Neuropsychologia 84 (2016) 89–104

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Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Longitudinal study of preterm and full-term infants: High-density EEG

analyses of cortical activity in response to visual motion
Seth B. Agyei n, F.R. (Ruud) van der Weel, Audrey L.H. van der Meer
Developmental Neuroscience Laboratory, Department of Psychology, Norwegian University of Science and Technology, NTNU, Norway

art ic l e i nf o a b s t r a c t

Article history: Electroencephalogram (EEG) was used to investigate brain electrical activity of full-term and preterm
Received 25 July 2015 infants at 4 and 12 months of age as a functional response mechanism to structured optic flow and
Received in revised form random visual motion. EEG data were recorded with an array of 128-channel sensors. Visual evoked
14 January 2016
potentials (VEPs) and temporal spectral evolution (TSE, time-dependent amplitude changes) were ana-
Accepted 3 February 2016
Available online 4 February 2016
lysed. VEP results showed a significant improvement in full-term infants' latencies with age for forwards
and reversed optic flow but not random visual motion. Full-term infants at 12 months significantly
Keywords: differentiated between the motion conditions, with the shortest latency observed for forwards optic flow
EEG and the longest latency for random visual motion, while preterm infants did not improve their latencies
Infants
with age, nor were they able to differentiate between the motion conditions at 12 months. Differences in
Prematurity
induced activities were also observed where comparisons between TSEs of the motion conditions and a
Motion perception
Optic flow static non-flow pattern showed desynchronised theta-band activity in both full-term and preterm in-
Random motion fants, with synchronised alpha-beta band activity observed only in the full-term infants at 12 months.
Visual motion Full-term infants at 12 months with a substantial amount of self-produced locomotor experience and
Visual perception neural maturation coupled with faster oscillating cell assemblies, rely on the perception of structured
Locomotion optic flow to move around efficiently in the environment. The poorer responses in the preterm infants
Self-motion could be related to impairment of the dorsal visual stream specialized in the processing of visual motion.
VEP
& 2016 Elsevier Ltd. All rights reserved.
TSE
Time-frequency analysis
ERP

1. Introduction
Most daily activities including social interactions and cognitive
skills such as object categorisation, reading, and navigating
through the environment depend on perception and correct in-
terpretation of visual information. Considering the relevance of
these abilities to everyday life, it is important to understand the
developmental processes underlying how infants learn to make
use of relevant visual information for perception.
During daily activities, it is important to recognise the land-
marks in the environment and their egocentric positions in de-
fining how relative an object's position is to an observer and vice
versa (Wall and Smith, 2008; Warren, 1976). The concept where
major images emanate from a central point in a structured form
within the angle of sight when there is a change of scenery either
by locomotion in any direction or as an object approaches an ob-
server is referred to as radial optic flow (Gibson, 1979). The visual
motion perception that is achieved by this change is crucial for
adjusting posture (Vaina and Rushton, 2000), perceiving time-to-
n
Corresponding author.
contact (Kayed and Van der Meer, 2009), avoiding obstacles
(Turano et al., 2005; Wilkie and Wann, 2003), and reaching a
target efficiently by determining heading direction (Lappe et al.,
1999). The relation between optic flow perception and action has
often been studied in terms of motor activities (e.g., Bruggeman
et al., 2007). It has been shown that perception of optic flow plays
a major role in the control of walking speed and direction (Brug-
geman and Warren, 2010; Lamontagne et al., 2007; Vilhelmsen
et al., 2015; Warren et al., 2001). The estimation of speed in order
to effectively reach a target is achieved by integrating inputs from
the visual system with locomotor variables (Saleem et al., 2013).
Improvement in visual perception by actual motor learning
through action-to-perception transfer has been reported in adults
(Beets et al., 2010). Young infants, on the other hand, are not as
efficient as adults in detecting optic flow (Gilmore et al., 2004,
2007; Van der Meer et al., 2008).
Rudimentary perception of optic flow patterns appears within
the first weeks and months after birth (Gilmore et al., 2004), with
adults able to readily distinguish between expansion/contraction,
rotational, and translational (horizontal/vertical) forms of motion
(Gilmore et al., 2007). Behaviourally, infants younger than a month
of age exhibit defensive responses such as backward head tilting

http://dx.doi.org/10.1016/j.neuropsychologia.2016.02.001
0028-3932/& 2016 Elsevier Ltd. All rights reserved.
90 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
and frequent eye blinking in reaction to structured motion, with
even neonates as young as 3 days old observed to exhibit re-
sponses through backward head movements when exposed to
backwards flow stimuli (Jouen et al., 2000; Shirai and Yamaguchi,
2010). These defensive behavioural responses in very young in-
fants, however, have been interpreted to be the result of multi-
modal integrative and cooperative processes in which visual,
vestibular, and proprioceptive senses are involved rather than a
direct consequence of motion perception (Jouen et al., 2000).
Further studies using electroencephalogram (EEG) have shown
that infants younger than 6–8 weeks do not discriminate between
motion directions and do not smoothly pursue small moving ob-
jects but such abilities improve rapidly around 6–14 weeks after
birth (Rosander et al., 2007). These motion patterns show unique
developmental trends with age in infants (Shirai and Yamaguchi,
2010). Here, perception of translational motion emerges at ap-
proximately two months of age whereas perception of radial
motion and its cortical responses develop rapidly afterwards from
just before 3 months until approximately 4 months of age (Shirai
and Yamaguchi, 2010). However, this fast perceptual development
starts decelerating after the first few months but approaches adult
level around 4 years of age (Kaufmann, 1995).
Various brain studies in humans and other primates have in-
vestigated the cerebral networks specialized for perception of vi-
suo-spatial information (for review, see Shirai and Yamaguchi
(2010)). In particular, perception of movement control including
self- and object-motion is processed via the dorsal visual stream
(see Creem and Proffitt (2001)). Neurons within the medial tem-
poral (MT/V5þ ) complex are generally sensitive to radial motion
processing, with the dorsal medial superior temporal (dMST) area
involved specifically in optic flow processing (Creem and Proffitt,
2001; Duffy and Wurtz, 1991; Dukelow et al., 2001; Fukushima,
2008; Greenlee, 2000; Imura et al., 2008; Itoh et al., 2005;
Newsome and Pare, 1988; Riecansky, 2004; Smith et al., 2006;
Tohyama and Fukushima, 2005; Wall et al., 2008).
The human brain is an organised dynamic network of inter-
connected neurons and associated synapses that work together
such that dysfunctions within the network can have adverse ef-
fects on behavioural patterns. Magnetic resonance imaging (MRI)
studies show that being born preterm causes differential brain
development that leads to abnormalities in the microstructure of
tissues and in cerebral morphology (Counsell and Boardman,
2005; Counsell et al., 2006). Premature birth with its continuously
increasing incidence (Martin et al., 2003, 2013) has therefore been
given considerable attention over the years. Some of the dys-
functions of preterm birth have been related to cognitive and
behavioural impairments (Aarnoudse-Moens et al., 2009; Bhutta
et al., 2002; De Jong et al., 2012; Delobel-Ayoub et al., 2009;
Johnson, 2007; Salt and Redshaw, 2006) including deficits in visual
perception and other neurodevelopmental disorders (see De Jong
et al. (2012)).
Some studies have reported deficit in motion and form per-
ception in premature children that was either a consequence of
being born preterm (MacKay et al., 2005; Taylor et al., 2009) or a
result of the accompanying periventricular leukomalacia (PVL)
(Downie et al., 2003; Jakobson et al., 2006). Using behavioural
experiments, further studies have shed more light on the deficit in
motion and form perception where differences between global
motion (optic flow) perception and form perception have been
found (Guzzetta et al., 2009). They reported that preterm children
with and without brain damage appeared to perform worse than
full-term controls in global motion perception, with PVL preterm
infants performing worse on form perception than preterm infants
without PVL (Guzzetta et al., 2009). These observations suggested
impairment of the dorsal stream during visual processing in pre-
term children with and without brain damage. In four cohort
studies in which several assessment techniques were used and the
correlations between the results and MRI indicators of brain ab-
normalities were analysed, it was also pointed out that the im-
pairment of the visual dorsal stream is a possible cause for the
cluster of developmental problems seen in children born prema-
turely (Atkinson and Braddick, 2007). These findings are further
supported by other studies where global motion, global form, and
biological motion (combination of cues for form and motion)
perception were compared in preterm children (e.g., Taylor et al.,
2009). Global motion perception deficit was observed more den-
sely than global form deficit, and difficulties in biological motion
perception were also present (cf., Atkinson et al., 2008b). Further
studies (e.g., Van Braeckel et al., 2010) that investigated the motor
skills of preterm children of 7–11 years report that they perform
less accurately or slower in movement pointing tasks, implying
less efficient elementary visuomotor processing and impaired
functioning of the dorsal visual stream. Other studies with the aim
to help detect early brain damage in premature infants have fur-
ther formulated specific markers of visual cortical function in the
first postnatal months for both normally and atypically developing
infants (Atkinson et al., 1992, 2008a,; Braddick et al., 1992, 2005).
Such studies showed that the severity of detected brain injury in
preterm infants was correlated with impaired orientation-reversal
visual event-related potentials and the cortical control of visual
attention through fixation shifting. These studies also showed
preterm infants to display worse performances on given cortical
tests compared to full-term infants.
During visual perception tasks, EEG primarily records electrical
activities of pyramidal neurons with high temporal resolution (in
the millisecond scale) that permits the study of the neuronal basis
of motion perception and the functional specialisations of cortical
structures (Agyei et al., 2015; Dukelow et al., 2001; Sakkalis et al.,
2008; Tucker, 1993). Motion-sensitive visual evoked potential
(VEP) waveforms in EEG are thought to originate from V5/MT þ in
occipital and parietal visual areas (Kobayashi et al., 2004; Wall
et al., 2008), and are characterized by a negative N2 peak com-
ponent that occurs around 270–290 ms post stimulus in 11–12-
month-old infants (Agyei et al., 2015) and around 130–200 ms in
adults (Fielder et al., 1983; Heinrich et al., 2005). Previous studies
reported the N2 visual component in infants to be longer in la-
tency and higher in amplitude compared to adults (Van der Meer
et al., 2008), with the longer N2 latencies improving with infants'
age (Agyei et al., 2015). Other studies of early visual N1, P1 and P2
components (e.g., Fielder et al., 1983; Hammarrenger et al., 2007)
have shown similar results where latencies were observed to de-
crease as children became older.
In addition to the use of VEPs in EEG studies, investigation of
neural activities in the time-frequency domain has allowed for the
study of cognitive and perceptual functions through observations
of the natural frequencies in EEG (Agyei et al., 2015; Basar et al.,
1999; Formaggio et al., 2010; Ganzetti and Mantini, 2013; Salari
et al., 2012). Analyses in the time-frequency domain permit the
extraction of event-related frequency changes in EEG that cannot
be observed in VEPs by using averaging techniques. These fre-
quency changes are observed as event-related (de)synchronisation
(ERD/ERS) oscillatory activities that represent decreases/increases
in amplitude/power of specific frequency bands (Pfurtscheller and
Lopes da Silva, 1999), an indication of decrease/increase in syn-
chrony of the underlying neuronal populations (Hoechstetter et al.,
2004; Pfurtscheller et al., 1994). Based on spectral profiles within
specific frequency bands, different classes of oscillations have been
distinguished over the years: delta-band (1–4 Hz), theta-band (4–
7 Hz), alpha-band (7–13 Hz), beta-band (13–30 Hz), and gamma-
band (30–150 Hz), with these rhythms shown to reflect neuro-
physiological processes that manifest functionally different roles
(Buzsaki and Draguhn, 2004; Engel and Fries, 2010; Ganzetti and
 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
Mantini, 2013; Saby and Marshall, 2012). For example, while delta-
band oscillations play a role in processes such as signal detection,
event-related oscillations in the theta-band have been reported to
play an important role in cognitive processes (Başar et al., 2000;
Freunberger et al., 2011; Gruber and Müller, 2006; Khader et al.,
2010; Klimesch et al., 1996). Event-related synchronisations in the
alpha-band may reflect control of inhibition and cortical proces-
sing (Doppelmayr et al., 1998, 2005; Freunberger et al., 2011; Kli-
mesch, 1999; Klimesch et al., 2007; Sauseng and Klimesch, 2008).
Further studies with visual stimuli (e.g., Wróbel, 2000) have linked
beta oscillatory responses to multisensory stimulation and the
shifting of neural systems to a state of attention that ultimately
allows for gamma synchronization and the utilisation of the re-
sulting information for perception (Herrmann et al., 2004, 2010).
Particularly in infants, low-frequency oscillations especially in the
theta-alpha range undergo systematic development from early
childhood to adulthood (Stroganova and Orekhova, 2007; Stroga-
nova et al., 1999). These low-frequency rhythms in infants have
been attributed to general signs of immaturity (Orekhova et al.,
2006; Stroganova and Orekhova, 2007). Recent infant studies have
implicated low-amplitude desynchronised theta-band activities
over visual areas when motion stimuli were compared with static
stimuli (Agyei et al., 2015; Van der Meer et al., 2008), with further
observation of high-amplitude activities especially in alpha-band
frequency observed in one-year-old infants (Agyei et al., 2015).
This transition of EEG spectral power/amplitudes from lower to
higher frequencies during development is considered a sign of
maturation in various psychophysiological studies (Hudspeth and
Pribram, 1992; Stroganova et al., 1999).
The present study explores the development of the visuo-
cognitive systems, especially visual motion perception during early
infancy. The study presents information that contributes to the
understanding of the normal development of visual motion per-
ception in infants and the developmental impairments associated
with motion perception in preterm birth. Using EEG longitudinal
data, the paper compares preterm and full-term infants at the ages
of 4 months and 12 months through a combination of VEP and
time-frequency analyses. VEPs were assumed to represent re-
sponses of cortical neurons to changes in afferent activity (Brecelj,
2003; Van der Meer et al., 2008), while event-related time-fre-
quency responses represent interactions of local cortical neurons
that control the frequency components of an ongoing EEG
(Pfurtscheller and Lopes da Silva, 1999). It was expected that
perception of optic flow would rapidly improve with increasing
age especially in the full-term infants, with no such marked im-
provement in perception of random visual motion, and that low-
frequency decrease in amplitudes would generally be observed.
2. Methods
2.1. Participants
Twenty full-term and preterm normally developing infants
were recruited for the study through birth announcements, con-
tact with parents and/or through the Neonatal Intensive Care Unit
at St. Olav's University Hospital in Trondheim. The full-term in-
fants had mean gestational age of 39.9 weeks (SD ¼ 0.9, med-
ian ¼39.6, range¼38.4–41) and mean birth weight of 3693 g
(SD ¼628, median ¼3500, range¼3085–5120). The preterm in-
fants (moderate to very preterm) were born at mean gestational
age of 31.4 weeks (SD ¼1.8, median¼ 31.4, range¼28.4–33). Their
mean birth weight was 1622 g (SD ¼ 453, median ¼1530,
range¼1000–2670). The preterm infants did not have any major
neurological deficits including severe brain damage, retinopathy of
prematurity (ROP) and other perinatal issues requiring serious
91
medical interventions that may lead to abnormal development.
Infants were tested at 4 months and later at 12 months using a
longitudinal design. One preterm infant was excluded from the
study for presenting inadequate data for analysis at 12 months
since he became very uncomfortable early on in the testing. Hence,
one full-term infant was also excluded from further analysis. Thus,
longitudinal analyses were performed on 18 infants in total for
both testing sessions (full-term: 5 girls, 4 boys; preterm: 3 girls,
6 boys).
For the first testing session, the mean age of the preterm in-
fants was 4 months and 26 days (SD ¼ 6.9) with a range of 139–158
days, and the mean age of the full-term infants was 4 months and
16 days (SD ¼ 21.3) with a range of 111–164 days. Infants at the first
testing session had no experience with self-locomotion. For the
second session, mean age was 12 months and 18 days (SD ¼ 18.6)
with range 356–414 days for preterm infants, and 11 months and
20 days (SD ¼13.9) with range 333–371 days for the full-term in-
fants. Preterm ages were corrected for prematurity. All infants
could crawl and independently pull to stand or walk with help at
the time of the second testing session except three preterm infants
who had not started crawling or pulling to stand and were bot-
tom-shuffling instead (parental report and observation).
Electroencephalography is a physiological procedure that is
known to have no painful or harmful effects on participants. Par-
ents gave their informed consent prior to the experiment and had
the right to withdraw from the testing at any time before or during
the experiment. The Norwegian Regional Ethics Committee and
the Norwegian Data Services for the Social Sciences approved the
study.
2.2. Experimental stimuli and paradigm
Stimuli were programmed using E-Prime (Psychological soft-
ware tool) and mirror-reversed projected by an ASK M2 projector
onto a wide white screen (1.1 m  0.8 m) at a visual angle of 68°
horizontal by 47° vertical. Image resolution was 593 pixels per
metre at a refresh rate of 60 Hz. The screen was placed at a dis-
tance of 80 cm from the infant (see Fig. 1). To discriminate be-
tween coherent and incoherent radial motion, three conditions, i.e.
forwards optic flow, reversed optic flow, and random visual mo-
tion, as well as a static non-flow condition, were used. Each con-
dition consisted of 100 black dots (5 mm virtual radius) that were
randomly positioned on the screen. Each condition was presented
for 1.5 s, with stimulus contrast around 99.5% and mean lumi-
nance at 68 cd/m2. In the motion conditions, dot particles moved
at a constant rate of 30 mm per frame at 60 fps such that they
moved inwards and towards or outwards and away from a central
fixation point, 1.69 mm in diameter, that subtended an angle of
0.16° at the centre of the screen. Dot particles appeared small
when far away from the eye in virtual space or large when closer
to the eye as they decreased or increased in size at a rate of 0.025
pixel per pixel with reference to the central fixation point. Sizes of
dot particles that appeared on the screen ranged from 2 mm to
17 mm in radius.
In the forwards optic flow condition, dots moved coherently
towards the infant where movement was parallel to the z-axis
towards the eyes with zero velocity in the x- and y-axis. The re-
versed optic flow condition had similar properties as the forwards
optic flow condition except that the coherent movement of dots
was in the opposite direction and away from the infant. In the
random condition, dot particles moved incoherently in random
directions in virtual space but with similar properties as stated
above. For the static condition, however, dot particles had zero
velocity in all directions and remained in the same position on the
screen for the entire duration of a trial. The order of presentation
of the stimuli was random, with the static condition always
92 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
Fig. 1. Experimental set-up: actual appearance of the experimental room with a
12-month-old infant sitting in a baby car seat and the 128-sensors placed on his
head. The parent appears on the right side and the assistant on the other side of the
infant. Moving dots simulating optic flow and random motion appear on the large
screen in front of the infant. The eye tracker is on the desk in between the infant
and the screen.
appearing in between successive presentations of the motion
conditions in order to avoid motion adaptation.
Stimuli were presented as a uniform dot distribution to avoid
accretion of dots at the centre or edges of the screen. Particles that
moved outside the range of sight on the screen were automatically
resized and repositioned on the screen where all particles in each
motion condition had an equal probability of placement.
2.3. Data acquisition
EEG activity was recorded with a Geodesic Sensor Net (GSN)
200 (Tucker, 1993; Tucker et al., 1994). The net consisted of an
array of 128 Ag/AgCl sensors that were evenly distributed on the
infant's head. A high-input EGI amplifier was connected to the
GSN 200 to ensure signals were amplified with maximum im-
pedance set to the recommended value of 50 kΩ for optimal sig-
nal-to-noise ratio (Budai et al., 1995; Ferree et al., 2001; Picton
et al., 2000). Amplified signals were recorded with Net Station
software on a Macintosh computer and sampled at 500 Hz. Tobii
X50 camera was used to track the gaze of the infants, with the
visual feed processed by ClearView software on an HP computer.
Two additional cameras positioned at different angles in front of
the infants were used to record digital videos to track the beha-
viour of infants during the experiment. Recorded data were sub-
sequently stored for offline analyses.
2.4. Procedure
Parents signed the consent form when they arrived with their
infant prior to the experiment. The infant was then allowed time
to get used to the laboratory surroundings by playing with toys
and generally exploring the new environment. In the process, an
assistant measured the infant's head circumference to allow for
the correct size selection of the GSN 200. To optimise electrical
conductivity of the net, it was immersed in a saline electrolyte
solution and partially dried before being mounted on the infant's
head while the infant was seated on the parent's lap. Distractors
such as colourful soap bubbles and small sounding toys were used
to attract the infant's attention from the net as it was being
mounted. Immediately after mounting the net, the infant was
moved into a dimly lit experimental room while other assistants
moved to the control room to manage the computers necessary for
data acquisition. A glass partition that was both soundproof and
transparent separated the control room from the experimental
room. The infant either sat on the parent's lap for the first testing
session or in a baby car seat during the second testing session
while positioned in front of the screen, with the parent in close
proximity (Fig. 1). The impedance of the electrodes was then
checked with the net connected to the amplifier, while electrode
contact was improved if necessary. An assistant was present in the
experimental room to help the infant focus on the screen and to
monitor the experiment, while the parent was present for the
entire duration of the experiment to avoid any stressful effect an
absent parent may have on the infant.
The experimental session immediately began after calibrating
the infant's eye movement in virtual space to the Tobii X50 cam-
era. The session started with the optic flow experiment followed
by two other visual motion experiments. The optic flow experi-
ment lasted between 5 and 7 min. From 80 to 120 trials were
presented per infant, where approximately half of those were
static non-flow trials. Data acquisition was carried out in one block
but when an infant showed signs of boredom or disinterest, the
session was paused in order for the assistant and/or parent to
revive the level of interest by playing with the infant for a short
period before resuming the presentations. An experimental ses-
sion ended if an infant showed considerable level of disinterest,
fussiness, or tiredness.
2.5. Data analysis
EEG data were analysed with Brain Electrical Source Analysis
(BESA) research software version 6.0 and BESA statistics 1.0 (BESA
GmbH). In the initial pre-processing step, EEG recordings were
segmented with the Net Station software and exported as raw files
for further offline analyses. Appropriate auxiliary files containing
trigger and sensor information were imported and attached.
Epochs around the triggers of stimuli were set with averaging
epoch at  200 to 800 ms at a baseline definition of 100 to 0 ms.
To remove slow drift in the data, high-pass filter was set at 1.6 Hz.
Low-pass filter was at 60 Hz while notch filter was set at 50 Hz to
remove lines interference from the recorded data. By visual in-
spection together with the visual feed from the eye-tracker, arte-
fact-contaminated channels and epochs resulting from head or
body movements as well as instances where infants were not
looking at the screen were excluded from further analyses or the
data interpolated where necessary. In scanning for artefacts,
threshold values for gradient and low signal were set at 75 μV and
0.1 μV, respectively, while maximum amplitude was set at 200–
230 μV. Physiological artefacts from activities such as blinking and
eye movements (Lindsen and Bhattacharya, 2010; Pham et al.,
2011) were corrected from the data using manual and semi-au-
tomatic forms of artefact correction that were designed to separate
brain activities from artefacts using appropriate spatial filters
(Berg and Scherg, 1994; Fujioka et al., 2011; Ille et al., 2002; Shao
et al., 2009).
The mean numbers of accepted motion trials for full-term in-
fants at 4 months and 12 months were 43 (SD ¼ 4.9, range¼31–66)
and 42 (SD ¼ 4.8, range¼31–72), respectively, while those for
preterm infants were 46 (SD ¼4.9, range¼27–73) and 40 (SD ¼2.8,
range¼ 31–48) at 4 months and 12 months, respectively. Trial
numbers were more or less evenly distributed across the three
motion conditions. The static control condition had mean numbers
of accepted trials of 48 (SD ¼13.1), 48 (SD ¼ 18.1), 50 (SD ¼17.1),
and 40 (SD ¼6.6) for full-term infants at 4 months, full-term in-
fants at 12 months, preterm infants at 4 months, and preterm
infants at 12 months, respectively.
 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
VEP peak analysis was carried out using individual averages.
Individual averages were obtained for each infant by averaging
individual data over whole EEG continuous file and interpolating
to the standard 81-electrode configuration of the international 10-
10 standard electrode system by re-referencing to an artificial re-
ference calculated from the average potentials over the scalp. The
individual averages for infants in each of the testing sessions were
combined into grand averages for each session. Grand average
VEPs gave approximate time intervals that served as reference
intervals for selecting individual N2 components at different
electrode sites. Further, the N2 components of the VEP waveforms
were identified using 3D spherical spline whole-head voltage
maps of EEG scalp signal distributions that helped to visualise
maximum N2 activity in occipito-parietal areas for the most
dominant VEP waveform. Values for peak latencies and peak am-
plitudes of the individual averages were recorded. Peak latencies
were measured as the time from stimulus onset to the peak of
each scalp N2 component while peak amplitudes represented
maximum amplitudes of the N2 component relative to the pres-
timulus baseline. The values were then subjected to further VEP
analyses.
Time-frequency analysis was performed in brain space using
pre-defined multiple source dipoles that modelled activities in the
visual areas of the parietal and visual cortices. Measuring brain
oscillatory activities using surface electrodes may not be ideal
since scalp waveforms receive mixed contributions from under-
lying brain sources. This is due to the wide distribution of focal
brain activity as a result of the smearing effect of brain volume
conduction in EEG and the nature of dipole fields. Therefore, to
achieve optimal separation of focal brain activities, a source
montage was used. It was obtained using a multiple source model
(Scherg and Berg, 1991; Scherg et al., 2002) where source wave-
forms maximally separated activities from different brain regions.
The source montage consisted of 17 sources that modelled activ-
ities in the visual pathway as well as any residual activities in
other regions of the brain. Of these sources, the visual cortex lat-
eral left (VClL), visual cortex radial right (VCrR) and the parietal
midline (PM) sources (see Fig. 2) that are believed to be active in
the visual processing of motion stimuli (Probst et al., 1993; Van der
Weel and Van der Meer, 2009; Zeki et al., 1991) were further
analysed. To analyse brain activities using these sources, a 4-shell
ellipsoidal head model (Berg and Scherg, 1994; Hoechstetter et al.,
2004; Scherg et al., 2002) with the source dipoles inserted, was
created for each infant where the artefact-corrected coordinate
files were appended. Bone thickness and conductivity were ad-
justed at 3.0 mm and 0.02 s, respectively, as recommended for
infants (Grieve et al., 2003; BESA information). Settings for epoch,
filters and average parameters were the same as in the VEP ana-
lyses. Time-frequency displays showing the change in amplitudes
over time (TSE, temporal spectral evolution) were generated from
single trials by averaging spectral density amplitudes over trials.
Each displayed graph was a plot of spectral amplitude density of
one montage channel over time and frequency normalised to the
baseline for each frequency. Signals from average evoked re-
sponses were removed from the single trial time series before
calculating TSEs in order to have only TSE displays of induced
oscillatory brain activities. Comparisons between the motion
conditions and static non-flow condition were computed. TSE
displays were set to frequency cut-off of 4–40 Hz at frequency and
time sampling of 1 Hz, 50 ms. Frequency cut-off was also adjusted
to further investigate oscillatory activities within the delta and
gamma frequency ranges.
The probability of significance in amplitude values and fre-
quency ranges between the TSEs of the motion conditions and the
static condition for all infants in each testing session was com-
puted using the statistics software. An average of TSE statistics for
93
infants in each testing session was computed such that significant
time-frequency ranges were used as a guide when finding patterns
of oscillatory activities in each infant's TSE displays. The multiple
comparisons problem was addressed using a combination of per-
mutation testing and data clustering technique (see Bullmore et al.
(1999), Ernst (2004) and Maris and Oostenveld (2007)) where data
clusters that showed initial significant effect between conditions
were first defined. These clusters were assigned initial cluster
values comprising of the sum of all t-values of all data points for
each initial cluster. The initial cluster values were then passed
through permutation testing using paired t-test and assigned new
cluster values. The significance of the initial clusters could then be
determined from the distribution of the calculated cluster values
assigned to each initial cluster after permutation. Number of per-
mutations was 512 and frequency cut-offs were the same as stated
above with the significance level for building clusters in time and/
or frequency (cluster alpha) set at 0.005.
Further, comparisons between the motion conditions and static
condition for each infant were performed in order to compute
probability maps to separately test for significant differences in the
TSEs (change in amplitude from baseline to particular time-fre-
quency sampling points) for each individual infant. This allowed
the observation of significant oscillatory activity patterns across
the visual areas of interest for each infant in each testing session
that were not visible in the overall averaged TSEs. To correct for
multiple testing, Bonferroni procedure and permutation tests de-
scribed by Simes (1986) and Auranen (2002) were applied to each
set of time samples belonging to one frequency bin. Frequency cut-
offs and time-frequency sampling points were maintained as sta-
ted earlier.
3. Results
3.1. VEP responses
For each group and each testing session, four posterior elec-
trodes that showed the highest N2 amplitude values in the for-
wards optic flow condition of the grand average VEPs (Fig. 3) were
chosen for further analysis (cf., Agyei et al., 2015; Van der Meer
et al., 2008). The four grand average electrodes for full-term in-
fants at 4 months were PO4, PO3, POz, and O1, and those at 12
months were PO4, PO8, Oz, and O2. The corresponding electrodes
for preterm infants at 4 months were POz, PO4, Oz, and O2, while
the electrodes at 12 months were POz, PO3, Oz, and O1 (Fig. 3).
Latencies and amplitudes of the VEPs were analysed separately
using repeated-measures ANOVAs. Within-subjects factor was
motion condition (forwards optic flow, reversed optic flow, ran-
dom motion) and age (4 months and 12 months), while between-
subjects factor was participant group (full-term, preterm). Latency
values from the electrode with the highest N2 amplitude in the
forwards optic flow condition were used in the ANOVA, with
Bonferroni correction used to adjust for multiple comparisons. The
chosen electrode varied across participants and testing sessions
but was always one of the four mentioned above and was the
same for the three motion conditions in each infant.
The mean N2 peak latency after stimulus onset for forwards
optic flow in full-term infants at 4 months was 426 ms (SD ¼70),
with corresponding values for reversed optic flow and random
motion at 440 ms (SD ¼ 72) and 450 ms (SD ¼80), respectively. At
12 months, mean latency values of full-term infants were reduced
to 277 ms (SD ¼49) for forwards optic flow, 338 ms (SD ¼39) for
reversed optic flow, and 405 ms (SD ¼66) for random visual mo-
tion. N2 mean peak latencies of preterm infants at 4 months for
forwards optic flow, reversed optic flow, and random motion were
325 ms (SD ¼63), 359 ms (SD ¼ 63), and 372 ms (SD ¼64),
94 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
Fig. 2. Head model with associated visual cortical areas VClL (left), PM (middle) and VClR (right). The signal magnitude reflects the estimated source activity in the related
brain region if one brain region is active. The approximate Talairach coordinates of the sources were VClL (x ¼  45, y ¼  57, z¼ 6.5), PM (x¼ 0.0, y ¼  72, z ¼ 37), and VClR
(x¼ 45, y ¼  57, z¼ 6.5).
respectively, while corresponding values at 12 months were
392 ms (SD ¼55), 386 ms (SD ¼ 57), and 378 ms (SD ¼51),
respectively.
For latency, a significant three-way interaction of condition,
age, and group was found, F(2, 32) ¼8.13, p o0.005, indicating that
only the full-term infants at 12 months of age decreased their la-
tencies significantly from random visual motion to reversed optic
flow to forwards optic flow with approximately 60 ms between
each condition (see Fig. 4A). However, the preterm infants did not
differentiate between the three visual motion conditions, neither
at 4 months nor at 12 months. The preterm infants did not de-
crease their latencies with age (Fig. 4A).
Further, a significant two-way interaction of age and group was
found, F(1, 16) ¼27.75, p o0.005, suggesting that irrespective of
visual motion condition and only at 4 months of age, preterm
infants had significantly shorter latencies than full-term infants
(Fig. 4A). The mean N2 latency of forwards optic flow in full-term
infants decreased by about 150 ms from 4 months to 12 months.
However, mean latency of random visual motion decreased around
45 ms for the same age interval in the full-term infants.
Mean N2 peak amplitudes for full-term infants at 4 months
were 7.1 mV (SD ¼3.6) for forwards optic flow, 5.4 mV (SD ¼4.4) for
reversed optic flow, and 4.2 mV (SD ¼2.4) for random motion,
while mean amplitude values at 12 months were 5.7 mV (SD ¼3.8),
2.7 mV (SD ¼1.7), and 0.9 mV (SD ¼2.1) for forwards optic flow, re-
versed optic flow, and random motion, respectively. Preterm in-
fants at 4 months had mean peak amplitudes of 5.2 mV (SD ¼2.6)
for forwards optic flow, 1.4 mV (SD ¼2.2) for reversed optic flow,
and 2.2 mV (SD ¼ 1.9) for random motion, with corresponding va-
lues for preterm infants at 12 months being 4.3 mV (SD ¼3.2),
3.4 mV (SD ¼1.0), and 4.5 mV (SD ¼3.2) for forwards optic flow,
reversed optic flow, and random motion, respectively.
For amplitudes, a significant two-way interaction between age
and group was found, F(1, 16) ¼11.23, p o0.005, implying that
preterm infants showed significantly lower amplitudes than full-
term infants but only at 4 months (see Fig. 4B).
3.2. Individual analysis
Individual analysis was performed on the VEP latency values
for full-term and preterm infants at 12 months considering that
only full-term infants at 12 months showed significant differences
between the motion conditions, with no such differences observed
in the preterm infants at 4 months and even at 12 months. The
individual analysis explored the possibility of finding a criterion
that distinguished the preterm infants that were extremely de-
layed in their VEP responses compared to the other full-term and
preterm infants during the end of the first year of life. Field (2009)
defined an outlier as the value that was smaller or larger than the
mean 7SD*2.5 of a reference value. Using the VEP latency values
of the motion conditions in the full-term infants at 12 months as
the reference for comparison, the criterion showed three preterm
infants L, O, and P to have outlier latency values particularly for
both forwards and reversed optic flow conditions where their VEP
latencies were found to be longer than the mean þ SD*2.5 of the
average VEP latency in the full-term infants at 12 months (Table 1).
Two infants, J and R, also showed outlier latency values but only
for the forwards optic flow condition. None of these preterm in-
fants with outlier values showed delayed motor responses, neither
were they bottom shufflers at the time of the second testing.
 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104 95

Fig. 3. Grand average motion VEPs in full-term infants at 4 months (A) and 12 months (B), and in preterm infants at 4 months (C) and 12 months (D). Amplitudes are on the
y-axis and latencies on the x-axis. The actual N2 peak latencies for forwards optic flow are indicated at PO4 in full-term infants and POz in preterm infants. Differences in N2
peak latencies for the three motion conditions were observed only in full-term infants at 12 months where latency increased from forwards optic flow to reversed optic flow
and random motion. No significant differences between N2 peak latencies were observed between the three motion conditions in full-term infants at 4 months and preterm
infants at 4 and 12 months. N2 peak latencies were also shorter for preterm infants at 4 months than full-term infants at 4 months. (E) The head drawing (nose up) shows
scalp localisation of the 81 standard electrodes with the electrodes of interest indicated with filled black circles (from top to bottom and left to right): PO3, POz, PO4, PO8, O1,
Oz, O2. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

Fig. 4. Group means (and SDs) of N2 peak latencies (A) and amplitudes (B) in full-term and preterm infants. *Significant at p o 0.05, **Significant at p o0.005, ***Significant
at p o0.001.
96 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104

Table 1
VEP latencies (ms) of the visual motion conditions for full-term infants (A–I) and preterm infants (J–R) at 12 months of age. Preterm infants L, O, and P showed latency values
for both optic flow conditions that were larger than mean þSD*2.5 of the average latency values of the corresponding optic flow conditions in the full-term infants.
GA ¼ gestational age in weeks þ days.

Full-term GA Forwards optic Reversed optic Random visual Preterm GA Forwards optic Reversed optic Random visual
infants flow flow motion infants flow flow motion

A 39 þ 5 354 368 456 J 30 484 402 392

B 40 þ 6 236 290 360 K 28 þ 4 318 390 330
C 39 þ 6 284 350 380 L 31 þ 3 456 434 462
D 39 280 350 422 M 32 þ 5 304 288 328
E 41 298 290 420 N 30 þ 6 370 422 374
F 41 220 344 296 O 33 438 442 398
G 39 322 344 438 P 32 þ 3 416 438 384
H 38 þ 4 234 268 340 Q 32 þ 6 374 394 408
I 39 þ 2 310 338 368 R 28 þ 3 400 384 388
Mean 282 327 387
SD 45 35 52
Mean þ (SD*2.5) 394 414 516

3.3. TSE responses
Fig. 5 shows the results of the permutation test displaying the
average for infants in each testing session when TSEs of the motion
conditions were compared with the static condition. The permu-
tation test showed significant negative clusters (suggesting sig-
nificantly smaller values in the motion conditions than static non-
flow condition) in at least one of the visual areas of interest in both
full-term and preterm infants. The visual areas showed significant
negative clusters that appeared to be dominated by activity within
the theta-band range. Theta-band activity was most prevalent and
widespread in full-term infants at 4 months (Fig. 5A) compared to
full-term infants at 12 months (Fig. 5B) and preterm infants at
both 4 months and 12 months (Fig. 5C and D). This prevalent
theta-band activity occurred over relatively longer periods of time
when infants were younger (Fig. 5A and C) compared to shorter
periods of time when infants in each respective group were older
(Fig. 5B and D). Similar TSE results were obtained when TSEs of

Fig. 5. Average visualisation of significant data clusters in the visual sources of interest when the motion conditions were compared with the static non-flow condition in
full-term infants at 4 months (A) and 12 months (B), and preterm infants at 4 months (C) and 12 months (D). Light blue colours represent negative clusters (i.e. motion
condition had smaller t-values than static non-flow) and positive clusters are marked with light red colours (i.e. motion condition had larger t-values than static non-flow).
Significant negative cluster in the visual areas (VClL, PM, VClR) is marked with light blue voxel marks. Each visual area is dominated by activity in the theta-band but over
longer periods of time and more prevalent in the infants at 4 months than those at 12 months for both full-term and preterm infants, with the most prevalent theta-band
activity appearing in the 4-month-old full-term infants. In parentheses are the respective cluster means for motion conditions, cluster means for static non-flow, and the
probability level at which the specific cluster is significant, in that order. Stimulus onset is indicated with a vertical line at 0 ms. Epoch is from  200 ms to 800 ms. (For
interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104 97

Fig. 6. TSE plots (A, B) and the corresponding TSE probability maps (C, D) across brain regions of interest (VClL, PM, VClR) when the motion conditions were compared with
the static non-flow condition in a typical full-term infant at 4 months (A, C) and 12 months (B, D). For the TSE plots, increased spectral amplitude (induced synchronised
activity) is shown as red coloured contours while decreased spectral amplitude (induced desynchronised activity) is shown as blue coloured contours. Induced theta-band
desynchronised activities were observed in all the visual areas of interest in the full-term infants at both ages. Induced alpha-beta band synchronised activities can be
observed in two or more visual areas but only at 12 months (B). For the TSE probability maps, significant increase and decrease of TSEs (p o 0.05) in the motion conditions
compared to the static non-flow are shown with red and blue voxel marks, respectively. TSEs of the motion conditions showed significant decrease in amplitudes in induced
theta-band activity than static non-flow. Further, induced amplitude increases particularly in the alpha-beta range can be observed in the older infants (D). Epoch is from
 200 ms to 800 ms and baseline at  100 to 0 ms. Stimulus onset is indicated with a vertical red line at 0 ms. (For interpretation of the references to colour in this figure
legend, the reader is referred to the web version of this article.)

each of the motion conditions were separately compared with the
TSEs of the static condition, with no significant differences ob-
served when TSEs were compared between pairs of the three
motion conditions.
TSEs of the motion conditions showed lower amplitude values
in theta-band range than the static control condition in the visual
areas of interest for full-term and preterm infants at both
4 months and 12 months. These activities within the theta-band
range appeared as desynchronised oscillatory activities in the TSEs
of the full-term (Fig. 6) and preterm (Fig. 7) infants at 4 months
and 12 months when the motion conditions were compared with
the static non-flow condition. Additionally, the decrease in low-
frequency amplitudes were observed to be desynchronised with
activities induced by the motion conditions in both full-term and
preterm infants such that suppression of theta-band activity as a
result of the presentation of the motion conditions was observed
in the visual areas from about 500 ms to end of stimulus. However,
the observed theta-band desynchronisation in the TSEs of the
motion conditions was rather seen as synchronised theta-band
activities in the same time range in the TSEs of the static non-flow
condition for both full-term and preterm infants at 4 months and
12 months.
Further statistical analysis of each infant when comparing the
TSEs of the motion conditions with the TSEs of the static condition
showed significant high-amplitude oscillatory activities in at least
two of the visual areas of interest but only in the full-term infants
at 12 months (see Fig. 6B, D). TSEs of the motion conditions when
compared to the static condition showed high amplitudes within
the alpha-beta frequency band which occurred at different la-
tencies from start to around 450 ms post-stimulus, and around
600 ms to end of stimulus. These high amplitude increases were
synchronised with induced expression of alpha-beta frequencies
at peak latencies around 250 ms after stimulus onset. The alpha-
beta frequency band activities appeared as synchronisations in the
98 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104

Fig. 7. TSE plots (A, B) and the corresponding TSE probability maps (C, D) across brain regions (VClL, PM, VClR) when the motion conditions were compared with the static
non-flow in a typical preterm infant at 4 months (A, C) and 12 months (B, D). In the TSE plots, induced synchronised and desynchronised activities are shown in red and blue
contours, respectively. Only induced theta-band desynchronised activities are predominantly observed in all the visual areas in the preterm infants at both 4 months and 12
months. In the TSE probability maps, significant decrease of TSE spectral amplitudes (p o 0.05) in the motion conditions compared to static non-flow is shown in blue voxel
marks. TSEs of the motion conditions showed significant decreased amplitudes in induced theta-band activity with respect to the static non-flow condition. Stimulus onset is
indicated with a vertical red line at 0 ms. Epoch is from  200 ms to 800 ms and baseline at  100 to 0 ms. (For interpretation of the references to colour in this figure legend,
the reader is referred to the web version of this article.)

TSEs of the motion conditions compared with the static condition
in the full-term infants. No significant differences in induced ac-
tivities were found when TSEs were compared between the mo-
tion conditions in each infant. Further, the observed induced al-
pha-beta synchronised activities in the TSEs of the motion con-
ditions in the full-term infants occurred within the same fre-
quency range as the alpha-beta desynchronised activities observed
in the static non-flow condition. Unlike in the older full-term in-
fants, however, no such high-frequency activities were generally
observed in the preterm infants at 12 months (see Fig. 7). None-
theless, a few preterm infants at 12 months (3 out of 9) showed
significant high-frequency synchronised activities particularly in
the beta-frequency band albeit not as prominent as the synchro-
nised activities observed in the older full-term infants. In addition,
the three preterm infants who showed outlier latency values for
the optic flow conditions did not have any high-frequency oscil-
latory activities in their TSEs at 12 months. In the TSEs of each
individual infant and in the TSEs of each infant group, no
significant induced activities were observed in any other fre-
quency bands, including the delta and gamma band frequencies
when frequency cut-off was analysed below 4 Hz and above 40 Hz.
4. Discussion
The present longitudinal study investigated the perception of
visual motion information during early infancy, and the differ-
ences in visual motion perception between normally developing
full-term and preterm infants. High-density EEG was used to ob-
serve cortical electrical activity as a perceptual response to struc-
tured radial optic flow (forwards and reversed) and to random
visual motion. Motion specific N2 components of the VEP wave-
forms for 4- and 12-month-old full-term and preterm infants were
compared for latencies and amplitudes, with induced EEG activ-
ities further analysed.
A significant improvement in latencies from forwards optic
 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
flow to reversed optic flow and random motion was observed only
in full-term infants at 12 months, with no marked improvement in
latencies between the motion conditions when full-term infants
were younger. The older full-term infants showed shortest latency
for forwards optic flow and longest latency for random visual
motion. The result corroborates earlier findings from the study
that longitudinally compared full-term infants at 3–4 months and
11–12 months using similar experimental paradigm (Agyei et al.,
2015). One contributing factor to this observed improvement in
visual motion perception could be neural maturation that allowed
for more efficient processing of the visual motion information at
12 months. It has been shown that fibre volume of white matter
aggrandises due to ongoing axonal myelination during the early
maturational stages until adulthood (Jito et al., 2008; Paus et al.,
2001). Myelin sheath over the axons serves to increase the speed
of propagation of electrical impulses. Increased myelination as
infants aged from 4 to 12 months may have contributed to the
faster propagation of motion information and the shorter latencies
observed at 12 months. Thus, full-term infants appeared to show
better responses when perceiving structured radial optic flow in-
formation (shown by the shorter latencies), and they seemed af-
fected by the lack of structure in random visual motion as evi-
denced by the longest latencies in the random condition. Full-term
infants' N2 latencies in response to random visual motion did not
become saliently shorter with age. It is possible that the lack of
structured information in a random visual scene hinders visual
motion perception in infants in the early stages of independent
self-motion. Further, other neurological studies have reported that
the numbers of dendrites and synaptic connections in the primary
visual cortex increase during the first months of life and that they
reach a peak level between the ages of 8 months and 2 years
(Klaver et al., 2011; Loenneker et al., 2011). It has also been ob-
served that the rate of metabolic activity in occipital, parietal, and
temporal cortices increases strongly after 3 months, while in visual
association cortex and frontal cortex, the rate of increase occurs
after 6–8 months of age (Klaver et al., 2011; Loenneker et al., 2011).
These increases in the number of dendrites and synaptic connec-
tions, as well as the rate of metabolic activity could mean that
functional specialisations of the neurons become optimal around
the second half of the first year of life. Thus, latency differentia-
tions between the three motion conditions that occurred only in
full-term infants at 12 months but not when they were 4 months
old could be associated with improved functional specialisations of
neurons in the dorsal visual stream of the older infants.
The shorter latencies observed in the older full-term infants
when presented with the structured optic flow conditions could
also be attributed to infants' frequent use of structured informa-
tion for effective navigation (Bruggeman and Warren, 2010;
Bruggeman et al., 2007; Lamontagne et al., 2007; Lee and Aronson,
1974; Slobounov et al., 2006). Infants start to passively explore the
environment soon after birth either in a stroller or when being
carried by their caregivers until they begin crawling or walking
(see e.g., Raudies et al., 2012). With crawling and/or walking, in-
fants are able to actively explore the surroundings through their
own movement. Considering that passive experience of motion
has been shown to reveal a minimum level of improvement in
sensitivity to optic flow between 3 and 6 months (Gilmore et al.,
2004), the passive experience acquired by the younger full-term
infants could have partially accounted for their inability to dis-
tinguish between the three motion conditions. This inability of the
younger infants to distinguish between the motion conditions is
further supported by studies in 4-month-old infants that showed
that infants at this age are poor at discriminating between differ-
ent directions simulated by optic flow patterns (Gilmore and Re-
ttke, 2003). Further, behavioural studies on postural control show
a strong coupling between visual motion perception and postural
99
control (Anderson et al., 2001; Higgins et al., 1996; Lejeune et al.,
2006). Such studies found that infants who had crawling experi-
ence were more sensitive to optic flow stimuli for postural control.
Infants that perceived optic flow in the anteroposterior direction
in a moving room were also able to substantially improve their
postural responses particularly after they learned to sit and crawl
(Bertenthal et al., 1997). Thus, the experience from self-produced
locomotion affords infants the ability to make better use of the
information embedded in optic flow (Anderson et al., 2001; Hig-
gins et al., 1996; Lejeune et al., 2006). Self-produced locomotion
experience may therefore be more relevant for normal develop-
ment of visual perception than passive experience. Niell and
Stryker (2010) showed that neural responses in the visual cortex
are modulated by visual input from locomotion but strongly dri-
ven responses of neurons in the visual cortex arise from motor-
related input to the cortex from self-generated actions (Keller
et al., 2012; Szuts et al., 2011). Further, functional perception of
structured radial flow develops with acquired independent loco-
motion (Van der Meer et al., 2008), with only self-generated ac-
tions leading to a strong link between perception and action in the
developing brain (James and Swain, 2011; Schwarzer et al., 2013).
In the present study, parental records showed full-term infants to
have approximately 3 months of crawling experience, with five
infants able to walk for at least 2 weeks by the second testing
session. It is plausible that, in addition to maturation, the active
self-locomotion experience acquired by the older full-term infants
may have led to faster recruitment and activation of neural net-
works responsible for motion recognition compared to the
younger infants who may have only experienced locomotion
passively.
Results also indicated that preterm infants did not show la-
tency differences in the motion conditions from 4 months to 12
months. Even though most of the preterm infants had similar
months of crawling experience as full-term infants at the time of
the second testing, they did not differentiate between the three
motion conditions at 12 months unlike the full-term infants. It has
been shown that preterm infants at corrected age of 2–3 months
are delayed several weeks compared to full-term infants when
differentiating between changes of direction (Birtles et al., 2007;
Braddick et al., 2005). Most neuroimaging studies agree on the
idea that there is white matter abnormality characterised by the
appearance of diffuse and excessive high signal intensity (DEHSI)
throughout the cerebral cortex in preterm infants at corrected ages
(Atkinson et al., 2008a; Counsell and Boardman, 2005; Counsell
et al., 2003, 2006; Maalouf et al., 1999; Salt and Redshaw, 2006;
Skiold et al., 2010). Other follow-up studies (e.g., Hart et al., 2011;
Skiold et al., 2012) show no association between DEHSI and pos-
sible brain damage while others assert that DEHSI should be
considered a form of white matter injury rather than white matter
immaturity (e.g., Domizio et al., 2005). Nonetheless, it is probable
that white matter abnormality that underlies the impairment of
the dorsal visual stream could have adversely affected the effective
propagation of axonal electrical impulses during transmission of
motion information in the preterm infants. This could have partly
accounted for the unimproved latencies in the preterm infants
with age.
Further, studies with docosahexaenoic acid (DHA), the long
polyunsaturated fatty acid that is transferred to the foetus in the
third trimester of pregnancy, show that DHA is an important
component involved in synaptogenesis, brain tissue synthesis,
cellular differentiation, and neurotransmitter metabolism (Neur-
inger et al., 1986; Sabel et al., 2009; Stein, 2001). Other studies
report impaired functioning of the dorsal pathway due to in-
sufficient supply of DHA (Auestad et al., 2001; Carlson and
Werkman, 1996; O'Connor et al., 2001; Werkman and Carlson,
1996). Since the developmental period of the dorsal stream is
100 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
believed to be concentrated around the third trimester of preg-
nancy (Hammarrenger et al., 2007; Klaver et al., 2011) and the cells
of the dorsal pathway need high levels of polyunsaturated fatty
acids for the optimal functioning of physiological processes (Sabel
et al., 2009; Stein, 2001), it is possible that the unimproved la-
tencies observed in the preterm infants who were all born at ge-
stational age of 33 weeks or less may have been related to their
being deprived of sufficient essential fatty acids such as DHA.
However, it is also possible that the unimproved latencies and the
inability to differentiate between the motion conditions in the
preterm infants at 12 months could have been a normal delay
related to premature birth that may be recovered at a later age. A
follow-up study to monitor the developmental progress of the
preterm group could help ascertain the validity of this notion.
Interestingly, preterm infants at 4 months showed significantly
shorter latencies regardless of visual motion condition compared
to the full-term infants at 4 months. The fact that preterm infants
were tested corrected for prematurity could have contributed to
this faster perceptual response, considering that the 4-month-old
preterm infants had up to 3 months longer exposure and experi-
ence to real-world visual flow than the 4-month-old full-term
infants. The individual analysis of the preterm infants further
pointed to three infants that showed extremely longer latencies in
response to the structured optic flow conditions compared to the
other infants. Since these three preterm infants were born at later
gestational ages relative to the other preterm infants and were
neither bottom shufflers nor showed any signs of delayed motor
development prior to testing, it is rather likely that their longer
latencies represent normal developmental delays that may be re-
covered with age. The suggested longitudinal follow-up on the
preterm infants could help uphold the criterion used in the in-
dividual analysis as an early screening tool to detect impairments
of visual motion perception in premature infants.
Comparison of the amplitudes of the N2 components revealed
lower activation values in preterm infants at 4 months than in full-
terms at 4 months. Given that amplitudes of brain electrical wa-
veforms represent the synchronous activity of excited neurons, it
is considered that higher amplitudes may reflect more synchro-
nous signals elicited by activated neurons in large cortical areas
(Pfurtscheller and Lopes da Silva, 1999; Pfurtscheller et al., 1994).
When compared to the full-term infants at 4 months, the lower
amplitudes in preterm infants at 4 months could reflect a rela-
tively lower number of synchronously active neurons that were
activated in response to the presented motion stimuli. This num-
ber of synchronously active neurons may have been better adapted
to respond to motion stimuli in the younger preterm infants
compared to the younger full-term infants, considering the pre-
term infants' earlier exposure to optic flow information. However,
the activation values recorded for all the infant groups were gen-
erally high when compared to adults (cf., Van der Meer et al.,
2008). These large activation values that may reflect activation of
large cortical areas could imply less specialized and adapted neural
networks involved in the perception of visual motion in the infants
in general (see Huttenlocher and Dabholkar (1997)). The larger
activation values in the infants could also have been a result of
infants' relatively thinner skulls that allowed for less impedance
when measuring cortical electrical activity (Grieve et al., 2003).
Skull thickness and bone density in the infants were adjusted
using recommended values during the TSE analysis where the
time-dependent changes in amplitudes were explored.
Investigating the differences in induced activities showed that
both full-term and preterm infants had significantly low amplitude
values in the theta-band range over the visual areas of interest
when the motion conditions were compared with the static non-
flow control condition. More prevalent theta-band activities oc-
curred in the younger infants compared to the older infants in
each group. Theta-band activities were observed as desynchro-
nised oscillatory activities in the TSE plots. Studies have observed
low-frequency activities of large amplitudes in infant EEG as a
general sign of immaturity (Agyei et al., 2015; Carmeli et al., 2005;
Pfurtscheller et al., 1994; Stroganova and Orekhova, 2007; Thierry,
2005). These studies are corroborated by the findings in the pre-
sent paper where induced activities within the theta-band range
were observed when the TSEs of the motion conditions were
compared with the static dot pattern. Given that optimal synaptic
plasticity occurs in the infant brain (Casey et al., 2000; Stroganova
and Orekhova, 2007), with the implication of theta-band activities
during the successful encoding of memory information (Freun-
berger et al., 2011; Khader et al., 2010; Klimesch et al., 1996), it is
possible that the observation of theta-band activities in the infants
could reflect the formation of cortical synapses involved in the
processing of the motion information. Further, slowly oscillating
cell assemblies are usually composed of more neurons in com-
parison to faster oscillating assemblies, with amplitude of oscil-
lation found to be proportional to the number of synchronously
firing neurons (Elul, 1971; Pfurtscheller and Klimesch, 1992;
Pfurtscheller and Lopes da Silva, 1999; Pfurtscheller et al., 1994;
Singer, 1993). The more prevalent and widespread theta-band
activities in the younger infants could suggest the recruitment of
larger neuronal networks during processing of the visual motion
conditions (Pfurtscheller and Lopes da Silva, 1999), a general in-
dication of the involvement of less specialised cortical networks
involved in motion information processing in infancy.
The theta-band activity was more prevalent and widespread in
full-term infants at 4 months compared to preterm infants at
4 months. The less specialised and larger cortical neuronal net-
works in the full-term infants at 4 months could further help ex-
plain the observation of slower perceptual responses (shown by
the longer N2 latencies as stated above) in the full-term infants at
4 months compared to the preterm infants at 4 months whose
responses to visual motion were relatively faster. Considering that
theta-band oscillatory activities were found in all infants both at
4 and 12 months in response to the radial motion stimuli, it is
possible that oscillatory activities within the theta-band frequency
may be a general property of the immature neuronal networks
that are responsible for the processing of motion information in
the first year of life.
High-amplitude values in the alpha-beta frequency band were
further observed in the full-term infants but only at 12 months.
The alpha-beta frequency was seen as synchronised activities in
the TSE plots over the visual areas of interest. Alpha and beta
rhythms may be important for cross-network functional con-
nectivity (Ganzetti and Mantini, 2013) and may serve to con-
solidate and link actions across wide areas of the brain (De Pas-
quale et al., 2010, 2012). Synchronised oscillatory activity that ra-
pidly changes within specific brain circuits may characterize long-
range neuronal communication (De Pasquale et al., 2012) that may
enable the progressive maintenance and modulation of different
aspects of task representations within brain circuits (Deco and
Corbetta, 2011; Engel et al., 2001; Gilbert and Sigman, 2007;
Vanni, 1999). The faster oscillating alpha-beta synchronised fre-
quency band activities in the older full-term infants give credence
to the emergence of more specialised functional neuronal net-
works within the visual areas of the older full-term infants when
processing motion information. These synchronised activities at
higher frequencies may also suggest the involvement of activated
subsets of cortical areas and the use of higher cortical structures
during the global perception of radial motion. Thus, there ap-
peared to have been a progression from the slowly oscillating
theta-band frequency that was particularly prevalent when infants
were younger to the faster alpha-beta frequency band during
processing of radial motion in the older full-term infants. This
 S.B. Agyei et al. / Neuropsychologia 84 (2016) 89–104
progression may become more apparent as infants develop into
adults since adult studies have implicated increased gamma-band
power in the visual cortex during motion processing (Hoogen-
boom et al., 2006; Krishnan et al., 2005). The faster gamma-band
frequency is shown to be a more effective way of establishing
rapid coupling between cell assemblies where information pro-
cessing is more specific and locally confined (Fries, 2005; Fries
et al., 2008; Singer, 1993).
However, unlike the TSEs of the full-term infants at 12 months,
the TSEs of the older preterm infants were observed to show no
synchronised oscillatory activities in the alpha-beta range when
the TSEs of the motion conditions were compared with the static
control pattern. TSEs of the preterm infants at 12 months were still
dominated by activities within the theta-band frequency albeit not
as prevalent as when they were younger. The absence of high-
frequency oscillatory activities in the preterm infants at 12 months
may indicate that their cortical growth may have been slower than
the full-term infants as they may not have sufficiently developed
specialized neural networks for rapid processing of visual motion
information compared to the full-term infants at 12 months. Since
the dorsal visual stream develops and matures relatively earlier
(Hammarrenger et al., 2007), being born preterm may have dis-
rupted the association fibres and synaptic development in the
dorsal stream that help to fine-tune cortical growth during late
foetal and early extrauterine life (Huppi et al., 1998; Kapellou et al.,
2006; Mewes et al., 2006). This disruption in the development of
the dorsal visual stream as a result of the infants being born pre-
term may have impeded efficient cortical growth and contributed
to the absence of higher frequency oscillatory activities when they
were older. Other studies (e.g., Agyei et al., 2016; Kapellou et al.,
2006) have also suggested slower cortical growth in preterm in-
fants compared to full-terms.
While induced theta-band desynchronisation was observed in
the TSEs of the motion conditions in the infants, induced theta-
band synchronisation was rather observed in the TSEs of the static
condition. Neuronal assemblies may have therefore fired in syn-
chrony under the perception of the static dot pattern but this
synchronised activity was suppressed when infants perceived the
motion conditions. With task complexity contributing to en-
hancement of theta desynchronisations (Pfurtscheller et al., 1994),
it is possible that differences in task complexities of the presented
stimuli, from the relatively simple static dot pattern to the more
complex radial motion conditions, may have contributed to these
observed oscillatory differences when perceiving the motion
conditions and the static dot pattern.
In the present longitudinal study, developmental improve-
ments in brain activities as observed in VEPs and TSEs of full-term
and preterm infants when processing radial motion information
were presented. Full-term infants were shown to functionally
discriminate between different patterns of radial motion condi-
tions with age, while preterm infants showed no such develop-
mental differences. In addition, both full-term and preterm infants
showed desynchronised theta-band oscillatory activities when
processing the motion conditions, with only the full-term infants
at 12 months further showing synchronisations in alpha-beta
frequency bands in response to the motion conditions. These im-
provements in the functional neuronal networks of full-term in-
fants in perceiving visual motion were attributed to neurodeve-
lopmental changes coupled with active locomotor experience. The
poorer responses in the preterm infants were associated with
abnormalities related to visual dorsal stream vulnerabilities. Fol-
low-up studies on the preterm infants, together with more long-
itudinal research in full-term infants will be carried out in future
to help acquire a better understanding of the developmental
progress of visual motion perception in preterm and full-term
infants. Considering that the present paper studied moderate to
101
very preterm infants, the present findings should not be general-
ised to all groups of preterm infants, especially those born below
28 weeks of gestation. Further future research could examine
different groups of premature infants, including those classified as
extremely preterm in order to have a comprehensive under-
standing of the effects and severity of prematurity on the devel-
opment of visual motion perception.
Acknowledgements
This project was partly made possible by the Norwegian Ex-
traFoundation for Health and Rehabilitation. The authors are
grateful to Broen van Besien and Eirik Paulsen for programming
the visual stimuli, and to the parents and their infants for taking
part in the study. They are also grateful to Belde Mutaf for her
contribution during her Master's thesis, and to Magnus Holth and
Kenneth Vilhelmsen for their help with testing, as well as the
neonatologist at St. Olav's University Hospital, Ragnhild Støen, for
her help with the recruitment of the preterm infants.
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