DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY

REVIEW

Visuospatial and visuomotor deficits in preterm children: the

involvement of cerebellar dysfunctioning
KOENRAAD N J A VAN BRAECKEL 1

| H GERRY TAYLOR 2

1 Division of Neonatology, Beatrix Childrens Hospital, University Medical Center Groningen, University of Groningen, Groningen, the Netherlands. 2 Department of
Pediatrics, Case Western Reserve University and Rainbow Babies & Childrens Hospital, University Hospitals Case Medical Center, Cleveland, OH, USA.
Correspondence to Dr K N J A Van Braeckel, Afdeling Neonatologie, Beatrix Kinderziekenhuis, Postbus 30.001, 9700RB Groningen, the Netherlands. E-mail: k.van.braeckel@umcg.nl

PUBLICATION DATA

Accepted for publication 4th April 2013.

One of the more consistent findings in follow-up studies of preterm children is a deficit in
visuospatial and visuomotor skills. Impairment of the dorsal visual stream and basal ganglia
damage have been hypothesized to underlie this deficit. However, given recent findings of
impaired cerebellar development in preterm children without lesions to this structure, and
the involvement of the cerebellum in visuospatial and visuomotor functioning, we argue the
cerebellum should be included in models relating impaired development of brain networks to
visuospatial and visuomotor deficits in this population. Here, we review the current literature
on impaired cerebellar development in preterm children, and suggest possible underlying
mechanisms.

As a result of improved care in the past few decades, an increasing

number of children survive preterm birth (<37 weeks gestational
age) without serious neurological complications.1 Research into the
long-term consequences of preterm birth in this group has focused
on more subtle signs of impairment.2 One of the more consistent
findings in follow-up studies is a deficit in visual and visuomotor
skills.25 Impairment of the dorsal visual stream, a neural network
linking the occipital and posterior parietal cortices and its connections with prefrontal and premotor cortex, and hippocampal
regions6 has been hypothesized to underlie these deficits in preterm
children.25 Basal ganglia damage sustained in the first 6 months of
life independent of cortical injury has also been shown to underlie
altered visual development in children.7 However, given recent
findings of impaired cerebellar development in preterm children
without lesions to this structure,8 and the involvement of the cerebellum in visuospatial and visuomotor functioning,9,10 we argue
that the cerebellum should be included in models relating impaired
development of brain networks to visual and visuomotor deficits in
this population. To this end, we consider the role of the cerebellum
in visuospatial and visuomotor skills, review the present literature
on impaired cerebellar development in preterm children, and suggest possible underlying mechanisms.

CEREBELLAR INVOLVEMENT IN VISUOSPATIAL AND

VISUOMOTOR FUNCTIONING
For most of the 20th century, the cerebellum has been associated
with coordination, balance, and motor speech regulation. In 1986,
Leiner et al.11 proposed cerebellar involvement in cognition on
the basis of anatomical, physiological, and clinical data. Subsequent research documented involvement of the cerebellum in
planning, learning, and language.12 Botez9 was one of the first to
report visuospatial deficits in a large group of patients with bilateral cerebellar damage. More recent studies in adults with focal
cerebellar infarcts confirmed visuospatial and visuomotor
deficits.1315 In children, Levisohn et al.10 showed wide ranging

cognitiveaffective deficits including impaired visuomotor and

visuospatial functioning in a group of 3- to 14-year-olds, who
underwent cerebellar tumor resection without having received
cranial irradiation or chemotherapy.
Neuro-anatomical studies proposing an afferent and efferent
cerebello-cerebral network are in line with the results of these
clinical behavioral studies. An afferent system provides input from
the posterior parietal cortex through the pontine nuclei to the
lateral lobes of the cerebellum. An efferent system sends output
from the cerebellum through the thalamus back to the posterior
parietal cortex.16 Given the pivotal role of the posterior parietal
cortex in visuospatial and visuomotor functioning,6 such a
cerebello-cerebral network supports the suggestion of cerebellar
involvement in visuospatial and visuomotor functioning.
Cerebellar contributions to these functions are further supported by findings from functional magnetic resonance imaging
(fMRI). Functional magnetic resonance imaging in healthy adults
reveals activation of the cerebellum during non-motor visuospatial
tasks, such as line bisection, judgment of line orientation, mental
rotation of shapes, and mental navigation.17 Other studies indicate
an association of visuospatial functioning with the topography of
the lateral lobes of the cerebellum,17,18 as is consistent with
neuro-anatomical connections between the cerebellar lateral lobes
and the posterior parietal cortex.16 Although most of these studies
have been conducted with samples of adults, they suggest a special
role for the lateral cerebellar lobes in spatial cognition.

IMPAIRED CEREBELLAR DEVELOPMENT IN PRETERM

CHILDREN
In Table I, findings from studies8,1924 of cerebellar volume in
preterm children are summarized. The findings document
early and persisting volume reductions across childhood until
adulthood, as well as an association of volume reductions with
lower gestational age and birthweight, suggesting that preterm
birth disrupts early cerebellar development. This decreased vol-

The Authors. Developmental Medicine & Child Neurology 2013 Mac Keith Press, 55 (Suppl. 4): 1922

DOI: 10.1111/dmcn.12301 19

ume is more pronounced in the lateral lobes than in the midline

regions, with no differences in vermis size between preterm and
term children.22,25 These studies also reveal a strong positive relation between reduced cerebellar volume, specifically of the lateral
cerebellar lobes, and visuospatial and visuomotor functioning later
in life. Impaired development of the lateral lobes in preterm children may therefore contribute to visuospatial and visuomotor
impairments in preterm children.

LIKELY MECHANISMS UNDERLYING IMPAIRED

CEREBELLAR DEVELOPMENT IN PRETERM CHILDREN
One potential mechanism for impaired cerebellar development in
very preterm children is a crossed trophic effect of cerebral insult
on the development of the cerebellum, also referred to as diaschisis. Diaschisis refers to a loss of function in a neurally connected
region remote from a brain lesion. A second potential mechanism
is disrupted growth of the cerebellums granular layer secondary
to preterm birth, a structure that is undergoing rapid changes in
the later stages of fetal development.
Rollins et al.26 described crossed trophic effects or diaschisis in
extremely preterm infants, and suggested that cerebellar atrophy is
most often a secondary degenerative phenomenon after severe
intracranial hemorrhage and/or ischemic necrosis of white matter.
More recently, Limperopoulos et al.27 found both a reduction in
contralateral cerebellar volume with unilateral cerebral parenchymal injury and a reduction in total cerebellar volume with bilateral
cerebral lesions in very preterm infants. Messerschmidt et al.19 also
found cerebellar growth impairment in very preterm children with
cerebral injuries. Consistently, Allin et al.22 and Argyropoulou
et al.25 found positive associations between cerebral white matter
volume and cerebellar volume in very preterm children.
Preterm children enter the world during a vulnerable period in
the development of the cerebellum. From about 16 weeks gestational age until about 7 weeks after term birth, granule cells proliferate and migrate from the external granular layer to the
internal granular layer of the cerebellum.28 Granular cell proliferation and migration are especially critical for cerebellar development given that most neurons in the cerebellum are granule cells
and the number of these cells in the adult cerebellum, about 1011,
far exceeds the total number of neurons in the entire cerebral cortex.29 Haldipur et al.30 compared molecular markers of cerebellar
development in preterm infants who survived 5 to 36 days ex utero with those in gestationally age-matched stillborn infants. The
live-born preterm infants had significant reductions in the thickness of the cerebellum relative to the stillborn infants, as well as
an increased packing density of cells within the external and the
internal granular layers. They concluded that the neurogenesis of
the cerebellum is altered by events after preterm birth and that
granular layer development is specifically affected. This selective
effect is consistent with the results from the MRI study of Limperopoulos et al.,8 who found cerebellar underdevelopment in
their subgroup of preterm children without cerebral injury. The
finding by Allin et al.22 of cerebellar underdevelopment specific to
the lateral lobes is also consistent with these findings, as the granular layers are situated in the lateral lobes. We speculate that
increased risk for altered development of the granular layers in
preterm children results in poorer efference to parietal areas of
the cerebrum and thus in poorer parietal development (cerebellocerebral diaschisis/crossed trophic effect). Such poorer parietal
development may jeopardize the development of the dorsal visual
stream and lead to impairment in visuospatial and visuomotor
functioning.
20 Developmental Medicine & Child Neurology 2013, 55 (Suppl. 4): 1922

What this paper adds

Preterm birth can result in direct insult to the cerebellum or in cerebro-cerebellar diaschisis, but may also affect cerebellar development in the absence
of brain lesions.
Further research is needed to understand these effects and their relation to
the deficits in visuospatial and visuomotor functioning commonly observed in
preterm children.

However, Srinivasan et al.31 showed cerebellar growth impairment in very preterm infants only in association with supratentorial
lesions, whereas cerebellar volume in very preterm infants without
supratentorial lesions did not differ from that of term comparison
infants. Similarly, Shah et al.32 observed associations of cerebellar
volumes in preterm infants with cerebral white matter injury but
not in preterm infants without cerebral white matter injury. These
findings support the possibility that cerebral injury associated with
prematurity results in poorer afference to the cerebellum (cerebrocerebellar diaschisis), but they appear to contradict those of Limperopoulos et al.8 indicating cerebellar underdevelopment in their
subgroup of preterm children without cerebral injury. However,
the latter investigators found that the difference in cerebellar volume between preterm children without cerebral injury and term
comparison children, although significant, was smaller than that
between preterm children with cerebral injury and the term comparison group. Adverse effects of perinatal events on cerebellar
development (second mechanism) may thus be small relative to the
effects of cerebro-cerebellar diaschisis. The results of Limperopoulos et al.8 lead us to speculate that preterm children with brain
injury sustain an additive negative impact of preterm birth on cerebellar development (second mechanism), over and above the effects
of cerebro-cerebellar diaschisis, resulting in smaller cerebellar volumes in preterm children with cerebral injury than in children without cerebral injury. Studies comparing the cerebellar volumes of
subsets of preterm children with and without cerebral injury with
those of term children would shed light on this possibility. Finally,
smaller cerebellar volumes may result in the development of alternative neural pathways. Interestingly, such an alternative network
may not be accompanied by poorer functional development, as has
been shown for language development in preterm adults.33 This
suggests that the preterm infants brains capacity for the recruitment of alternative neural pathways plays an important role in the
infants functional development.

CONCLUSION
In summary, there is a growing body of evidence suggesting a
heightened risk for impaired cerebellar development in preterm
children, even in the absence of identifiable perinatal cerebellar
insults. Reduced cerebellar volumes, moreover, are associated with
poorer visuospatial and visuomotor functioning in preterm children. Afferent and efferent connections between the cerebellum
and parietal regions also support involvement of the cerebellum in
visuospatial and visuomotor functioning. We thus propose to
include cerebellar underdevelopment in explanatory models to
account for poorer visuospatial and visuomotor functioning in preterm children. Studies focusing on the status of the motor and cognitive processes specifically subserved by the cerebellum in this
population would allow the construction of clinical tests assessing
the motor and cognitive aspects of cerebellar functioning in preterm children. These tests could also be applied to assess cerebellar
functioning in term-born children with learning problems and in
typically developing children. Motor processes could be investigated by testing classical motor functions, such as upper limb

Visuospatial and Visuomotor Deficits in Preterm Children Koenraad N J A Van Braeckel and H Gerry Taylor 21

2931

2931

25.9 (1.8)

29.5 (2.43)

Allin et al.21

Allin et al.22

Taylor et al.23

Kalpakidou
et al.24

12

37

67

67

26

31

169

37wk
0d42wk 6d

Term

3842wk

3842wk

39.4 (SD 1.3)

Gestational
age-matched

39.6 (SD 0.8)

17

36

50

50

39

31

20

Gestational
age, wk
n
Comparison group

20y

16.8 (1.3y)

14.9y

14.9y

1, 3, 5, 7d
postnatally
plus weekly
up to third
month
adjusted
age
8y

40.1wk (1.5)

Age at
assessment
of cerebellum

MRI

MRI

MRI

MRI

MRI

Ultrasound

MRI

Method of
cerebellar
assessment

1, 4, 8, and
1415y

1, 4, 8, and
1415y

8y

2436mo

Age at
testing

IQ (WISC-R/K-ABC) plus
neuropsychological
plus neurological

IQ (WISC-III) plus
visuomotor (VMI) plus
psychiatric diagnoses
plus behavioural
problems (CBCL) plus
neurological
IQ (WISC-R/K-ABC) plus
neuropsychological
plus neurological

Neurological plus
neuromotor (BSID)
plus mental
development (BSID)

Type of testing

1. Volumes of cerebellum and other brain structures

were significantly smaller in the preterm group.
2. Smaller volumes of cerebellum and other brain
structures in the preterm group were correlated
significantly with lower full-scale IQ, verbal IQ,
performance IQ, and VMI.
1. Cerebellar volume was significantly smaller in the
preterm group.
2. Smaller cerebellar volume in the preterm group
was correlated significantly with lower full-scale IQ,
visuospatial subtests of WISC-R, reading age, and
working memory.
3. Cerebellar volume in the preterm group did not
correlate with motor neurological signs.
Smaller lateral but not midline cerebellar volume was
correlated significantly with lower scores on the
visuospatial subtests of WISC-R, and reading age.
Volumes of cerebellar white and grey matter and
other brain structures were significantly smaller in
the preterm group.
Right cerebellar grey matter volume was significantly
smaller in the preterm group despite a normal
ultrasound neonatally.

1. Cerebellar volumes were smaller in preterm infants

without demonstrable cerebral or cerebellar insults.
2. Reduced gestational age at birth and birthweight
were related to decreased cerebellar volume.
The preterm group with reduced cerebellar volume
showed a poorer neuromotor and mental
development than the preterm group with a
supratentorial brain injury and a normal cerebellar
ultrasound.

Major findings

MRI, magnetic resonance imaging; BSID, Bayley Scales of Infant Development; WISC, Wechsler Intelligence Scales; VMI, Visual-Motor Integration Test; CBCL, Child Behavior Checklist;
K-ABC, Kaufmann-Assessment Battery for Children.

28.7 (1.7)

27.0 (1.6)

Messerschmidt
et al.19

Peterson et al.20

29.1 (3.4)

Limperopoulos
et al.8

Study

Gestational
age, wk
n
Preterm group

Table I: Overview of studies assessing cerebellar volume in preterm-born groups

coordination, eye movements, motor speech, motor learning, and

motor timing and rhythm.21,34 The investigation of cognitive
processes is more challenging, as we know little about the independent contribution of the cerebellum to cognition. However, existing
research reveals deficits in executive, visuospatial, language, reading, and memory functioning after acquired or ontogenetic cerebellar injury in children and adults.35,36 A promising direction for
future investigation is to examine the cerebellums selective involvement in timing, structuring, and learning aspects of cognitive functions. Such studies may well lead to new tools to identify individual
learning needs and would help guide the design of educational
approaches that consider the role of cerebellar contributions to

learning.37 A further benefit is the opportunity to explore the interplay of changes in cerebellar structure and function with growth in
cognitive and learning skills. Associations between motor and cognitive development, such as those between fine manual control and
visual processing38 along with evidence for cerebellar contribution
to diverse cognitive functions, raise the possibility of wide-ranging
effects of cerebellar abnormalities on development.

CONFLICTS OF INTEREST
No financial assistance has been received in support of this paper
and the authors have not declared any conflicts of interest.

REFERENCES
1. Lemons JA, Bauer CR, Oh W, et al. Very low birth
weight outcomes of the National Institute of Child
Health and Human Development Neonatal Research
Network, January 1995 through December 1996. Pediatrics 2001; 107: 18.
2. Foreman N, Fielder A, Minshell C, Hurrion E, Sergienko E. Visual search, perception, and visual-motor

14. Kalashnikova LA, Zueva YV, Pugacheva OV, Korsakova

NK. Cognitive impairments in cerebellar infarcts. Neurosci Behav Physiol 2005; 35: 7739.
15. Molinari M, Petrosini L, Misciagna S, Leggio MG. Visuospatial abilities in cerebellar disorders. J Neurol Neurosurg Psychiatry 2004; 75: 23540.
16. Schmahmann JD, Pandya DN. Disconnection syn-

26. Rollins NK, Wen TS, Dominguez R. Crossed cerebellar

atrophy in children: a neurologic sequela of extreme prematurity. Pediatr Radiol 1995; 25: S205.
27. Limperopoulos C, Soul JS, Haidar H, et al. Impaired
trophic interactions between the cerebellum and the
cerebrum among preterm infants. Pediatrics 2005; 116:
84450.

skill in healthy children born at 2732 weeks gestation. J Exp Child Psychol 1997; 64: 2741.
3. Atkinson J, Braddick O. Visual and visuocognitive development in children born very prematurely. Progr Brain
Res 2007; 164: 12349.
4. Van Braeckel K, Butcher PR, Geuze RH, van Duijn MAJ,

dromes of basal ganglia, thalamus, and cerebrocerebellar

systems. Cortex 2008; 44: 103766.
17. Stoodley CJ. The cerebellum and cognition: evidence
from functional imaging studies. Cerebellum 2012; 11:
35265.
18. Lee TMC, Liu H-L, Hung KN, et al. The cerebellums

28. Ten Donkelaar HJ, Lammens M, Wesseling P, Thijssen

HOM, Renier WO. Development and developmental
disorders of the human cerebellum. J Neurol 2003; 250:
102536.
29. Volpe JJ. Cerebellum of the premature infant: rapidly
developing, vulnerable, clinically important. J Child Neu-

Bos AF, Bouma A. Less efficient elementary visuomotor

processes in 7- to 10-year-old preterm-born children
without cerebral palsy: an indication of impaired dorsal
stream processes. Neuropsychology 2008; 22: 75564.
5. Butcher PR, Bouma A, Stremmelaar EF, Bos AF, Smithson M, Van Braeckel KNJA. Visuospatial perception in
children born preterm with no major neurological disor-

involvement in the judgment of spatial orientation: a

functional magnetic resonance imaging study. Neuropsychologia 2005; 43: 18707.
19. Messerschmidt A, Fuiko R, Prayer D, et al. Disrupted
cerebellar development in preterm infants is associated
with impaired neurodevelopmental outcome. Eur J Pediatr 2008; 167: 11417.

rol 2009; 24: 1085104.

30. Haldipur P, Bharti U, Alberti C, et al. Preterm delivery
disrupts the developmental program of the cerebellum.
PLoS ONE 2011; 6: e23449.
31. Srinivasan L, Allsop J, Counsell SJ, Boardman JP,
Edwards AD, Rutherford M. Smaller cerebellar volumes
in very preterm infants at term-equivalent age are associ-

ders. Neuropsychology 2012; 26: 72334.

6. Kravitz DJ, Saleem KS, Baker CI, Mishkin M. A new
neural framework for visuospatial processing. Nat Rev
Neurosci 2011; 12: 21730.
7. Mercuri E, Atkinson J, Braddick O, et al. Basal ganglia
damage and impaired visual function in the newborn

20. Peterson BS, Vohr B, Staib LH, et al. Regional brain

volume abnormalities and long-term cognitive outcome
in preterm infants. JAMA 2000; 284: 193947.
21. Allin M, Matsumoto H, Santhouse AM, et al. Cognitive
and motor function and the size of the cerebellum
in adolescents born very pre-term. Brain 2001; 124: 60

ated with the presence of supratentorial lesions. Am J

Neuroradiol 2006; 27: 5739.
32. Shah DK, Anderson PJ, Carlin JB, et al. Reduction in
cerebellar volumes in preterm infants: relationship to
white matter injury and neurodevelopment at two years
of age. Pediatr Res 2006; 60: 97102.

infant. Arch Dis Child 1997; 77: F1114.

8. Limperopoulos C, Soul JS, Gauvreau K, et al. Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 2005; 115: 68895.
9. Botez MI. Cerebellum and non-motor behaviour. Rom J
Neurol Psychiatry 1993; 31: 18993.
10. Levisohn L, Cronin-Golob A, Schmahmann JD. Neuro-

6.
22. Allin MPG, Salaria S, Nosarti C, Wyatt J, Rifkin L,
Murray RM. Vermis and lateral lobes of the cerebellum
in adolescents born very preterm. Brain Imag 2005; 16:
18214.
23. Taylor HG, Filipek PA, Juranek J, Bangert B, Minich
N, Hack M. Brain volumes in adolescents with very low

33. Constable RT, Vohr BR, Scheinost D, et al. A left cerebellar pathway mediates language in prematurely-born
adults. Neuroimage 2013; 64: 3718.
34. Dennis M, Salman MS, Juranek J, Fletcher JM. Cerebellar motor function in spina bifida meningomyelocele.
Cerebellum 2010; 9: 48498.
35. Tavano A, Grasso R, Gagliardi C, et al. Disorders of

psychological consequences of cerebellar tumor resection

in children: cerebellar cognitive affective syndrome in a
paediatric population. Brain 2000; 123: 104150.
11. Leiner HC, Leiner AL, Dow RS. Does the cerebellum
contribute to mental skills? Behav Neurosci 1986; 100:
44354.

birth weight: effects on brain structure and associations

with neuropsychological outcomes. Dev Neuropsychol
2011; 36: 96117.
24. Kalpakidou AK, Allin MP, Walshe M, et al. Neonatal
brain injury and neuroanatomy of memory processing
following very preterm birth in adulthood: an fMRI

cognitive and affective development in cerebellar malformations. Brain 2007; 130: 264660.
36. Steinlin M. Cerebellar disorders in childhood: cognitive
problems. Cerebellum 2008; 7: 60710.
37. Jolles DD, Crone EA. Training the developing brain: a
neurocognitive approach. Front Hum Neurosci 2012; 6:

12. Bailleuix H, De Smet HJ, Paquier PF, De Deyn PP,

Marien P. Cerebellar neurocognition: insights into the bottom of the brain. Clin Neurol Neurosurg 2008; 110: 76373.
13. Hokkanen LSK, Kauranen V, Roine RO, Salonen O,
Kotila M. Subtle cognitive deficits after cerebellar deficits. Eur J Neurol 2006; 13: 16170.

study. PLoS ONE 2012; 7: e34858.

25. Argyropoulou MI, Xydis V, Drougia A, et al. MRI measurements of the pons and cerebellum in children born
preterm; associations with the severity of periventricular
leukomalacia and perinatal risk factors. Neuroradiology
2003; 45: 7304.

113.
38. Davis EE, Pitchford NJ, Limback E. The interrelation
between cognitive and motor development in typically
developing children aged 4-11 years is underpinned by
visual processing and fine manual control. Br J Psychol
2011; 102: 56984.

22 Developmental Medicine & Child Neurology 2013, 55 (Suppl. 4): 1922