The shift from local to global visual processing in 6-year-old children is associated with grey matter loss.

Abstract

A real-world visual scene consists of local elements (e.g. trees) that are arranged coherently into a global configuration (e.g. a forest). Children show psychological evolution from a preference for local visual information to an adult-like preference for global visual information, with the transition in visual preference occurring around 6 years of age. The brain regions involved in this shift in visual preference have not been described.
We used voxel-based morphometry (VBM) to study children during this developmental window to investigate changes in gray matter that underlie the shift from a bias for local to global visual information. Six-year-old children were assigned to groups according to their judgment on a global/local task. The first group included children who still presented with local visual processing biases, and the second group included children who showed global visual processing biases. VBM results indicated that compared to children with local visual processing biases, children with global visual processing biases had a loss of gray matter in the right occipital and parietal visuospatial areas.
These anatomical findings are in agreement with previous findings in children with neurodevelopmental disorders and represent the first structural identification of brain regions that allow healthy children to develop a global perception of the visual world.

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The Shift from Local to Global Visual Processing in 6-
Year-Old Children Is Associated with Grey Matter Loss
Nicolas Poirel1*, Gre ´gory Simon1, Mathieu Cassotti1,2, Gae ¨lle Leroux1, Guy Perchey1,3, Ce ´line Lanoe ¨1,
Ame ´lie Lubin1, Marie-Rene ´e Turbelin1,3, Sandrine Rossi1, Arlette Pineau1, Olivier Houde ´1,4
1UMR 6232, CI-NAPS, CNRS, CEA, Caen University and Paris Descartes University, Sorbonne, France, 2Centre de Gestion Scientifique, Mines ParisTech, Paris, France,
3Centre Hospitalier Universitaire, Caen, France, 4Institut Universitaire de France, Paris, France
Abstract
Background: A real-world visual scene consists of local elements (e.g. trees) that are arranged coherently into a global
configuration (e.g. a forest). Children show psychological evolution from a preference for local visual information to an
adult-like preference for global visual information, with the transition in visual preference occurring around 6 years of age.
The brain regions involved in this shift in visual preference have not been described.
Methods and Results: We used voxel-based morphometry (VBM) to study children during this developmental window to
investigate changes in gray matter that underlie the shift from a bias for local to global visual information. Six-year-old
children were assigned to groups according to their judgment on a global/local task. The first group included children who
still presented with local visual processing biases, and the second group included children who showed global visual
processing biases. VBM results indicated that compared to children with local visual processing biases, children with global
visual processing biases had a loss of gray matter in the right occipital and parietal visuospatial areas.
Conclusions: These anatomical findings are in agreement with previous findings in children with neurodevelopmental
disorders and represent the first structural identification of brain regions that allow healthy children to develop a global
perception of the visual world.
Citation: Poirel N, Simon G, Cassotti M, Leroux G, Perchey G, et al. (2011) The Shift from Local to Global Visual Processing in 6-Year-Old Children Is Associated with
Grey Matter Loss. PLoS ONE 6(6): e20879. doi:10.1371/journal.pone.0020879
Editor: Georges Chapouthier, Universite ´ Pierre et Marie Curie, France
Received March 31, 2011; Accepted May 11, 2011; Published June 8, 2011
Copyright: ? 2011 Poirel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors received no external funding sources for this study.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: nicolas.poirel@parisdescartes.fr
Introduction
Recent evidences from magnetic resonance imaging (MRI) show
thathumanbraindevelopmentischaracterizedbynonlineardynamic
loss of gray mater (GM) with age that varies according to brain region
[1,2]. Even if the fine-tuning of GM is now well established, little is
known about the relationship between brain structure variation and
perception evolution in children [3]. Reduction in synaptic density, a
phenomenon called ‘‘synaptic pruning,’’ is a fundamental neural
plasticity mechanism that may underlie selective behavioral special-
ization [4]. The present study investigated selective specialization
during a well-known developmental period in children in which the
mode of visual perception changes.
The visual world consists of local elements (e.g. trees) that are
arranged coherently into a global configuration (e.g. a forest).
Converging paradigms using compound stimuli (large global forms
composed of arrangements of small local forms; see [5] and Fig. 1)
clearly indicate an evolution from local preference (also called
local bias) in young children to an adult-like global preference (also
called global bias) by 9 years of age, with a transition occurring
around 6 years of age [6,7,8]. This transition may be due to a shift
in visuospatial strategy, i.e. a shift from a strategy of local sampling
of visual information processing to an exhaustive adult-like global
exploration of the visual stimuli [8,9]. The brain regions allowing
this shift in visual preference have not been identified, although
neuropsychological and neuroimaging studies have indicated that
different brain regions process global and local information. Adult
patients with right hemisphere injuries show impaired processing
of global level information, whereas patients with left hemisphere
injuries present with deficits in processing local elements [10,11].
These observations have been confirmed using functional imaging
in healthy adults [12,13] and in 14-year-olds [14]. Interestingly,
children with perinatal brain lesions to the left or right hemi-
spheres present with visuospatial deficits that mirror those in adult
patients (see [15] for a review). Longitudinal studies of 5- to 12-
year-old children by Stiles et al. also showed that overall, children
with right perinatal lesions can accurately perceive local but not
global elements of visual information, whereas children with left
perinatal lesions show the reverse pattern. The authors also noted
that although all of the children showed improved performance in
terms of visual perception as they got older, the deficit pattern
persisted for both groups. These studies revealed important
information about the relationships between brain lesions and
visuospatial development. However, the shift in bias from local to
global visual processing that occurs around age 6 in healthy
children has never been investigated.
The current study used voxel-based morphometry (VBM) of
anatomical MRI images of children’s brains to determine whether
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the shift from a local to a global visual processing bias corre-
sponded to changes in gray matter. It has been proposed that the
right hemisphere supports global information processing; thus, we
expected that compared to children with a local visual processing
bias (hereafter termed the ‘‘local bias’’ group), those with a global
visual processing bias (the ‘‘global bias’’ group) would show GM
loss mostly in right brain regions. This GM loss would represent
selective brain specialization for global visual processing. More
specifically, we expected to find GM loss in the right primary
visual cortex and in the right lingual gyrus, areas that are strongly
implicated in global processing in adults [12,16]. Finally, the shift
in visual processing bias might also induce GM loss in the right
parietal regions [17]. Because the switch in visual preference
concerns global visual processing, we did not expect differences
between the two groups of children in the left hemisphere, which is
involved in local visual processing, as noted above.
To test these hypotheses, we compared anatomical MRI images
from 6-year-old children who presented with either a local or a
global visual processing bias. In agreement with the principle of
selective specialization, our hypothesis was that reduction in right
hemisphere GM in children in the global bias group would be
associated with the emergence of adult-like global visual
perception.
Methods
Participants
Twenty-five children from Caen (Calvados, France) participated
in this study (mean age, 6 years61.6 months; 16 girls; 21 right
handed children). The children had no history of neurological
disease and no cerebral abnormalities as assessed by T1-weighted
MRI. The local ethics committee (CPP Nord-Ouest III, France)
approved the study. Written consent was obtained from the
parents and the children themselves after detailed discussion and
explanations.
MRI acquisition and analysis
Anatomical images were acquired for each child on the same 3
T MRI scanner (Achieva, Philips Medical System, the Nether-
lands) using 3D T1-weighted spoiled gradient images (FOV:
256 mm; slice thickness: 1.33 mm; 128 slices; matrix size 1926192
voxels; 5 min 7 s duration). Brain images were acquired while the
children passively watched a cartoon on an MRI-compatible
screen. The sedative effects of the audio/visual system on children
in MRI scanners have been demonstrated: specifically, this system
reduces motion, provides a positive experience, and decreases wait
times [18].
The T1 images were spatially normalized and segmented with
SPM5 software (Welcome Department of Cognitive Neurology,
www.fil.ion.ucl.ac.uk/spm) using a specific template built using the
T1 images of our sample of children (the anatomical images were
acquired with the same MRI scanner). A factorial VBM analysis
[19] was performed using SPM5 software on normalized,
modulated, and smoothed GM images by contrasting the two
groups of children on the basis of their local/global scores (see
below). This included a total brain volume correction for each
subject.
Local/global task
All children were presented with the global/local task at school
after the laboratory MRI session [5,20]. A total of 24 compound
stimulus triads were presented to measure global/local bias in
visual perception. Specifically, children judged which of two
figures was most similar to a reference figure (Fig. 1). The
judgment could be made based on either the local or global
aspect of the reference. Children were instructed to give their
first, most immediate similarity judgment for each trial. A
measure of global/local precedence was calculated afterwards for
each participant by subtracting the number of local choices from
the number of global choices. The value range was 224 to 24,
with a more positive value indicating a greater bias toward global
visual information.
Results
Behavioral results
The children were grouped according to their scores on the
local/global task. Children with negative scores were included in
the local bias group, and children with positive scores were
included in the global bias group (Fig. 1). In this sample, seven
children showed a local visual processing bias (6 girls; 7 right-
handed; mean score on the global/local task, 222.660.8) and 18
children showed a global visual processing bias (10 girls; 14 right-
handed; mean score on the global/local task, 23.360.3). The
global/local task scores differed significantly between the local
bias group and the global bias group (t(23)=67, p,0.0001).
Figure 1. Representative example of a global/local triad stimulus (left), mean global/local task scores (middle), and mean age
(right) for the local bias group (yellow) and the global bias group (pink). *p,0.05; ns=non-significant.
doi:10.1371/journal.pone.0020879.g001
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Importantly, the mean age was not significantly different for the
two groups (t(23)=0.99, p=0.33; Fig. 1).
VBM results
Contrast analyses were performed to identify changes in GM
density between the two groups of children. GM variations were
reported when voxels were significantly different at p,0.001
uncorrected, with a minimum of 50 voxels in clusters (Table 1).
The contrast analysis between the two groups revealed that
compared to the local bias group, the global bias group showed
losses in GM in the occipital cortex, along the right part of the
calcarine sulcus, the right inferior occipital gyrus extending to the
middle occipital gyrus, and the lingual gyri (bilaterally) (Fig. 2).
Note that the cluster in the lingual gyrus in the right hemisphere
was larger than in the left hemisphere (279 vs. 58 voxels). Finally,
GM loss was also observed in the parietal cortex, including losses
in the right precuneus and the postcentral gyrus. The reverse
comparison, i.e., subtraction of the GM density results of the local
bias group from those of the global bias group revealed no
significant differences.
Discussion
This study is the first to directly examine changes in GM density
during the developmental window in childhood when there is a
shift from a local visual processing bias to an adult-like global
visual processing bias. In agreement with our previous findings,
children at the transition age of 6 years presented either a local
visual processing bias or an adult-like global visual processing bias
[8]. Using VBM, we showed GM loss along the right calcarine
sulcus in the global bias group of children compared to the local
bias group of children, suggesting a fine-tuning of the primary
visual cortex for processing global visual information. GM
differences were also found in the right lingual gyrus and in the
right parietal region.
In adults, the right middle occipital cortex is more activated
during global tasks than during local tasks [16]. This early visual
area is predominant during processing of natural visual scenes with
low spatial frequency and is known to convey global information
during visual processing [21]. At the same time, the right lingual
gyrus is thought to function in global processing in adults [12].
Consequently, the GM loss in these regions that we observed in
children may reflect selective specialization in the early stages of
visual processing of global information. These results are in line
with our recent data showing that the capturing of attention by
global cues affects brain processing in the early visual stages
processing [22]. The present study also revealed a GM loss in the
right parietal cortex, which is involved in attentional focus toward
global information [11,21,23]. More specifically, the GM variation
in the precuneus may reflect the shift in attention to global rather
than local features [24]. As was also shown in the present work, the
postcentral gyrus is involved in global perception of coherent
scenes [25]. Interestingly, repetitive transcranial magnetic stimu-
lation (rTMS) findings indicate that the parietal cortex plays a key
role in attention toward global information [26]. In particular,
when the right posterior parietal cortex is stimulated by rTMS, the
guidance of attention toward the salient global form of a stimulus
is disrupted. Our results are clearly in agreement with the
aforementioned roles of the parietal cortex. Taken together, the
data showing loss of GM in the right parietal and visual areas in
some 6-year-olds may reflect anatomical maturation processes that
allow children to shift from a mode of local to global processing of
visual information. Our results also suggest that a neurodevelop-
mental disorder of the dorsal stream, including in the right parietal
and visual regions found in the present work, would create specific
difficulties in processing global visual information. Recent
neurodevelopmental data in individuals with Williams syndrome
are in agreement with this idea [27]. Williams patients, usually
defined as local spatial processors [28], present specifically reduced
parietal and visual dorsal activation during global processing,
whereas activation in the ventral occipito-temporal cortex is
equivalent to controls. These results fit well with our findings that
the emergence of a global visual preference in healthy children is
accompanied by GM loss in the occipito-parietal dorsal pathway
of the brain.
Finally, the present findings may provide a better understanding
of some psychiatric disorders, such as schizophrenia. Indeed,
global information processing is defective even in the early stages
of perception in schizophrenia patients, resulting in a visual
attraction toward the local properties of real-world scenes [29].
Table 1. Anatomic localization, localization extent, MNI coordinates, and Z scores for maximal gray matter volume differences
between the local bias group and the global bias group of children.
Anatomic localizationNumber of voxels Hemisphere
MNI coordinates
Z score
XYZ
Local bias minus Global bias
Calcarine 204R4
2100
253.94
Lingual279R 13
290
2193.93
Inf/Mid Occipital 278R28
297
283.83
R 24
2102
22 3.16
Precuneus224R8
256 65 3.73
60R8
26752 3.56
Postcentral56R 44
239663.51
Lingual58L
222
271
213.43
Global bias minus Local bias
No significant difference
L: left; R: right.
doi:10.1371/journal.pone.0020879.t001
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Difficulties in processing global information in schizophrenia
patients are proposed to be due to impairment of the dorsal
pathway [30]. According to the recent view that impairment in
brain structure maturation is responsible, at least in part, for
schizophrenia [31], the use of VBM with a focus on the brain
regions identified in this study may be useful for exploring the
neurodevelopmental origins of this pathology.
In conclusion, how we perceive the visual world as a coherent
whole has been a central question in experimental psychology
since the end of the 19thcentury [32]. Since the end of the 20th
century, brain imaging techniques in adults and neuropsycholog-
ical findings in children have given us a greater understanding of
the neural basis of visual processing [12,15]. The present study is
the first to report specific brain regions that are involved in the
perception of global visual information in healthy children.
Acknowledgments
The authors thank the children who participated in the study and their
families.
Author Contributions
Conceived and designed the experiments: NP GL AP OH. Performed the
experiments: GL GP CL AL MRT SR AP OH. Analyzed the data: NP GS
MC GL. Contributed reagents/materials/analysis tools: NP GS MC OH.
Wrote the paper: NP.
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