line draw-
ings of everyday objects: visual matching (VISM); drawings occluded by
noise (NOISE); overlapping line drawings (OVERL); unconventional object
views (VIEW); De Vos (DE VOS). In the De Vos task, objects are embedded
in context or they are partially drawn, only contours are presented, a typical
Dorsal stream functioning in at-risk children 141
Analysis
Participants were included in the analysis if at least three out of five L94 tasks
had been completed. Because the probability of finding one or more abnor-
malities increases with the number of task evaluated, from .05 for one task to
.23 (change at no abnormalities is .77) for five tasks, we checked whether this
patient group was indeed a group at risk for dorsal stream dysfunction, i.e.
we tested with the binomial test whether the proportion abnormal perform-
ers was significantly higher than the probability in the general population. To
control for the variation in number of tasks completed, we calculated the mean
142 Chapter 7
Results
Figure 1. Expected
Figure 1. and observed
Expected and observed proportion
proportion abnormal
abnormal performances
performances on
on the
the L94
L94
7
Dorsal stream
Dorsal stream functioning
functioning in patients
in patients with and without with
object and without
recognition object
problems
recognition problems
Out of remaining 46 patients, 44 completed at least one motion perception task, 41 at
Out
least of
oneremaining 46 patients,
visuoconstructive task, and44
33 completed at least
the visual attention oneThis
task. motion perception
resulted in 29
task, 41inat
patients leastboth
whom oneatvisuoconstructive
least three L94 taskstask, and
and all 33 other
three the visual
dorsal attention
stream task.
This resulted
functions could in
be 29 patients
evaluated. Inin whom
Figure both
2 we at least
report three L94
the observed tasks and
proportions all three
of weak
other dorsal
functions in thestream functions
total patient group, could be with
the group evaluated. In Figure
normal L94 2 (n
outcomes we=report
11) andthe
observed
the group with abnormal L94 outcomes (n = 18). The median number of evaluated group
proportions of weak functions in the total patient group, the tasks
with normal
of other dorsal L94 outcomes
stream functions (n
was=seven
11) out
andofthe group
totally eightwith abnormal
(sub)tasks (rangeL94 out-
5-8).
comes (n we
Therefore, = 18). The that
expected median number of
the proportion of evaluated tasks
patients with of other
at least dorsal
two weak stream
functions,
functions
independentwas seven
of L94 out of
outcomes wastotally eight
.12. The (sub)tasks
proportion (range
of patients with 5-8).
at leastTherefore,
2
we expected
additional weakthat the proportion
functions of patients
was significantly with
higher than at least(ptwo
expected weak
= .04), functions,
as a result of
independent of L94
the relatively high outcomes
proportion was .12.
of patients withThe proportion
exactly of patients
3 additional with at
weak functions least
in the
2 additional
patient weak
group with functions
L94 was (p
abnormalities significantly higher than
< .01). The observed expected
proportions (pleast
for at = .04),
1
as a result of the relatively high proportion of patients with exactly 3 additional
weak function differed significantly between the patient groups (3/11 vs 13/18; p < .02),
weak functions
whereas in the
the observed patient group
proportions with
for 1 and L94 abnormalities
2 additional (p <
weak functions did.01). The ob-
not differ
served proportions
significantly for at(p
between groups least 1 weak
= .15) function
as result differed
of the small significantly
sample sizes. Thesebetween
results
the patient
indicate groups with
that patients (3/11 vs 13/18;
abnormal objectprecognition
< .02), whereas the representations
in suboptimal observed propor-
tions
have afor 1 and 2 additional
significantly weak
increased risk of a functions did stream
general dorsal not differ significantly between
dysfunction.
groups (p = .15) as result of the small sample sizes. These results indicate
that patients with abnormal object recognition in suboptimal representations
have a significantly increased risk of a general dorsal stream dysfunction.
144 Chapter 7 Assessing visual motion perception problems| 131
Figure 2. Expected and observed proportion weak dorsal functions in addition to L94 outcomes
Table 2. Age parameters, proportion of weak performers per function and tasks, and task outcomes
for patient with normal and abnormal performances on L94.
Patients with 3 additional function evaluations
a
Normal L94 ≥ 1 abnormal L94 task p-value
n = 11 n = 18
Median age
Chronological 6;2 6;2 ns
(range) (4;1 – 8;7) (4;1 – 10;2)
Performance 5;6 4;8 ns
(range) (3;1 – 7;8) (2;5 – 6;8)
Motion perception
# weak 1/11 9/18 .03
Global motion task
# weak 0/10 7/16 .02
median coherence level .42 .53 .04
(range) (0.32-0.58) (0.12-0.83)
Motion speed task
# weak 0/9 0/5 ns
median speed difference deg/s 4.83 4.28 ns
(range) (1.70 - 9.66) (1.27 – 23.24)
Motion-defined form task 7
# weak 1/10 5/16 ns
median proportion correct .92 .71 < .01
(range) (0.73 -1.00) (0.00 – 0.97)
Visual attention
# weak 1/11 9/18 .03
Search task 4 distracters
# weak 1/11 7/18 ns
median search time sec 0.73 1.21 .01
(range) (0.00 -1.97) (0.56 – 3.45)
Search task 9 distracters
# weak 0/11 3/18 ns
median search time sec 1.13 1.74 < .01
(range) (0.72 - 1.71) (0.71 – 6.72)
Search task 19 distracters
# weak 0/11 3/18 ns
median search time sec 2.11 3.90 < .01
(range) (0.99 - 3.46) (1.17 - 11.55)
mistakes
# weak 0/11 9/18 < .01
median number 0.00 1.00 < .01
(range) (0.00 - 0.00) (0.00 -11.00)
reaction time task
# weak 0/11 1/18 ns
median response time 1.32 1.49 ns
(range) (0.90 - 2.55) (0.94 - 2.83)
146 Chapter 7
Table 2. Age parameters, proportion of weak performers per function and tasks, and task outcomes
for patient with normal and abnormal performances on L94. (continued)
Patients with 3 additional function evaluations
a
Normal L94 ≥ 1 abnormal L94 task p-value
n = 11 n = 18
Visuoconstructive skills
# weak 2/11 3/18 ns
VMI
# weak 0/6 2/16 ns
median standard score 96.50 92.00 ns
(range) (83 - 106) (73 - 142)
Mosaics (SON-R)
# weak 2/11 2/18
median standard score 10.00 10.50 ns
(range) (3 -12) (5– 15)
a
The significance of differences in median scores were tested with Mann-Whitney test and the sig-
nificance of differences in proportions were tested with the Fisher’s Exact Test (2x2-table, one-sided
significance)
Discussion
In this study, we first demonstrated that children with early brain damage are
at risk for dorsal stream problems, such as problems with object recognition in
[21]
suboptimal representations, by comparing their performances on the L94
with published norm values. While controlling for their developmental age, 29
of 46 children with early brain damage performed significantly abnormal on
one or multiple object recognition subtasks. This was significantly higher than
th
expected in the general population, given the use of 5 percentile cut-off val-
ues and number of tasks evaluated. We then studied whether general dorsal
stream problems were common in children with impaired object recognition
and compared their performances to that of children with early brain damage
with unimpaired object recognition. We defined a general dorsal stream dys-
th
function as a weak performance (score below 10 percentile) on at least two
additional dorsal stream functions, such as motion perception, visual atten-
tion, visuocontstructive skills. The results showed that in 6 of 18 patients with
impaired object recognition a general dorsal stream dysfunction was present,
another 7 patients performed weakly on one additional dorsal stream function.
Dorsal stream problems were uncommon in patients without object recogni-
tion problems: they were only found in 3 of 11 patients with unimpaired object
recognition. Therefore, the risk of a general dorsal stream dysfunction can be
considered increased in children with object recognition problems, but dorsal
Dorsal stream functioning in at-risk children 147
stream dysfunctions are rather specific than general. Motion perception and
visual attention, but not visuoconstructive skills, were specifically affected.
Patients with object recognition problems performed worse on the global
motion and motion-defined form task and were significantly slower on the
visual search tasks. They also made more mistakes, which makes a speed-
accuracy trade-off less likely. The available data are insufficient to study causal
or interactional relationships between functions. One possibility is that weak
visual attention leads to weak motion and object perception scores, but per-
formances on the assessed tasks could also be weak as a result of difficulties
in object discrimination, impulse control and cognitive flexibility. Therefore, to
test hierarchical models, not only a larger sample size but also assessment of
additional indicators is required.
The presence of object recognition and motion perception problems in com-
bination with the normal visuoconstructive performances on the Beery VMI
support the more fundamental idea that developmental age estimations based
on PIQ subtests can be used to control for effects of motor impairments in
[24]
addition to intellectual impairments. Because the Beery VMI can provide 7
age equivalents, it might be suggested that the outcome of the Beery VMI
could be used to estimate developmental age and control for motor impair-
ments by using these age equivalents as entry of the norm tables. Although
[24]
performance IQ and the outcome of the Beery VMI are significantly related,
we consider the developmental age estimation based on PIQ subtests more
reliable, because the estimation is based on multiple subtest results instead of
a single test outcome. In current study, we found two abnormal performers on
the Beery VMI. The use of the age equivalents of the Beery VMI would make
this impossible.
Further, a more detailed analysis of inconclusive items, i.e. items that were
not named correctly in the control conditions of the L94 and the motion-defined
form task and were excluded from the calculation of perception scores, might
help explain performance patterns in children at risk. Inconclusive items can
indicate differences in experience or object knowledge, but also the pres-
ence of other problems such as problems in language development, naming,
especially in relation to words (items) with lower word frequencies, memory
and attention, or a combination of these problems. Differences in the number
of inconclusive items between a group with unimpaired and impaired object
recognition could provide indications for the reason why abnormal performers
were unable to name or describe objects in the control items.
We conclude that in children with early brain damage, dorsal stream functions
and their aspects seem specifically and not generally affected, and that more
148 Chapter 7
Acknowledgement
References
1. Atkinson, J., et al., Neurobiological models of visuospatial cognition in children
with Williams syndrome: measures of dorsal-stream and frontal function. Devel-
opmental Neuropsychology, 2003. 23(1-2): p. 139-72.
2. Gunn, A., et al., Dorsal and ventral stream sensitivity in normal development and
hemiplegia. Neuroreport, 2002. 13(6): p. 843-847.
3. Fazzi, E., et al., Visual-perceptual impairment in children with periventricular
leukomalacia. Brain Dev, 2004. 26(8): p. 506-12.
4. Braddick, O.J., et al., Brain areas sensitive to coherent visual motion. Perception,
2001. 30(1): p. 61-72.
5. Stiers, P., et al., Mapping multiple visual areas in the human brain with a short
fMRI sequence. Neuroimage, 2006. 29(1): p. 74-89.
6. James, T.W., et al., Ventral occipital lesions impair object recognition but not
object-directed grasping: an fMRI study. Brain, 2003. 126(Pt 11): p. 2463-75.
7. Pollmann, S., et al., Separating distractor rejection and target detection in poste-
rior parietal cortex--an event-related fMRI study of visual marking. Neuroimage,
2003. 18(2): p. 310-23.
8. Ho, C.S., et al., Deficient motion perception in the fellow eye of amblyopic chil-
dren. Vision Research, 2005. 45(12): p. 1615-1627.
9. Reiss, J.E., J.E. Hoffman, and B. Landau, Motion processing specialization in Wil- 7
liams syndrome. Vision Research, 2005. 45(27): p. 3379-3390.
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Chapter
Chapter 7:
7: Appendix
Appendix 1
1
General procedure
All controls were tested at the children’s primary schools. Task administration
was done by trained senior psychology students or neuropsychologists.
Visual Tasks
search task | 139
at the department
Theof Psychologic
computerised and
visual Pedagogic
search Sciences
tasks, developed of Leuven
by master Catholic
thesis students at the
1 department of Psychologic and Pedagogic
(size Sciences of Leuven at
Catholic University, 1
University, consisted of greyscale pictures 5 x 5 degrees 40 cm dis-
tance) on a greyconsisted of greyscale pictures (size 5 x 5 degrees at 40 cm distance) on a grey
background (area size approximately 37x29 degrees, see
background (area size approximately 37x29 degrees, see example in Figure 1).
example in Figure 1).
7A1
Figure
Figure 1. 1. Example
Example of visual
of the the visual search
search tasknine
task with with nine
distracters and 1 target (bike).
distracters and 1 target (bike).
Before testing was started, all pictures were presented on the screen to familiarise the
Before testing participants
was started, allpictures.
with the picturesThe were presented
participants ontothe
were asked screen
name to
the individual
Testing was started with a simple reaction-time task with five trials. In
the reaction-time task only the central picture and the target picture were
presented. Because the location of the target stimulus would pop-out to the
participants, the reaction time was considered identical to the motor response
time. The motor response time not only included the time needed by the
participants to point out the target stimulus, but also the time needed by the
administrator to press the spacebar.
In the next stage, three visual search tasks were presented with four, nine
and nineteen distracters. Each task consisted of 10 trials. If needed, the par-
ticipant was encouraged to keep looking. To control for effects of fatigue and
task experience, testing was ended with the above reaction time task.
All reaction times were saved and the administrator noted all false alarms
(mistakes: child pointed out a wrong picture). Reaction times for false alarms
were excluded. Median reaction times were calculated for both reaction time
tasks and for each visual search task. Because the presence of distracters in
the search tasks made pop-out less likely, a serial search process (scanning
individual pictures) was assumed to be needed to detect the targets. In a
serial search process, the reaction time is the sum of the motor response
time and the visual search time. Visual search time was our primary outcome
measure, so median reaction times of the reaction time tasks were distracted
from median reaction times of the search tasks.
th
10 percentile cut-offs for the visual search tasks
The control group consisted of 60 typically developing children (25 boys, 35
girls) without any signs of neurological or visual impairment and with a normal
visual acuity. They were recruited through primary schools in Rotterdam, The
Netherlands. Their chronological age ranged from 4y3m to 7y4m (M = 5y7m
SD = 9m). We divided the group in three age groups, equal to those for the
motion perception tasks. Cut-off values can be found in Table 1.
th
Table 1. 10 percentile scores for visual search outcomes in different age groups.
5 items 10 items 20 items Reaction task
Search time Search time Search time Response Total number
n (sec) (sec) (sec) time (sec) of errors
4y3m -4y7m 7 1.38 2.75 5.91 2.54 2
4y9m -5y8m 23 1.23 2.20 5.47 2.03 1
5y10m - 7y4m 26 1.09 2.66 4.16 1.70 1
Appendix 1: Visual search task 155
References
1. Ledeganck, Luyten M & Vandebussche E. Visueel zoekgedrag bij kinderen met
cerebrale of oculaire visuele inperking: een empirisch onderzoek (Visual search of
children with cerebral or ocular visual impairment: an empyrical study). Catholic
University Leuven, Belgium, Dept. Psychologic and Pedagogic Sciences, 2002.
7A1
Chapter
Chapter 8
8
Pel, J. J. M., van der Zee, Y. J., Boot, F. H., Evenhuis, H. M., &
van der Steen, J. (2013). Remote eye tracking assesses age
dependence processing of coherent motion in typically-developing
children. Journal of Medical Engineering & Technology, 37(2), 109-
115. doi:doi:10.3109/03091902.2012.752043
158 Chapter 8
Abstract
The aim of this study was to quantify processing of different types of coher-
ent motion in terms of ocular motor response times in a group of normally
developing children (age 0-12+ years old) using remote eye tracking. Motion
coherence was applied in three different types of Random Dot Kinematograms
(RDKs): vertical (RDK1) and diagonal (RDK2) motion and expansion (RDK3).
Orienting eye movements were quantified using the Reaction Time to the
first Fixation (RTF). The children were divided into two groups: the ‘young-
est group’ between 0-3+ years and the ‘oldest group’ between 4-12+ years
old. The results showed that RTF was significantly prolonged in the ‘youngest
group’ compared to the ‘oldest group’ for each RDK. In the ‘oldest group’, RTF
was significantly affected by the type of RDK shown. The presented results
suggest that based on ocular motor responses age dependence of processing
different types of coherent motion may be revealed.
Introduction
like expansion. In so-called motion-defined form stimuli, these edges are used
[10]
to make different forms visible. However, it is still unknown to what extent
these edge effects contribute to coherent motion detection. Finally, most RDK
tasks require subjects to understand the specific test instructions and to be
able to give verbal or motor responses. In children under the age of 3-4 years
or children with intellectual disabilities, these tasks cannot be performed ad-
equately. Moreover, the outcome measures depend on the skills of an observer
who assesses orienting responses as a measure for correct motion detection.
To overcome (part of) these problems, we developed a method to quantify
visual orienting responses to RDKs in children using remote eye tracking tech-
[11]
nology. Visual stimuli are presented on an eye tracker monitor. The stimuli
that are shown test basic eye movements (saccades and pursuit), lower order
visual functions (visual acuity and contrast) and higher order visual functions
(form and motion coherence and competitive dots and non-competitive dots).
Upon presentation, orienting behaviour in response to these stimuli is mea-
sured. This approach requires no specific verbal instructions prior to the test or
active cooperation in terms of pointing or pressing a button. In addition, it allows
objective quantification of orienting responses in terms of reaction time and fixa-
[11]
tion areas. The first aim of this study was to compare processing of coherent
motion in terms of reaction times to three different types of RDKs in children
between 0-13 years of age: coherent motion in vertical (RDK1) and diagonal
(RDK2) motion and expansion (RDK3). Our second aim was to investigate if the
presence of motion edges in RDK1 and RDK2 affected orienting behaviour.
Study population
We approached 430 healthy children between 0-13 years old in the region
Rijnmond, Rotterdam, The Netherlands. The children aged 0 till 4 years (0-
3+), the so-called ‘youngest group’ attended a regular day-care centre and
the children aged 4 till 13 (4-12+) years, the so-called ‘oldest group’ attended
a regular primary school. Parents were informed about the study by letter
and 188 (~44%) written consents were received. Children had normal or
corrected-to-normal vision. We included for this study 104 females, 6.2 (SD =
3.5) years and 84 males, 5.7 (SD = 3.6) years. The experimental procedures
were approved by the Medical Ethical Committee of Erasmus University Medi-
cal Centre, Rotterdam, The Netherlands (METC-2006-055). The study adhered
to the Declaration of Helsinki for research involving human subjects.
Motion perception and eye tracking 161
Table 1. An overview of the main characteristics of the three types of RDKs shown to healthy sub-
jects of 0-12+ years old; see also Figure 1 for a schematic illustration of each RDK.
Coherent Motion
Dot RDK1 RDK2 RDK3
direction vertical diagonal Expansion
velocity (degree/s) 11.8 11.8 11.8
size (degree) 0.25 0.25 0.25
2
density (dots/degree ) 2.6 1.3 2.6
Results
Figure 2. The top panel illustrates superimposed the orienting gaze to the two target areas (one
on the left side and one on the right side) of RDK1. After detection of the vertical coherent motion,
the subject made an eye movement into the target area. The bottom panel illustrates
superimposed the orienting gaze starting at the onset of presentation of the four types of RDK2.
Figure 3 shows for RDK3 the distance between the gaze point and the mid-
After detection of the coherent diagonal motion, three of the eye movements of this subject
resulted in transient edge fixation, while one time, a saccade was made into the target area (the
top right monitor corner).
point of expansion and the preset eight degree borderline (the dashed line).
Figure 3 shows for RDK3 the distance between the gaze point and the mid-point of
From the time values at which gaze crossed the 8 degrees border, the Reaction
expansion and the preset eight degree borderline (the dashed line). From the time values
Time to Fixation was calculated. Note that the duration of presentation is 4 s.
at which gaze crossed the 8 degrees border, the Reaction Time to Fixation was
calculated. Note that the duration of presentation is 4s. We plotted the first 2.0s for
We plotted the first 2.0 s for illustration purpose only.
illustration purpose only.
Figure 3. The top panel shows the visual angles between gaze and centre of the target area
against time of 4 coherent expansion motion stimuli presented in RDK3. The bottom panel shows
the cumulative plot of the time values that gaze crossed an 8 degrees border (dashed line) of the
target area. An exponential curve with time constant tau was fitted to this cumulative plot to
old. The fastest reaction times with small variability were found in children
quantify the Reaction Times to Fixation (RTF).
rate in assessing RTF-values in the ‘youngest group’ was highest when using
variability were found in children between 8-12+ years.
RDK1 and RDK3 (vertical and expansion motion) and in the ‘oldest group’ this
rate was almost equally high for all three RDK’s. The Kolmogorov-Smirnov test
showed normal distribution for the RTF values per RDK in the ‘oldest group’. In
addition, only 9 children in the ‘youngest group’ delivered an RTF value for all
RDK’s, whereas this figure was 92 in the children of the ‘oldest group’. Based
on the Mann-Whitney U-test, RTF values were significantly prolonged in the
‘youngest group’ compared to the ‘oldest group’ for each RDK. For the ‘oldest
group’, the Mauchly’s test, as part of the one-way repeated-measures ANOVA,
2
indicated that the assumption of sphericity was not violated, Х (2) = 2.46, p
= .293 (epsilon=.64). The results showed that RTF was significantly affected
by the type of RDK shown, F(2,182) = 14.66, p < .001. Pairwise comparison
within subjects revealed significant differences between RDK1-RDK2 (mean
difference -80 ms (SD 15 ms); p < .001) and between RDK1-RDK3 (mean
difference -70 ms (SD 15 ms), p < 0.001). Finally, we found that 7% of
all subjects fixated edges of motion discontinuities in RDK1. In RDK2 this
percentage was increased to 64%.
166 Chapter 8
150 | Chapter 8
Figure 4. In the top, middle and bottom panel, RTF-values of the control group to respectively
RDK1, RDK2 and RDK3 are plotted against age. In each panel, an age-related power line was fitted
to the data (dashed lines).
Table 2. An overview of the objectively assessed orienting responses to three types of coherent
In Tabletasks
motion 2, an results
over-view is presented
presented of the
in two orienting responses
subgroups: to the0-3+
children aged threeyears
RDKs.(n
The
= 78) and children
aged
results4-12+ years old
are presented in (n
two= subgroups:
110). children between 0-3+ years old (n = 78) and
children between 4-12+ years old (n = 110). The success rate inCoherent
assessingmotion values
RTF-values in
the
Age‘youngest
group group’ was highest when using RDK1 and
Parameter RDK3 (vertical and
RDK1 expansion
RDK2 RDK3
motion) and in theSuccesses
0-3+ years ‘oldest group’
% this rate was almost equally
72 high for all three
53 RDK’s. 81
(number)
The Kolmogorov-Smirnov (56/78)
test showed normal distribution (28/53)
for the RTF values per RDK in (34/42)
Discussion
The aim of the present study was to quantify the processing of motion of
three different RDKs in normally developing children by means of orient-
ing responses. In the ‘oldest group’ the RDKs with vertical coherent motion
induced significantly faster ocular motor responses, up to 70 ms, than the
RDKs with diagonal and expansion motion. One explanation might be that the
diagonal motion stimulus contained only half the number of dots displayed
on the monitor making this stimulus less pronounced compared to the coher-
ent vertical and even the expansion motion. Differences in RTF-values might
also relate to differences in target areas used, since each target area was
different in size and screen location. We tested the influence of target area
size on RTF by increasing and decreasing each area by 25%. We found that
the RTF-values differed on average not more than 30 ms (i.e. a maximum of
less than two sample values given a sample frequency of 50 Hz), indicating
that area size only partially could explain the difference found in RTF-values.
Previously, it was shown that cells in hV5+, located in the inferior temporal
[12-16]
sulcus (ITS), are highly sensitive to directional motion. Processing of
optic flow stimuli like rotation or expansion, predominantly activate cells in
MST.
[17-21]
The presented results suggest that, based on the reaction times 8
to fixation, age dependence exists in processing different types of coherent
motion.
Performance of motion processing is mostly based on psychophysical thresh-
old methods or visual event-related potentials (VERPs). Based on thresholds,
it was found in healthy children aged 4-11+ that motion processing reached
[22]
adult levels at the age of 10-11+ years. Based on VERPs, processing of
expansion motion showed a similar time course, i.e. reaching of adult levels at
[23]
the age of 8-10+ years. The present data not only support these previous
findings, but in addition show quantitative differences in processing different
types of coherent motion. As stated, orienting eye and/or head responses are
reflexively induced towards visual stimuli when its information is processed by
the brain. At this level of processing visual information, processing of (visual)
perception to name the shape of the form or to indicate the direction of a mo-
tion, like in psychophysical threshold methods, might not even be completed
yet. In a future study, it would be interesting to test the RTF-values as a
function of decreasing coherent threshold levels. It might be that timelines of
maturation become different when levels of coherent motion decrease.
In the present study, we remotely assessed gaze while the RDKs were pre-
sented on the monitor of the eye tracker. Gaze responses can be analysed
168 Chapter 8
a case control experiment. The children that have our special attention include
(very) preterm born children with a high risk of having visual processing dys-
functions and children diagnosed with a loss of visual function without damage
to the ocular structures. The latter group is diagnosed with cerebral visual
impairment (CVI), a very broad diagnosis of exclusion and based on ana-
[28]
tomical landmarks. With the current eye tracker method, the wide range
of visual impairments that might occur in these children may be quantified in
terms of functional deficits. Testing the effectiveness of processing different
types of e.g. contrasts, colours and form and motion coherences enables the
construction of a unique visual profile per child. Such profile could support
specific rehabilitation or visual stimulation programs in children with CVI.
Conclusions
Acknowledgement
The authors would like to thank the children and their parents for their coop-
eration.
Declaration of Interest
This research was supported by a grant from the Novum Foundation; a non-
profit organisation providing financial support to (research) projects that
improve the quality of life of individuals with a visual impairment (www.
stichtingnovum.org).
170 Chapter 8
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ments in the newborn infant. Child Development 1979;50:442-8.
9. Wattam-Bell J. The development of visual motion processing. In: Vital-Durand F,
Atkinson J, Braddick OJ, editors. Infant Vision. Oxford: Oxford University Press;
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10. Mason AJ, Braddick OJ, Wattam-Bell J. Motion coherence threshold in infants
– different tasks identify at least two distinct motion systems. Vision Research
2003;43:1149-57.
11. Johnson SP, Mason U. Perception of kinetic illusory contours by two-month-old
infants. Child Development 2002;73:22-34.
12. Pel JJ, Manders JC, van der Steen J. Assessment of visual orienting behaviour in
young children using remote eye tracking: methodology and reliability. J Neurosci
Methods 2010;189:252-6.
13. Huk AC, Ress D, Heeger DJ. Neuronal basis of the motion aftereffect reconsidered.
Neuron 2001;32:161-72.
14. Rees G, Friston K, Koch C. A direct quantitative relationship between the functional
properties of human and macaque V5. Nature Neuroscience 2000;3:716-23.
15. Stiers P, Peeters R, Lagae L, van Hecke P, Sunaert S. Mapping multiple visual
areas in the human brain with a short fMRI sequence. Neuroimage 2006;29:74-
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16. Tootell RB, Reppas JB, Dale AM, Look RB, Sereno MI, Malach R, Brady TJ, Rosen
BR. Visual motion aftereffect in human cortical area MT revealed by functional
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18. Duffy CJ, Wurtz RH. Sensitivity of MST neurons to optic flow stimuli. I. A con-
tinuum of response selectivity to large-field stimuli. Journal of Neurophysiology
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Motion perception and eye tracking 171
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20. Dukelow SP, DeSouza JF, Culham JC, van den Berg AV, Menon RS, T. Vilis T.
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Chapter
Chapter 9
9
van der Zee, Y., Kooiker, M., Talamante Ojeda, M., & Pel J. Gestalt
perception in children with visual impairments: item-specific
performance and looking behavior. Accepted for publication in
Developmental Neuropsychology
174 Chapter 9
Abstract
Introduction
of 5 years, children born premature had lower scores than full-term controls
[7]
on multiple scales, including the simultaneous processing scale. Exclusion
of participants with cerebral palsy (9%), an indication of brain damage, visual
impairments (1% of the population had low vision, a visual acuity <3/10) and
[7]
hearing impairment (<1%) had no influence on the results. These data
suggested that prematurity combined with brain damage did not explain dif-
ferences in performances. Yet, the number of children with impairments was
too small to draw definite conclusions.
As stated, perceptual grouping of simple visual elements (e.g., lines and
arcs) into simple forms and shapes helps to create meaningful representations
of the world. In this process, visual attention plays a very important role. The
frontoparietal network is essential for both bottom-up attention (externally
driven and involving stimuli that are salient because of their inherent proper-
ties relative to the background) and top-down attention (internally driven on
[8]
prior knowledge, willful plans and current goals). Based on event-related
potential patterns, it was shown that visual objects organized according to
Gestalt principles were prioritized over competing non-Gestalt stimuli in
[9]
a bottom-up and automatic fashion. However, these electrophysiological
responses (~150 ms after stimulus onset) only relate to the first steps of
perceptual grouping of simple visual elements, and are not directly as-
sociated with the process of perceptual grouping that results in perception.
Alternatively, visual attention can be quantified from infancy onwards using
visually-guided eye movement responses. Differences in interactions between
eye movement responses and salience in target areas have been found in
children at risk of cerebral and ocular visual impairments compared to typi-
[10]
cally developing children. Specifically, in children at risk of cerebral visual
impairments (CVI), higher reaction times to large and high contrast stimuli
[11]
were found in combination with poorer fixation stability. These children
might have problems with bottom-up regulated visual attention orienting, not
only in visually-guided response tasks but also in visual recognition tasks, like
Gestalt Closure.
The aim of the present study was to investigate the role of visual attention
orienting in the Kaufman Gestalt closure task in children with cerebral and
ocular visual impairments. Digitized Gestalt items were shown one-by-one
on a monitor with an integrated eye tracker. Each participant was asked to
name the complete image that each item represented. For analysis purposes,
we grouped the items in animate (i.e. humans and animals) and inanimate
objects (i.e. everything else). For each item, eye movement responses were
collected to calculate the number of gaze shifts and fixation durations. We
Gestalt perception and eye tracking 177
Methods
Participants
For this study, a database was used that consisted of 122 clients of a rehabili-
tation centre for visually impaired and blind people. The experimental proce-
dures were approved by the local Medical Ethical Committee (MEC 2012-097)
and adhered to the tenets of the declaration of Helsinki (2013). The parents of
all children gave written informed consent. Of the total cohort of 122 patients,
72 patients underwent the Gestalt Closure test. The remaining 51 patients had
either a developmental level below 3 years old, or the task was not performed
due to a time limitation. The chronological age of the selected patients (42
male, 30 female) ranged from 4y6m to 13y8m (M = 9y8m, SD = 2y5m). Four
patients had syndromes: one CHARGE-syndrome, one Down syndrome, one
Noonan syndrome, one Sotos syndrome. Forty-four (60%) had nystagmus as
main diagnosis or as a symptom of another diagnosis, like albinism. Based
on the information in the medical records about ocular abnormalities, brain
9
damage, presence of paresis and visual diagnosis, the children were divided
in three different groups: ocular visual impairments (OVI), ocular and cerebral
visual impairment (OCVI) or cerebral visual impairments (CVI).
legally blind (visual acuity ≤0.1). Of the remaining seven patients six had a
subnormal visual acuity (< 0.8) and one had a normal visual acuity (≥ 0.8).
Behavioural problems were mentioned in nine patients: 3 had no diagnosis, one
had an autism spectrum disorder (ASD), two had attention deficit hyperactiv-
ity disorder (ADHD), one had ASD and ADHD, one had ADHD and oppositional
defiant disorder (ODD), one had an attachment disorder. In eleven patients
no estimation of the cognitive level was present. Of the remaining patients
three had a mild cognitive impairment (50 < TIQ < 70), four functioned at a
borderline cognitive level (70 < TIQ < 89), six at a below average level (70 <
TIQ < 89) and seven at an average level (TIQ ≥ 90). The chronological age of
the OVI group ranged from 4y8m to 13y7m (M = 9y9m, SD = 2y5m).
Table 1. Aetiology of brain damage and estimated cognitive levels in children in the groups OCVI (n
= 14) and CVI (n = 20).
OCVI CVI
n (%) n (%)
Aetiology of brain damage
No imaging data 6 (43) 5 (24)
Perinatal 8 (57) 12 (57)
Asphyxia 3 (21) 3 (15)
a
Hypoxic-ischemic encephalopathy (HIE) 2 (14) 6 (30)
Dysgenesis/agenesis 2 (14) 2 (10)
Postnatal brain damage
b
Acquired brain damage - 4 (20)
Peri- and/or postnatal
Hydrocephalus - 1 (5)
Mild atrophy 1 (7) -
Estimated cognitive level
Average (TIQ ≥ 90) 4 (29) 4 (20)
Below average (70 < TIQ < 89) 2 (14) 6 (30)
Borderline (70 < TIQ < 89) 4 (29) 3 (15)
Mild impairment (50 < TIQ < 70) 2 (14) 4 (20)
Moderate impairment (TIQ < 50) - 2 (10)
No data 2 (14) 1 (5)
a
Hypoxic-ischemic encephalopathy (HIE) includes different categories for perinatal brain damage,
i.e. Periventricular leukomalacia (PVL), Intraventricular haemorrhage (IVH), Cerebral Vascular Ac-
b
cident (CVA) or combinations of these categories; Acquired brain damage consists of different
categories, i.e. CVA, meningitis and tumour. 9
The mean age and the distribution of visual acuity levels of the three different
groups did not differ significantly. The distributions of the estimated cognitive
2
level did significantly differ (χ (2) = 11.29, p < .01) between groups: post-hoc
analyses showed a higher mean cognitive level of the OVI group than of the
two other groups.
Procedures
The subtest Gestalt Closure of the Kaufman Assessment Battery for children
second edition (KABC-II) consisted of one example item and 37 tests items
[12]
of increasing difficulty. The items contained incomplete black figures on
a white background and represent 12 animate objects (7 animals including
a dinosaur and 5 human faces or activities), and 25 inanimate objects. The
normal clinical procedure would be to start with the example item followed by
the age appropriate items. Here, we showed all items on a 24-inch monitor
with an integrated infrared eye-tracking system (Tobii T60-XL, Tobii Corpora-
tion, Sweden). In-between each item, a neutral display was shown with a
fixation point to let the child refocus on the centre of the monitor. The system
measured gaze position of each eye separately using cornea reflection and
compensated for free head movements. Each child sat at approximately 60
cm distance from the monitor. The visual angle towards the monitor was ap-
proximately 30x24 degrees (1280 x 1024 pixels). Eye movement responses
were recorded with a sampling rate of 60 Hz and the latency of the system was
approximately 25 ms. The experiments were conducted in a quiet room with
ambient light conditions. Prior to starting the Gestalt Closure test a standard-
ized 5-point calibration procedure of both eyes was performed. Item presenta-
tion time was dependent on the child’s verbal response, i.e. the examiner
pushed the spacebar after the first answer to each item and thereby ended the
item presentation. The examiner also noted whether the answer was correct.
After 4 consecutive errors the assessment was stopped. All data were stored
off-line.
Data analysis
Performance data
Firstly, we scored items the standard way, i.e. recognition was either correct
or incorrect. The items after discontinuation were assumed to be too difficult
and therefore scored as incorrect. Raw scores, i.e. the total correct items up to
four consecutive incorrect answers, were noted and the American norm values
Gestalt perception and eye tracking 181
[12]
for the age group 4-14 years old were used to classify the performances,
based on scaled scores (M = 10; SD = 3): scaled scores 1-5 (expected: 9%)
= weak; 6-7 = below average (expected: 16%); 8-11 = average (expected:
50%); 12-13 above average (expected: 16%); 14-19 = superior (expected:
9%). Secondly, a simple item analysis was done by calculating the percentage
of patients that correctly recognized each item. This way, we were able to
check whether items increased in difficulty as reported in the original popula-
tion. For the analysis of the subgroups, i.e. the animate and inanimate items,
we calculated the percentage of correct items with respect to the total number
of items presented in that subgroup.
Statistical analysis
We used IBM SPSS Statistics version 20 for statistical analyses. Non-paramet-
ric tests were used, since data were not normally distributed, even not after
data transformation. To compare groups with ordinal (number of items shown;
scaled scores) and skewed data (percentage correct of presented items),
Kruskal Wallis and Mann-Whitney U-tests were used. To test for differences
in performance while controlling for differences in cognitive level, we used
the partial Spearman correlation test. Binomial tests were used the compare
the expected percentage of weak, average and superior performers with the
actual percentages found in the patient groups. Finally, an explorative cor-
relation analysis was done between weak overall performance, visual acuity,
nystagmus and eye tracker results. p-Values ≤ .05 were considered significant.
182 Chapter 9
Results
The collection of the performance scores of one patient with albinism in the
group OVI (nOVI =37, 22 males, 15 females) failed, resulting in a total group of
seventy-one tested patients (Mage= 9y9m, SD = 2y5m; 41 males, 30 females).
Overall performance
Scaled scores
Analysis of the scaled scores showed that the distributions of scores signifi-
2
cantly differed across groups (χ (2) = 8.65, p =.01). The group CVI performed
significantly worse (Mdn = 2) than the group OVI (Mdn = 9; U = 197.5, p <
.01). Compared to the normal distribution of the scaled scores in the norm
population, half of the patients in the group CVI performed extremely weak.
A scaled score of 5 is expected in 9% of the population, yet, this scaled score
of 5 or lower was found in 9/37 (24%) of the OVI patients, 5/14 (36%) of the
OCVI patients and 12/20 (60%) CVI patients (ps < .01). Despite these weak
performances, still 12/37 (32%) of the OVI patients, (7/14) (50% of the OCVI
patients and only 12/37 (32%) of the CVI patients performed on an average
level (p = .05 and p < .01). The percentage of patients that performed at a
superior level was not higher than expected. The Spearman rho correlations
between the patient groups and 1) the scaled item scores (rs = -.31) and
2) the proportion weak performers (rs = .32) were significant (ps = .02).
Controlling for the cognitive level, group differences in scaled scores were
only near significant (rs,cognitive level = -.25, p = .07), but group differences
in the proportion of weak performers remained significant (rs,cognitive level =
.26, p = .05). This suggests that the performance of the group CVI remains
significantly weaker after correction for differences in cognitive level.
Item scores
The item scores showed a monotone decrease with increasing number of
presented items, suggesting that test difficulty increased per presented item
(Figure 1). Notably, the percentage correct animate items, especially the ani-
mal items, deviated from this general pattern. We found that the animal items
were more difficult to recognise or to name than the inanimate items. The
most difficult items were the dinosaur (item 7; 44% correct) and the elephant
(item 18; 39% correct).
general pattern. We found that the animal items were more difficult to recognise or to
name than the inanimate items. The most difficult items were the dinosaur (item 7; 44%
correct) and the elephant (item 18; 39% correct). Gestalt perception and eye tracking 183
Figure1.1.Percentage
Figure Percentageof of correct
correct answers
answers per item-group:
per item-group: inanimate
inanimate objectsobjects and animate
and animate objects, objects,
human(activity)
human (activity) and
and animals.
animals.
Analysis
Analysisof of
thethe
percentage correct
percentage answers
correct of the
answers of presented itemsitems
the presented showed that
showed
2
that significant
significant differences
differences on performances
on performances werepresent
were indeed indeed(χpresent
2
(χ (2)
(2) = 7.28, =
p=.03), see
7.28, p = .03),
also Figure see
2. The alsoCVI
group Figure
(Mdn2.=The
59.94)group CVI (Mdn
performed = 59.94)worse
significantly performed
than the group
significantly worse than
OVI (Mdn = 73.33; the group
U = 215.0, OVIThe
p=.01). (Mdn = 73.33;
difference U = 215.0,
between p = . CVI
the groups 01).and OCVI
The difference between the groups CVI and OCVI (Mdn = 67.95) and OCVI
(Mdn = 67.95) and OCVI and OVI were not significant. Significant negative correlations9
and OVI were not significant. Significant negative correlations (rs = -.34, p
(rs = -.34, p =.01; rs.cognitve level = -.29, p = .03) were found between the percentage
= .01; rs.cognitve level = -.29, p = .03) were found between the percentage
correctly recognized items and the patient groups, indicating that cognitive level does not
correctly recognized items and the patient groups, indicating that cognitive
explain the group difference found.
level does not explain the group difference found.
Gestalt perception and eye tracking | 167
Figure 2. Distribution of percentage correct answers given the number presented items in the
different patient groups.
Animate items
Analysis of the number of animate items presented showed that the number of presented
animal items differed across groups (χ2(2) = 6.82, p =.03), suggesting differences in
184 Chapter 9
Animate items
Analysis of the number of animate items presented showed that the number
2
of presented animal items differed across groups (χ (2) = 6.82, p = .03),
suggesting differences in performances. In the groups OVI and the OCVI, only
1 patient was presented less than 7 items (the total number of animal items)
(OVI: 2 items; OCVI: 5 items). In the group CVI, 7 patients were presented
less than 7 items; less than 3 items were presented to 5 patients, less than
5 items to 1 patient and less than 6 items were presented to 3 patients. The
number of presented items was significantly different between the groups OVI
and the CVI (U = 290.0, p < .01). Analysis of the percentage correct answers
of the presented items showed that significant differences in performances
2
were indeed present (χ (2) = 13.45, p < .01), see also Figure 3. The groups
CVI (Mdn = 50.00) and OCVI (Mdn = 64.29) performed significantly worse
than the group OVI (Mdn = 85.71; U = 171.5, p < .01 and U = 158.00, p =
.03). The difference between the groups CVI and OCVI was not significant.
A significant negative correlation (rs = -.43, p <.01) was found between the
percentage correctly recognized animals and the patient groups. This indi-
cates that children with brain damage tend to perform worse than children
without brain damage (OVI) on the animal items. Importantly, this correlation
remained significant when controlling for differences in cognitive level (rs.
level 9=
168 | Chapter
cognitve -.38, p < .01).
Figure 3. Distribution of percentage correct answers given the number presented animal items
(max 7 items) in the different patient groups.
Inanimate items
Inanimate items
To test whether the same pattern of group differences was also present in
To test whether the same pattern of group differences was also present in recognising
recognising the we
the inanimate items, inanimate
first selecteditems, weitems
7 inanimate firstwith
selected 7 inanimate
approximately the same items with ap-
proximately the
performance score same
as the performance
7 animal score
items. We selected itemas the16,7 19,
2, 10, animal items.
20, 23 and 24. We selected
The median difference in performance between these two item sets was -1% (range -6%
to +4%). Thus, compared to the animate items, these selected inanimate items were a
bit easier to recognize. Again, the number of presented inanimate items varied from 1 to
7 in the groups OVI an CVI and 2 to 7 in the group OCVI. The distribution of the number
of presented inanimate items significantly differed across the groups (χ2(2) = 11.45, p
Gestalt perception and eye tracking 185
item 2, 10, 16, 19, 20, 23 and 24. The median difference in performance
between these two item sets was -1% (range -6% to +4%). Thus, compared
to the animate items, these selected inanimate items were a bit easier to
recognize. Again, the number of presented inanimate items varied from 1 to 7
in the groups OVI an CVI and 2 to 7 in the group OCVI. The distribution of the
number of presented inanimate items significantly differed across the groups
2
(χ (2) = 11.45, p < .01). In the group CVI, a significantly smaller number of
items was presented (Mdn = 5) than in the group OVI (Mdn = 7; U = 212.5,
p < .01). The percentage correct answers, however, to the inanimate items
was not significantly different between the groups (MdnOVI = 85.71, MdnOCVI
= 71.43 MdnCVI = 60.00; p = .13). Correlations between performance and
groups were not significant (rs = -.21, rs.cognitve level = -.19). Thus, children
with CVI tend to perform in a similar way as the children with OCVI and OVI
on inanimate items.
Gaze patterns
Group characteristics
Of the seventy-two patients forty-five patients had at least 40% gaze data. The
group OVI consisted of 20 patients (12 males, 8 females). The chronological
age ranged from 5y0m to 13y7m (M = 9y10m, SD = 2y7m). Thirteen patients
had iris or retinal abnormalities: iris coloboma (n = 1); ocular or oculocutane-
9
ous albinism (n = 9); cone/rod dysfunction (n = 2); retinitis pigmentosa (n
= 1). Three patient had lens abnormalities: high myopia (n = 1), Stickler
Syndrome); cataract (n = 2). Three patients had congenital nystagmus and
the cause of visual problems was unknown in one patient. The group included
4 patients with a weak performance on the Gestalt test.
The group OCVI consisted of 11 patients (5 males, 6 females). The chrono-
logical age ranged from 6y5m to 13y7m (M = 9y7m, SD = 2y8m). Aetiology
of brain damage was: asphyxia (n = 3), dysgenesis (n = 1), periventricular
leukomalacia (n = 1), intraventricular haemorrhage (n = 1), atrophy (n = 1).
Imaging data was not available for four patients. Present ocular abnormalities
were: nystagmus (n = 5); ocular albinism (n = 2); optic nerve atrophy (n =
1); and retinitis pigmentosa (n = 2), unknown (n = 1). The group included 3
patients with a weak performance on the Gestalt test.
The group CVI consisted of 14 patients (10 males, 4 females). The chrono-
logical age ranged from 4y6m to 13y10m (M = 10y2m, SD = 2y6m). Aetiology
of brain damage was: asphyxia (n = 3), Arnold-Chiari malformation (n =
1), periventricular leukomalacia (n = 2), cerebral vascular incident (n = 3),
186 Chapter 9
tumour (n = 1). No imaging data was present in four patients. This group
included 8 patients with a weak performance on the Gestalt test.
The mean age and the estimated cognitive level of the three different groups
did not differ significantly, see Table 2. Group differences were present in the
2 2
distributions of the visual acuity (χ (2) = 7.27, p = .03) and nystagmus (χ (2)
= 12.22, p < .01). Post-hoc analyses showed a higher visual acuity and fewer
patients with nystagmus in the group CVI than of the two other groups (ps
≤.02). Visual acuity in the groups OVI and OCVI were considered comparable.
Table 2. Group characteristics of children with at least 40% gaze data in the groups OVI (n = 20),
OCVI (n = 11) and CVI (n = 14).
OVI OCVI CVI
Characteristic n (%) n (%) n (%) p-value
Glasses 9 (45) 8 (73) 6 (43)
Strabismus 7 (35) 4 (36) 10 (71) .09, ns
Nystagmus 15 (75) 11 (100) 5 (36) <.01
Visual acuity .03
≥ 0.8 1 (5) 4 (29)
0.5-0.8 4 (20) 3 (21)
0.4-0.5 3 (27) 3 (21)
≤ 0.3 15 (75) 8 (73) 4 (29)
Cognitive level .07, ns
Average (TIQ ≥ 90) 7 (35) 4 (36) 1 (7)
Below average (70 < TIQ < 89) 2 (10) 1 (9) 4 (29)
Borderline (70 < TIQ < 89) 3 (15) 3 (27) 3 (21)
Mild impairment (50 < TIQ < 70) 2 (10) 1 (9) 3 (21)
Moderate impairment (TIQ < 50) 2 (14)
No data 6 (30) 2 (18) 1 (7)
Item characteristics
In one CVI patient, no eye tracking data was available during the presentation
of the 7 animal and 7 selected inanimate items. In the remaining group of
44 patients, eye tracking data during the presentation of the animal items
was present for at least 4 items in 20/20 OVI patient, 11/11 OCVI patients
and 11/13 CVI patients. To control for individual differences in the number
of items, we used mean individual outcomes for group comparisons. Overall,
no significant group differences on the number of visits and the median visit
duration of each visit within the area of interest (AOI) were found, but we
2
did find a significant difference in the total visit duration (χ (2) = 6.38, p =
.04), see Table 3. This indicates that children with CVI tend to need more time
Gestalt perception and eye tracking 187
Table 3. Outcomes of eye tracking data (number of visits of area of interest, median visit duration 9
and total visit duration) on animal items in the groups OVI (n = 20), OCVI (n = 11) and CVI (n = 13).
OVI OCVI CVI p-value
Mean
# visits AOI 7 (1-33) 10 (3-15) 6 (2-28) ns
Median visit duration 0.7 (0.1-3.4) 0.7 (0.1-3.3) 1.3 (0.1-4.7) ns
Total visit duration 3.7 (1.0-6.7) 3.8 (0.5-12.0) 8.4 (0.2-14.4) .04
Butterfly
n 20 11 11
# visits AOI 4 (1-15) 2 (1-12) 3 (1-13) ns
Median visit duration 0.4 (0.1-3.5) 1.3 (0.1-3.6) 1.2 (0.2-6.1) ns
Total visit duration 2.4 (0.1-3.5) 2.2 (0.1-5.2) 2.7 (0.8-13.1) ns
Dog
n 20 11 13
# visits AOI 3 (1-19) 2 (1-11) 2 (1-22) ns
Median visit duration 1.0 (0.1-3.5) 0.6 (0.1-3.4) 1.7 (0.1-5.6) ns
Total visit duration 2.6 (0.7-7.0) 2.4 (0.1-4.4) 3.0 (0.1-20.7) ns
188 Chapter 9
Table 3. Outcomes of eye tracking data (number of visits of area of interest, median visit duration
and total visit duration) on animal items in the groups OVI (n = 20), OCVI (n = 11) and CVI (n =
13). (continued)
OVI OCVI CVI p-value
Dinosaur
n 20 11 12
# visits AOI 8 (1-47) 7 (1-25) 5 (1-63) ns
Median visit duration 0.7 (0.1-6.2) 0.8 (0.1-11.8) 2.4 (0.3-7.2) .08
Total visit duration 5.1 (1.8-26.6) 5.5 (0.6-11.8) 6.1 (1.6-30.2) ns
Fish
n 20 10 10
# visits AOI 3.0 (1-90) 5.5 (1-24) 7.0 (1-44) ns
Median visit duration 0.7 (0.1-4.4) 1.0 (0.1-3.2) 0.80 (0.3-6.4) ns
Total visit duration 2.8 (0.1-7.6) 2.9 (0.1-22.5) 6.35 (1.18-19.96) ns
Turtle
n 20 10 12
# visits AOI 10 (1-13) 10 (4-34) 8.5 (1-27) ns
Median visit duration 0.4 (0.1-4.0) 0.3 (0.1-6.0) 0.8 (0.1-7.0) ns
Total visit duration 3.2 (0.4-17.6) 5.6 (1.4-24.2) 5.3 (0.5-29.0) .10
Pig
n 19 10 10
# visits AOI 7.0 (1-29) 4.0 (1-17) 4.0 (1-12) ns
Median visit duration 0.3 (0.1-3.8) 0.6 (0.1-4.2) 1.6 (0.3-9.0) .03
Total visit duration 2.6 (0.1-7.4) 2.9 (0.1-23.0) 4.0 (1.9-18.0) .12
Elephant
n 20 10 9
# visits AOI 7 (2-44) 15 (2-35) 5 (1-94) ns
Median visit duration 0.4 (0.1-1.1) 0.3 (0.1-1.2) 0.6 (0.2-3.6) .03
Total visit duration 3.4 (0.1-6.7) 5.0 (0.1-16.3) 5.6 (1.0-43.0) ns
AOI = area of interest. p-values indicate statistically significant differences in eye tracking param-
eters between patient groups.
Table 4. Outcomes of eye tracking data (number of visits of area of interest, median visit duration
and total visit duration) of the seven selected object items in the groups OVI (n = 20), OCVI (n =
11) and CVI (n = 12).
OVI OCVI CVI p-value
Mean
# visits AOI 6 (1-34) 5 (2-13) 6 (2-19) ns
Median visit duration 1.0 (0.2-5.0) 1.3 (0.1-2.6) 1.3 (0.1-4.2) ns
Total visit duration 3.0 (0.8-7.8) 4.2 (0.6-5.9) 4.7 (1.0-14.8) ns
AOI = area of interest. p-values indicate statistically significant differences in eye tracking param-
eters between patient groups.
Gestalt perception and eye tracking 189
Discussion
study showed that early visual deprivation in patients with congenital cataract
aged 9-23 years was related to impairments in holistic (face) processing.
[22]
Our current results in a more general population of children with visual
impairments confirms that in children who have experienced some sort of
visual deprivation early in life, holistic visual processing in general seems to
be affected.
Notably, children with brain damage (groups CVI and OCVI) performed
significantly worse on the animate items than the group without brain damage
(OVI). Differences between groups on the inanimate items were smaller and
non-significant, suggesting that the overall difference can mainly be attributed
to the weak performance on the animal items. The gaze data collected with
the eye tracker reveals that the CVI children with weak performances fixate
these Gestalt items longer and even re-fixate them more often. This suggests
that this difference in performance may not attributed to a lack of effort.
Further analysis on the 7 animal items, items earlier in the test than the 7
selected object items but with a comparable difficulty level, shows that weak
performers within the group OVI spend less time within the area of interest
(AOI) per visit. There was no relation with visual acuity or nystagmus, which
suggests there is another reason why they perform weak. Maybe children with
OVI have learned other strategies, for example to guess more often to save
time and energy or to perform as fast as children without a visual impairment.
In order to study this hypothesis a control group should be added, and reac-
tion times and performances should be compared.
It has been shown that processing of either animate or inanimate pictures
can be selectively impaired in patients with damage to anterior visual areas.
[23-25]
More recently, fMRI studies found clusters of voxel population vectors
that were associated with animate and inanimate categories located anterior
[26, 27]
to retinotopic visual areas. However, in these studies, images of hun-
dreds of well-defined objects were presented to the subjects. In the present
study, visual processing of each item involved perceptually grouping of closely
projected elements to visualize a complete object, even when presented
incomplete information. To our surprise, we found a significantly worse perfor-
mance for naming the animate items in children with confirmed or suspected
brain damage. We could not find any support for our finding in literature. At
this point, we do not know if the differences we found between animate and
inanimate object recognition in children with cerebral visual impairments are
related to possible damage to the associated processing areas in the brain,
[26]
e.g. the occipital face area (OFA) and the extra-striate body area (EBA).
Gestalt perception and eye tracking 191
The available imaging data lack the detailed information that is required to
obtain insight in these specific regions.
This study has some limitations that need to be addressed. Firstly, the
Kaufman Gestalt closure task contains a fixed number of 37 items. We applied
the classic stopping rule, i.e. we stopped testing, when a subject gave 4 con-
secutive incorrect answers. As a result, the total number of tested items was
different between the subjects. For the between group comparisons per item,
we were able to control for this by calculating the correct items with respect
to the total number of items presented within each subject. The comparison of
the performance scores between the animate and inanimate items, however,
inevitably led to two different subgroups of patients. Secondly, in a majority of
the patients, only the global cognitive functioning was scored using total IQ.
We are aware of the fact that more exact data on verbal and non-verbal IQ is
preferable to control for differences in developmental level between groups.
Thirdly, the performance of the children in the present study was compared
with American norm group. We did investigate any cultural differences. Some
of the items were typical American illustrations, such as a land map of the US.
These items were not judged too strictly – and were not selected for further
item analysis. Fourthly, we did not check after the Gestalt closure test whether
children could name standard drawings of the same objects. Especially for the
animate items, this would have been a valuable control condition. Lastly, the
size of the area of interest dependent on the size of the Gestalt closure item.
9
As a result, some AOI’s were larger than others but not more than ~20%.
Presumably, this had some influence on the number of re-fixations, especially
for the small Gestalt closure items. In addition, we attempted to investigate
whether a subject fixated the different elements within the Gestalt closure
item to create an overview or that this was obtained with one central fixation.
Due to the variability in gaze behaviour, we were not able to find a consistent
pattern. In a future study, we would like to address this question using a
fixed set of Gestalt closure items of equal sizes and a higher resolution eye
tracker. Lastly, the quality of each eye tracking study depends on the quality
of the recorded gaze patterns. In our group, 45 of the 72 patients (63%) had
at least 40% valid gaze data. In the present study, the investigator was able
to keep track of the gaze tracking quality. Still, we applied this rather strict
criterion because we needed good continues gaze tracking data during item
presentation to be able to calculate the presented gaze parameters.
In the present study we presented data on Gestalt perception performance
in combination with looking behaviour in visually impaired children. Further
research is necessary to address causality of the results: did a different way
192 Chapter 9
Conclusions
This study showed that children with visual impairments more often performed
weak on the Kaufman Gestalt closure task than chronologically age-matched
controls, and that children with brain damage performed worse than children
without brain damage. Notably, children with brain damage (groups CVI and
OCVI) performed significantly worse on the animate items than the group
without brain damage (OVI). Based on the looking patterns obtained with the
eye tracker, we can conclude that weak Gestalt performance of the children in
the CVI group is not the result of intellectual disability or a lack of effort, but
instead seems a pure perceptual dysfunction.
Gestalt perception and eye tracking 193
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Functions in Children with Visual Pathology: A Longitudinal Study. Accepted for
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12. Kaufman, A. and N. Kaufman, Kaufman Assessment Battery for Children: technical
manual. second edition ed. 2004, Circle Pines, MN: American Guidance Service.
13. Bölte, S., et al., Gestalt perception and local-global processing in high-functioning
autism. Journal of Autism and Developmental Disorders, 2007. 37(8): p. 1493-
1504.
14. Uhlhaas, P.J., et al., Perceptual grouping in disorganized schizophrenia. Psychiatry
Research, 2006. 145(2-3): p. 105-117.
15. van de Ven, V., et al., Reduced intrinsic visual cortical connectivity is associated
with impaired perceptual closure in schizophrenia. Neuroimage Clinical, 2017. 15:
p. 45-52.
16. Hodapp, R.M., et al., K-ABC profiles in children with fragile X syndrome, Down
syndrome, and nonspecific mental retardation. American Journal of Mental Retar-
dation, 1992. 97(1): p. 39-46.
17. Koppitz, E.M., Diagnosing brain damage in young children with the Bender Gestalt
test. Journal of Consulting Psychology, 1962. 26: p. 541-546.
194 Chapter 9
General discussion
General discussion 197
The overall aim of this study, supported by Royal Dutch Visio, Centre of Ex-
pertise for blind and partially sighted people, was to provide new information
to advance efficient evidence-based diagnostic procedures for cerebral visual
impairment in children, in order to improve detection and neuropsychological
diagnosis in clinical practice.
We first investigated the potential of the crowding ratio for early detection
of cerebral visual impairment on different levels of the care chain. Next, we
specifically focussed on aspects of dorsal stream dysfunction (motion per-
ception, object recognition, visual attention, visuoconstructive functioning),
investigating the applicability and shortcomings of available quantitative neu-
ropsychological tests for their diagnosis and detection. We further performed
first epidemiological explorations of dorsal stream dysfunctioning in children.
Because neuropsychological testing is only reliably feasible from the age of
4 years onwards, we included children aged 4 to 7 years into the study, both
children at risk for cerebral visual impairment because of (suspected) brain
damage and a control group of typically developing school children.
For younger children and children with disabilities, a joint collaboration with
the Neuroscience department was initiated for the development of a new
diagnostic method based on the assessment of (reflexive) eye movements
towards visual stimuli using remote eye tracking. Here, we performed explor-
atory data analysis on normal gaze patterns to motion coherent stimuli and to
items that require the ability to visually integrate parts of the representation
of objects into a whole (Gestalt perception) by quantification of reaction times
and fixation qualities.
10
Principal findings
Table 1. Impeding factors for detection, habilitation and intervention of cerebral visual impairment
General practitioner, (Child) ophthalmologist, Special services for visually
neonatologist, orthoptist, optometrist, impaired people or low
paediatrician, child optician vision services
neurologist, rehabilitation
specialist, intellectual
disability physician
o Unconsciousness of cerebral o Limited resources to assess o Lack of objective eligibility
visual impairment, especially all children at risk, specifically criteria for neuropsychological
of impairments other than low children with developmental assessment
vision delay or intellectual disabilities o Not all visual functions in
o Lack of easily applicable o Unconsciousness of possible children can be assessed with
detection instrument impairment of visual functions quantitative tests
o Assumption that assessment other than visual acuity and o Dutch eligibility criteria
of visual functions in children visual fields for long-term intervention
with an intellectual disability or o No referral of children with and habilitation and for
developmental delay is (sub)normal vision for accessibility to and refunding
- too difficult evaluation of visual perception of aids and appliances
- too big a burden for the child insufficiently include
- not useful in all children children with cerebral visual
impairment and (sub)normal
visual acuity
Crowding
In low vision services, the decision which children to select for neuropsycho-
logical assessment of cerebral visual functioning would be facilitated by adding
crowding assessment to routine orthoptic intake assessments. In recent years
this has already become more common.
Professionals should be aware that results are likely affected by test char-
acteristics, like symbol spacing (fixed or proportional) and test distance, and
patient characteristics, i.e. presence of absence of brain damage, low vision
[13-15] [15]
or nystagmus. Results of the study of Huurneman et al suggest that
testing at a long distance (5 m) with a test with a fixed symbol spacing results
in higher crowding in children with low vision and nystagmus. Children with low
vision but no nystagmus performed comparable to children with normal vision.
In our study with a chart with a proportional symbol spacing (inter symbol
[13]
spacing 50%) children with ocular abnormalities, including nystagmus,
performed comparable to children without abnormalities, whereas crowding
was higher in children with brain damage. For children with cerebral visual
General discussion 203
impairment, testing at a distance may be more difficult than for children with
ocular abnormalities, leading to worse outcomes. This could be investigated,
too, in the research project in youth healthcare, suggested above.
[16]
Crowding problems may also have implications for reading. If all crowd-
ing ratios are size independent, as in amblyopics, critical spacing assessed
with the crowding cards can be used to estimate critical spacing for reading
[16]
(spacing between letters). Adjustment of the spacing in text according to
the individual’s critical spacing could then optimise reading rate. This could
explain why magnification is generally considered to help, because spacing as
well as letter size increase.
Neuropsychological assessment
Based on Chapter 6 and 7 we recommend that multiple aspects and func-
tions should be routinely included in neuropsychological assessment of dorsal
stream dysfunction in children at risk, because problems were found to be
mostly isolated and heterogeneous. In low vision services, use of the child´s
performance age in the interpretation of test outcomes, as recommended
and used in Chapter 5-7, is increasing, but not yet standard. We showed
in Chapter 6 how the use of chronological age leads to overdiagnosis of
[17]
motion perception dysfunction. Testing of performal IQ or expert estima-
tion of performance age should be routinely performed by psychologists and
behavioural scientists in low vision services. Efficiency of different diagnostic
strategies should be systematically evaluated.
Generally, the neuropsychologic tests applied in this study appeared valid
and applicable, but several aspects can be improved. On a group level, they 10
discriminate between children at risk and typically developing children. How-
ever, normal limits remain a bottleneck for all tasks, requiring evaluation in
larger samples. This does not necessarily hamper their current clinical ap-
plication as observational instruments: confidence intervals of normal limits
may give an indication whether a child belongs to the weakest 5 or 10 percent
performers, but more work has to be done to obtain valid reference values.
For subtests of the L94 in which children have to name objects (VIEW, De
Vos, NOISE), the influence of children’s verbal development and word fre-
quency used in their socioeconomic environment on concurrent validity has
to be investigated further, too. Current norms of the nearly 25 years old L94
should urgently be updated in new study groups.
In Dutch low vision services, quantitative neuropsychological tests of mo-
tion perception and visual search or selective visual attention, as applied
and evaluated in our study, are not yet part of routine neuropsychological
204 Chapter 10
We conclude that our study has considerably added to insights into the
value and shortcomings of internationally available diagnostic tests for dorsal
stream function problems in children, leading to specific, underpinned recom-
mendations for selection of tests and further steps in research, as well as
technical improvements of the tests, used in the current study. The eye tracker
paradigms introduced in this thesis even enable quantitative testing of motion
perception problems in very young and intellectually disabled children and
Gestalt perception in children suspected of brain damage. This new approach
will definitely add value to the existing neuropsychological assessments.
We established that dorsal stream problems in children with (suspected)
brain damage are rather isolated than generalised, so multiple aspects should
be part of neuropsychological assessments. And we evaluated crowding as a
screening method for cerebral visual dysfunction. Although a lot of work has
yet to be done before the tests are completely fit for use in clinical practice, we
could formulate first recommendations for improvement of both the referral
process towards specialised low vision services and within these services, the
selection of clients for neuropsychological assessment.
General discussion 207
References
1. MacKay, T.L., et al., Deficits in the processing of local and global motion in very
low birthweight children. Neuropsychologia, 2005. 43(12): p. 1738-48.
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lands Oogheelkundig Gezelschap.
13. van der Zee, Y.J., P. Stiers, and H.M. Evenhuis, Should we add visual acuity ratios
to referral criteria for potential cerebral visual impairment? J Optom, 2017. 10(2):
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14. Huurneman, B., et al., A systematic review on ‘Foveal Crowding’ in visually im-
paired children and perceptual learning as a method to reduce Crowding. BMC
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15. Huurneman, B., et al., Crowding in central vision in normally sighted and visually
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208 Chapter 10
16. Levi, D.M., S. Song, and D.G. Pelli, Amblyopic reading is crowded. J Vis, 2007.
7(2): p. 21 1-17.
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with brain damage and the risk of overdiagnosis. Submitted.
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with intellectual disabilities. Res Dev Disabil, 2012. 33(5): p. 1670-6.
19. Boot, F.H., et al., Quantification of visual orienting responses to coherent form and
motion in typically developing children aged 0-12 years. Invest Ophthalmol Vis
Sci, 2012. 53(6): p. 2708-14.
20. Boot, F.H., et al., Delayed visual orienting responses in children with develop-
mental and/or intellectual disabilities. Journal of Intellectual Disability Research,
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tal and/or intellectual disabilities. J Intellect Disabil Res, 2012.
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Functions in Children with Visual Pathology: A Longitudinal Study. Accepted for
publication in Brain & Development, 2018.
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Chapter
Chapter 10:
10: Appendix
Appendix 1
1
Chapter 10: Appendix 1 211
Appendix 1. Care supply chain for children with visual impairments according to existing Dutch
guidelines for different professional disciplines
Pregnancy and birth
Complications?
No Yes
[1, 2]
General Practitioner or Midwife Pediatrician, neonatologist or child
Health screening, including inspection of the eyes neurologist
[3]
Referral to ophthalmologist within a week if: Developmental delay and brain damage:
o Suspicion of congenital ocular abnormalities, As part of diagnostic procedure: referral
specifically cataract and glaucoma for orthoptic/ophthalmologic assessment
Consultation or referral if: including strabismus, slitlamp biomicroscopy,
o Conjunctivitis ophthalmoscopy
[4]
Down Syndrome:
Referral for active orthoptic/ophthalmologic
screening at different ages
[6] [4]
Youth healthcare physician/ General Practitioner Down Syndrome Team
[5]
nurse Assessment of distance visual Ophthalmologist or orthoptist in
Preschool and school age: acuity and refractive errors if the team?
Scheduled screening of health parents or patient complain about
and development, including vision
inspection of the eyes and Referral to ophthalmologist if:
screening of distance visual o Visual acuity ≤0.2
acuity o Wearing a correction
- spherical >± 7 D or
cylindrical >± 3 D
Referral to ophthalmologist in o Monocular distance visual
case of: acuity: ≤ 6 years >0.2 and
- Fixation/following problem <1.0 6-20 years >0.2 and
- Abnormal ocular structures <1.0 and myopia and/or
- Monocular/binocular distance astigmatism or other ocular
visual acuity < 5/10 abnormalities or unrecognised
- Suspicion of cerebral visual amblyopia
impairment (risk groups)
Specialist assessment
[7]
Optometrist, Optician Ophthalmologist and orthoptist Ophthalmologist and orthoptist in
Checks of ocular condition and Detection or exclusion of ocular case of Down Syndrome:
[4]
10A1
refractive errors, prescription of abnormalities Active screening every 2 years,
glasses Referral to low vision service if specifically including cataract,
there is a request for help strabismus, amblyopia, refraction,
and one of the following criteria: nystagmus, visual acuity,
o Visual field defect: accomodation, keratoconus
- Concentrical <30°
- Hemianopsia
o Distance visual acuity:
- <0.3
- 0.3-0.5 + need special
support
o Near visual acuity:
- < 0.25
- Insufficient reading with
addition of +4
o Severe light sensitivity
Special services for visually
impaired people or low vision
services
Diagnostics, treatment and
habilitation
212 Chapter 10: Appendix 1
Chapter 9 is again a description of an eye tracker study. This time, the focus
was not on assessment of visually-guided responses, but on assessment of
different fixation strategies during a Gestalt perception task. Such task as-
sesses the ability to visualize a complete whole when presented incomplete
information or a partial picture, a so-called Gestalt item. To our knowledge,
this is one of the first studies on Gestalt perception in visually impaired chil-
dren with a special focus on (sustained) visual attention. The database of a
longitudinal eye tracking study consisted of 72 patients/clients of Royal Dutch
Visio who underwent the Gestalt closure test. Digitised Gestalt items were
shown one-by-one on a monitor with an integrated eye tracker to test the
performance and to quantify the number of fixations and the mean and total
fixation duration. The children were divided in three different groups: ocular
visual impairments (OVI; n = 38), ocular and cerebral visual impairment
(OCVI; n = 14) or cerebral visual impairments (CVI; n = 20). Children with
visual impairments performed more often weak than age-matched American
controls. Differences remained significant even after controlling for differences
in cognitive level. Children with brain damage performed significant worse on
the animate items than the group without brain damage. The data collected
on orienting attention revealed that this performance in the CVI children could
Sum
not be attributed to a lack of effort.
3. problems are specifically found for global motion and motion-defined form
perception;
4. motion speed problems are scarce, but motion speed discrimination is a
complex task and cognitive limitation hampers understanding of the test;
5. biological motion tests are too difficult for this developmental age group
and/or its’ validity is questionable;
6. other dorsal stream problems (object recognition, visual attention, visuo-
contructive functioning) are more often isolated than simultaneous pres-
ent;
7. object recognition problems are associated with weak motion perception
and weak visual attention, but not with weak visuoconstructive function-
ing;
8. the performances on Gestalt perception are weak compared to the children
without brain damage. Specifically recognising the animate items seems
impaired.
Sum
Samenvatting
Samenvatting
Samenvatting 225
Hoofdstuk 2 gaat over de vroege herkenning van kinderen die een verhoogd
risico hebben op cerebrale visuele problemen. De verschillende stappen in
de diagnostische keten, namelijk de jeugdgezondheidszorg, de oogheelkunde
en de visuele revalidatiecentra, stonden hierbij voor ons centraal. Het doel
van deze studie was te onderzoeken of in de uitkomsten van verschillende
gezichtsscherptetests (detectie vs. herkenning) en het meten van ‘crowding’
een extra bijdrage leveren bij de opsporing en doorverwijzing van kinderen
met een verhoogd risico op cerebrale visuele stoornissen. Crowding is het
verschijnsel dat iemand hinder heeft van omringende visuele informatie bij
het vaststellen van wat zij of hij ziet, ook bij een normale gezichtsscherpte.
Kinderen met verhoogde crowding kunnen bijvoorbeeld problemen hebben
bij het spelen (een vloer vol speelgoed), bij het eten (een volle gedekte tafel)
bij het winkelen (volle schappen in een supermarkt of een onbekende drukke
straat) of bij het lezen van lange woorden en teksten. Crowding kan worden
onderzocht door de prestaties op verschillende gezichtsscherptetests met
elkaar te vergelijken: testen met losse letters, waarbij de letter niet omringd
wordt met visuele informatie, en testen met letters omringd door andere let-
ters.
Uit ons onderzoek bleek dat in de jeugdgezondheidszorg de toevoeging van
diagnostiek gericht op crowding bij de screening op visuele problemen niet
wezenlijk bijdraagt aan de opsporing van kinderen met een verhoogd risico op
cerebrale visuele problemen. Daarentegen draagt deze ‘crowding diagnostiek’
in de oogheelkundige praktijk en het visueel revalidatiecentrum wel bij om on-
derscheid te maken tussen kinderen met alleen een oogheelkundig probleem
en kinderen met een verhoogd risico op een cerebraal visueel probleem.
Wij vonden echter ook dat bij het neuropsychologische onderzoek kinderen
met verhoogde crowding even vaak cerebrale visuele problemen hadden als
kinderen zonder verhoogde crowding. Onze conclusie is dan ook, dat crowding
en cerebrale visuele problemen wel vaak samengaan, maar dat de afgenomen
testen verschillende functies en vaardigheden meten. Verhoogde crowding kan
dan ook niet gebruikt worden als directe screeningsmethode voor cerebrale
visuele problemen, alleen voor screening op een verhoogd risico: op basis van
een verlaagde gezichtsscherpte zou slechts 29% van de onderzochte kinderen
met een verhoogd risico op een cerebraal visueel probleem worden doorver-
wezen, terwijl er bij 67% van deze groep sprake is van verhoogde crowding.
Verhoogde crowding is daarom mogelijk een waardevol aanvullend verwijscri-
terium. Wij adviseren oogartsen en visuele revalidatie- en adviescentra dan
ook om ‘crowding diagnostiek’ toe te voegen aan de standaard diagnostiek.
Samenvatting 227
SNL
Figuur 1. Een
Een voorbeeld
voorbeeld van
vantaken
takenvanvandrie
driesoorten
soortenbewegingswaarneming.
bewegingswaarneming. InIn
dede praktijk
praktijk is de
is de
achtergrond meestal
achtergrond meestal zwart
zwart en
en zijn
zijn de
de stippen
stippen meestal
meestal wit.
wit.
A. Globale
A. Globale beweging:
beweging: eeneen RDK
RDK waarin
waarin20%20%vanvandedestippen
stippentegelijk
tegelijkomhoog
omhoogbeweegt
beweegt(de
(destippen
stippen
met een
met een pijltje)
pijltje) en
en de
de rest
rest alle
alle kanten op. B.
kanten op. B. Biologische
Biologische beweging.
beweging. EenEen mensenfiguur
mensenfiguur met
met lichtjes
lichtjes
op de gewrichten, die naar rechts loopt. C. Vorm die bestaat uit beweging: een RDK waarin stippels
op de gewrichten, die naar rechts loopt. C. Vorm die bestaat uit beweging: een RDK waarin stippels
in de vorm van een vierkant omhoog bewegen en de rest omlaag. De grens van het vierkant is in
in de vorm van een vierkant omhoog bewegen en de rest omlaag. De grens van het vierkant is in
het echt niet te zien.
het echt niet te zien.
Met behulp van deze taken kan in getallen uitgedrukt worden hoe goed iemand beweging
Met
kan behulp
zien; van deze
wij noemen taken kan intaken.
dat ‘kwantitatieve’ getallen uitgedrukt
In voorbeeld A is worden hoe goed
het percentage ie-
stippen
mand beweging
dat iemand kan
minimaal zien;
nodig wijom
heeft noemen dat ‘kwantitatieve’
de samenhangende bewegingtaken.
te zien,In voorbeeld
zijn
‘drempel’. In voorbeeld C wordt de drempel meestal bepaald door het minimale
percentage stippen in het vierkant dat nodig is om het vierkant te onderscheiden. Het
228 Samenvatting
19/46 naar 24/46, ook het aantal kinderen met zwakke prestaties op 2 taken
nam significant toe en er was zelfs 1 kind dat zwak presteerde op alle 3 taken.
meten van visuele functies bij personen die niet kunnen meewerken met huidig
neuropsychologisch onderzoek. Het gaat hierbij bijvoorbeeld over kinderen
jonger dan 4 jaar of kinderen (en volwassenen) met verstandelijke beperkin-
gen. Bij deze methode maakten we gebruik van het feit, dat als de hersenen
een visuele stimulus goed kunnen verwerken, de ogen in een reflex naar deze
stimulus gaan kijken. We boden een drietal bewegingsperceptiestimuli op
basis van Random Dot Kinematograms (RDK’s) aan op een beeldscherm met
een ingebouwde camera voor het meten van oogbewegingen (de zogenaamde
eye tracker).
Deze methodiek hebben wij eerst op haalbaarheid en betrouwbaarheid ge-
test bij 188 kinderen (0-13 jaar) zonder visuele of neurologische problemen.
Wij toonden op het scherm drie verschillende RDK’s zien: één met verticale
beweging (RDK1), één met diagonale beweging (RDK2), en één met beweging
vanuit het centrum naar buiten (RDK3). De maat die met de software werd
gemeten, was de reactietijd van het kind: hoe lang deed het erover om zijn
ogen te fixeren op de goede plek.
De reactietijd was bij jonge kinderen (0-3 jaar) duidelijk langer dan bij
oudere kinderen (4-11+ jaar). Voor de oudere kinderen maakte ook het type
RDK uit voor de reactietijd.
Onze conclusie van deze eerste verkennende studie is dat het mogelijk is om
op basis van oogbewegingen uitspraken te doen over verschillende aspecten
van globale bewegingsperceptie. Dit is een bemoedigend resultaat voor de
verdere ontwikkeling van deze methode.
Wij hebben aangetoond dat de meeste van de door ons gebruikte kwantita-
tieve neuropsychologische tests bij kinderen toepasbaar en valide zijn. De
eye tracking studie, zoals beschreven in Hoofdstuk 8, was onderdeel van een
evaluatie- en validatiestudie die werd uitgevoerd door de afdeling Neurowe-
tenschappen van het Erasmus MC en Koninklijke Visio. Dit heeft recent geleid
tot de implementatie van het gebruik van de eye tracker bij onderzoeken in
SNL
de klinische praktijk bij Koninklijke Visio. De samenwerkende onderzoekers
van de afdelingen Geneeskunde voor Verstandelijk Gehandicapten en Neuro-
wetenschappen van het Erasmus MC sloegen een nieuwe weg in door ook een
andere neuropsychologische tests, namelijk een Gestalt-perceptie taak, zoals
beschreven in Hoofdstuk 9, te onderzoeken met de eye tracker.
Maar voordat deze taken kunnen worden toegevoegd aan het routine
diagnostisch onderzoek in visuele revalidatie- en adviescentra, moeten de
bijbehorende normaalwaarden beter worden onderzocht in grote groepen
kinderen. Dat is dus onze belangrijkste aanbeveling voor verder onderzoek.
Dit zal samenwerking van onderzoeksgroepen vergen, eventueel internatio-
naal. Op dit moment werken professionals van de Vestibulaire en Oculomotore
234 Samenvatting
Het is zover! Ik heb toestemming voor het drukken van dit proefschrift, dus
het einde van het promotietraject is in zicht. “Eindelijk!”. Ik zal vast niet de
enige zijn die dit denkt. Het is een lang traject geweest met zo z’n ups en z’n
downs en velen van jullie hebben op een of andere manier een deel van deze
reis met mij meegemaakt.
Allereerst dank aan alle deelnemende kinderen. Dank jullie, dat jullie mee
wilden doen! Meedoen was voor de een gemakkelijker dan voor de ander:
soms ging alles goed, soms ontdekte je dat je iets niet zo goed kon. De een
kon er dan nog om lachen, de ander werd er verdrietig of boos van. Toch bleef
iedereen meedoen. Ik heb bewondering voor jullie doorzettingsvermogen.
Dank dat ik van jullie mocht leren en dat ik dat weer mag delen met anderen.
Natuurlijk ook dank aan de deelnemende ouders en medewerkers van de
deelnemende scholen: Eduard van Beinum, Openbare basisschool Charlois, De
Bergse Zonnebloem, Visio-school. Dank ook aan de organisaties die bij mijn
onderzoek betrokken waren: Rijndam Revalidatiecentrum, Koninklijke Visio en
Erasmus MC. Zonder jullie had ik dit onderzoek en het proefschrift niet van de
grond gekregen en had ik veel kennis en ervaring niet op kunnen doen.
Ook ben ik veel dank verschuldigd aan Prof.dr. Heleen Evenhuis. Heleen,
zonder jouw initiatief, coaching, geduld, en eindeloze vertrouwen in mijn mo-
gelijkheden had ik deze wetenschappelijke en persoonlijke reis niet kunnen
maken en afronden. Jij trok de conclusie dat ook onderzoek naar Cerebrale
Visuele Informatieverwerkingsproblemen (CVI; Cerebral Visual Impairment)
van belang is. Door de samenwerking met Annemieke Blokker, destijds regio-
directeur van Koninklijke Visio, verbond je de wetenschap, vanuit de leerstoel
Geneeskunde voor Verstandelijk Gehandicapten bij het Erasmus MC, met de
praktijk van Koninklijke Visio en kreeg ik de kans die ik zocht: werken in het
veld van de neuropsychologie en het kunnen combineren van wetenschap
en praktijk. Deze combinatie is niet altijd gemakkelijk gebleken, maar was
D
zeker interessant en leerzaam. Dank voor het feit dat je bleef zoeken naar
alternatieve mogelijkheden, je concrete feedback en de tijd, die je ook na je
pensioen voor me vrij hebt gemaakt.
De inhoud van mijn onderzoek heb ik grotendeels te danken aan de voortrek-
kers in het internationale en nationale veld van de visuele neuropsychologie
en neurologie. In het bijzonder dank aan Dr. Peter Stiers. Dank je, Peter, dat je
me de eerste jaren van het traject hebt willen begeleiden. Ik heb fijne herin-
neringen aan onze inhoudelijke discussies en mijn bezoeken aan Leuven en
Maastricht. Dank, dat je jouw verzamelde data en het testmateriaal dat door
jou en jouw studenten ontwikkeld is, beschikbaar hebt gesteld voor nader
onderzoek. Ook wil ik o.a. de managers, collega-gedragswetenschappers,
238 Dankwoord
mij voor het eerst gedicht en werd het zaadje geplant dat wetenschappelijk
onderzoek ook wel iets voor mij zou kunnen zijn. Dank jullie voor de gezellige
en leerzame periode!
Werken en leren is het leukst in een omgeving met een warme belangstel-
lende sfeer. Wat heb ik toch veel fijne mensen om me heen! Beste (oud-)
collega’s van de Leerstoel Geneeskunde voor Verstandelijk Gehandicapten,
Huisartsgeneeskunde en van Koninklijke Visio en meiden van de GZ-oplei-
dingsgroep GZ17-E, dank voor jullie steun, lieve en motiverende woorden en
de benodigde afleiding als ik even geen zin had om met mijn promotietraject
bezig te zijn.
Lieve heit en mem, lieve familie en vrienden. Ik weet het, ik ben een eeu-
wige student. Ik zit vaak met mijn neus in de boeken, artikelen of werk aan
opdrachten en artikelen. Tijd en energie zijn net als geld, je kunt ook tijd en
energie maar 1x besteden, helaas. Dit had regelmatig tot gevolg dat ik jullie
minder vaak zag en sprak, dan dat ik zou willen. Wat heb ik genoten van het
samen zijn, de gesprekken, de lekkere kopjes thee, het samen lekker eten,
puzzelen, naar de film of theater gaan en uitwaaien. Tussendoor waren er de
gezellige telefoontjes, lieve kaartjes en appjes. Dank jullie wel hiervoor! Ho-
pelijk komt er met het afronden van dit traject een zee van tijd vrij, waardoor
we weer vaker samen kunnen genieten.
Lieve Bionka en Sjoukje, dank dat jullie mijn paranimfen willen zijn, me bij
willen staan bij het verdedigen van mijn proefschrift. Dank voor jullie hulp bij
de voorbereidingen, het meelezen en de gezelligheid.
Last but not least, lieve Roelof, vrijheid en onszelf verder ontwikkelen staan
hoog in ons vaandel. Dank voor de ruimte die je me hiervoor geeft. En wat
is het fijn om dit niet alleen te doen. Ik waardeer dat je mij achterna bent
gekomen en gezellig bij mij in Rotterdam bent komen wonen. Dank voor de
lieve zorg als ik weer eens geen puf meer had, de gezellige uitjes, de fijne
D
wandelingen en fietstochten in binnen- en buitenland. Ik hoop dat we nog lang
samen mogen genieten!
About
About the
the author
author
About the author 243
th
Ymie van der Zee was born on December 26 , 1978 in Oosterwolde (FRL),
the Netherlands. She finished her pre-university education at the CSG Liudger
in Drachten in 1998. That same year, she started as a student Psychology
at the Rijksuniversiteit Groningen. In 2000 she visited Iceland to combine a
vacation with a short introduction in clinical psychology in a hospital in Reyk-
javik (Sjúkrahús Reykjavíkur). After writing a master thesis titled “Parkinson’s
Disease: questionnaire-based research on sensation seeking combined with
experimental research on stimulus novelty effects in EEG-recordings”, she
started a six months traineeship at ‘Kind & Adolescent’, a university psycho-
logical centre in Ghent, Belgium. In 2003 she finished her study in psychology
with two majors, Clinical Psychology and Methodology, and two minors Neuro-/
Biopsychology and Developmental psychology. During the summer breaks of
2002 and 2003, and in 2004 till February 2005 she worked as professional
caregiver in a residential care centre for people with an intellectual disability
and additional problems like Borderline personality disorder and Gilles de la
Tourette (Talant, Beetsterzwaag, The Netherlands).
In February 2005 she started her PhD track on Cerebral Visual Impairment
(CVI), which started out as a collaborative effort of the Department of Intel-
lectual Disability Medicine of the Erasmus MC, Rotterdam, The Netherlands,
Royal Dutch Visio, Dutch Centre of Excellence for visually impaired and blind
people, The Netherlands and the Laboratory of Neuropsychology of the K.U.
Leuven, Belgium (later Department of Neuropsychology & Psychopharmacol-
ogy, University Maastricht, Maastricht, The Netherlands). The last years the
collaboration with Vestibular and Ocular Motor Research Group, Department of
Neuroscience, Erasmus MC, Rotterdam, the Netherlands intensified.
Results of these collaborations can be found in this doctor thesis, titled:
“Diagnosing Cerebral Visual Dysfunctions in Children: looking beyond Visual
Acuity and Visual Field”.
cv
Since 2010 she is mainly working as neuropsychologist at Royal Dutch Vi-
sio. She worked in multiple teams and focusses on children with and without
intellectual disabilities or brain damage. In 2017 she started her postmaster
education to obtain the registration as health psychologist (Gezondheidszorg-
psycholoog) to improve her clinical skills and combine research and clinical
practise in the future.
PhD
PhD Portfolio
Portfolio
PhD Portfolio 247
General courses
Master class ‘Improving your clinical research’ 2006
Methodologie van patiëntgebonden onderzoek en voorbereiding van subsidieaanvragen 2006
Statistiek in de kliniek, basisgebruik SPSS 14 2007
Specific courses
Paediatric Clinical Epidemiology (Erasmus Winter programme) 2006
International Classification of Functioning, Disability and Health (ICF; Koninklijke Visio) 2007
Active Memory; Pathways through the Brain in Memory and Action (NWO Cognition 2006
Summer School, Doorwerth; Poster presentation)
Kinderoogheelkunde (Boerhaave Nascholing, Leiden; Attendance and oral presentation) 2015
Presentations
Fine scale functional organization of the human ventral stream (Helmholtz lecture) 2006
Space and the parietal cortex (Helmholtz lecture) 2006
Functional Magnetic Resonance Imaging of Human Visual Cortex (Helmholtz lecture) 2007
Learning to see late in life (Lecture Erasmus MC) 2014
Video Interaction Guidance – Light version (Koninklijke Visio) 2015
Afscheidscollege Prof. Dr. Heleen Evenhuis. Van ontginnen naar oogsten. 15 jaar 2015
epidemiologisch onderzoek bij mensen met verstandelijke beperkingen (Erasmus MC)
(Inter)national conferences/Seminar
Kennis InZichtelijk: Hoe gebruik ik kennis om mijn werk met mensen met een visuele 2005
beperking te professionaliseren? (ZonMW InZicht; Attendance)
Bridging research, policy and practice (E-IASSID Congress, Maastricht; Oral 2006
presentation).
Brain Days: functional response to cerebral damage & development and adaptation of 2006
structure and function (Attendance)
VOGG (Vereniging voor ouders en verwanten van mensen met een verstandelijke 2007
handicap) Symposium. (Lelystad; Oral prestentation) P
Focus op onderzoek. Wetenschappelijk onderzoek ten behoeve van (de zorg aan) 2007
mensen met een verstandelijke beperking. (Kennisplein Gehandicaptensector en
ZonMw, Amsterdam; 2 oral prestentations)
Cognitieve revalidatie (ZonMw consortium Cognitieve Revalidatie; Attendance) 2007
Technologie en communicatie in het leven van mensen met een visuele beperking 2007
(Attendance)
Voortgang In Zicht (ZonMW InZicht; Attendance) 2007
10 jaar InZicht: een decennium innoveren en implementeren (ZonMW InZicht; 2008
Attendance)
IASSID Congress, Cape Town, South Africa (Oral presentation) 2008
InZicht Oogopslag (ZonMW InZicht; Attendance) 2010
Vroeghulpsymposium. Terugkijken & Vooruitzien (MEE - Integrale Vroeghulp Rotterdam; 2015
Attendance)
248 PhD Portfolio
2. Teaching Year
Lecturing
Guest Lecturer at ID physician training 2008
Regional meeting for orthoptists. Rotterdam 2008
Meeting for personnel of a rehabilitation center. Rotterdam 2008
Meeting for physicians of child health care centers. Rotterdam 2008
Meeting for personnel of special schools for blind and visually impaired children 2008 and
later
Supervising Master’s theses
Apiradee Poungjit. Master thesis Clinical Neuropsychology. Relation of Crowding Effect and 2009
Visual Search in Children: Comparison between children with a high risk of cerebral visual
impairment and normal children.
Suzanne Ton. Master thesis Clinical Neuropsychology and Child & Adolescent Psychology. 2010
Cerebral Visual Impairment in Children. A pilot study on motion perception in children with
cerebral damage and children without cerebral damage.
Jeanne van der Wulp. Master thesis Clinical Neuropsychology. Using eye movements to 2017
predict reading skills in children. An eye tracking study while reading aloud a narrative
Marisabel Talamante Ojeda. Master thesis in Neuroscience and Behavioral Biology. 2017
Perception tests in children with visual impairments: an eye movement approach
A digital version of this thesis is available at
https://epubs.ogc.nl/?epub=y.vanderzee