Developmental Science 17:1 (2014), pp 1–10 DOI: 10.1111/desc.

12093

PAPER
Parallel development of ERP and behavioural measurements of
visual segmentation
Carlijn van den Boomen,1,2 Victor A.F. Lamme3 and Chantal Kemner1,2,4
1. Department of Experimental Psychology, Helmholtz Institute, Utrecht, The Netherlands
2. Department of Developmental Psychology, Utrecht University, The Netherlands
3. Brain and Cognition, Department of Psychology, Faculty of Behavioral and Societal Sciences, University of Amsterdam,
The Netherlands
4. Rudolf Magnus Institute of Neuroscience, Department of Child and Adolescent Psychiatry, University Medical Centre, Utrecht,
The Netherlands

Abstract
Visual segmentation, a process in which elements are integrated into a form and segregated from the background, is known to
differ from adults at infancy. The further developmental trajectory of this process, and of the underlying brain mechanisms,
during childhood and adolescence is unknown. The aim of the study was to investigate the developmental trajectory of ERP
reflections of visual segmentation, and to relate this to behavioural performance. One hundred and eleven typically developing
children from 7 to 18 years of age were divided into six age groups. Each child performed two visual tasks. In a texture
segmentation task, the difference in event-related potential (ERP) response to homogeneous (no visual segmentation) and
checkered stimuli (visual segmentation) was investigated. In addition, behavioural performance on integration of elements into
contours was measured. Both behavioural and ERP measurements of visual segmentation differed from adults in 7–12 year-old
children. Behaviourally, young children were less able to integrate elements into a contour than older children. In addition, a
developmental change was present in the ERP pattern evoked by homogeneous versus checkered stimuli. The largest differences
in behaviour and ERPs were found between 7–8- and 9–10-, and between 11–12- and 13–14-year-old children, indicating the
strongest development between those age groups. Behavioural as well as ERP measurements at 13–14 years of age showed
similar results to those of adults. These results reveal that visual segmentation continues to develop until early puberty. Only by
13–14 years of age, children do integrate and segregate visual information as adults do. These results can be interpreted in terms
of functional connectivity within the visual cortex.

Introduction involved in the processing of basic features of small

The pace of brain development differs between brain
areas, and sensory areas, such as the visual cortex, show a
strong development relatively early in life, although they
continue to develop until at least early puberty (Gogtay,
Giedd, Luck, Hayashi, Greenstein, Vaituzis, Nugent,
Herman, Clasen, Toga, Rapoport & Thompson, 2004;
van den Boomen, van der Smagt & Kemner, 2012). This
development involves changes both within visual brain
areas, as well as in the connections between them, affecting
the flow of information between lower- and higher-level
areas of the visual hierarchy. Lower-level visual areas are
elements, such as line orientation; higher-level visual areas
in processing more general information on global parts of
an object, such as its shape (for a review, see Nassi &
Callaway, 2009). The full processing of an object relies on
processes in both lower and higher areas and involves,
among others, visual integration of local elements into a
form, detection of its borders, and segregation of this form
from its background, together leading to visual segmen-
tation (also known as visual or texture segregation). This
process is required for perception of objects such as faces,
geometric forms and letters, and therefore plays an
important role in social and cognitive development.

Address for correspondence: Carlijn van den Boomen, Utrecht University, Department of Experimental Psychology, Heidelberglaan 2, Van Unnik
Building Room 16.17, 3584 CS Utrecht, The Netherlands; e-mail: C.vandenboomen@uu.nl

© 2013 John Wiley & Sons Ltd

2 Carlijn van den Boomen et al.
Lamme and Roelfsema proposed a model to explain
the role of different types of neural functional connec-
tivity in visual segmentation (Lamme, Super & Spe-
kreijse, 1998; Lamme & Roelfsema, 2000; Roelfsema,
Lamme, Spekreijse & Bosch, 2002). In the model, there
are two types of connectivity: the first is feedforward
connectivity distributing information from lower (i.e. V1)
to higher areas (i.e. V2 and higher). The second is
recurrent connectivity, which can be subdivided into
feedback connectivity from higher to lower areas and
horizontal connectivity within brain areas. Visual
segmentation is eventually established using recurrent
connectivity.
The model is supported by research using single-cell
recording in the monkey visual brain (e.g. Lamme, 1995;
Zipser, Lamme & Schiller, 1996; Lamme et al., 1998;
Super, Spekreijse & Lamme, 2001). In these studies, the
contribution of different types of connectivity to the
processing of specific visual stimuli was investigated.
Typically, two types of stimuli are used: homogeneous
and textured stimuli such as checkered ones (Figure 1).
The latter type contains a pattern that can be processed
by integrating the oriented line elements within each
check and segregating the different checks from each
other. It was revealed that recurrent signals from higher-
level visual areas back to V1 are necessary for the
successful segmentation of textured stimuli, but not for
processing of homogeneous ones. This specific neural
signalling related to visual segmentation in monkeys is
typically expressed in the modulation of responses at
latencies beyond 100 ms, i.e. relatively late compared to
the signals related to feedforward processing (starting at
40 ms) (e.g. Lamme, 1995; Zipser et al., 1996; Lamme
et al., 1998; Super et al., 2001). Using the same para-
digm, a similar modulation of activation was found in
the event-related potential (ERP) of human adults,
expressed as a more negative peak for checkered than
homogeneous stimuli, also at somewhat longer latencies
and largest at the occipital electrodes (e.g. Lamme, van
Dijk & Spekreijse, 1992; Bach & Meigen, 1992, 1998;
Figure 1 Stimuli used in the texture segmentation task;
homogeneous (left) and checkered (right) stimuli.
© 2013 John Wiley & Sons Ltd
Figure 2 Examples of contours with different relative noise
density (left D = 1.2; right D = 0.75).
Caputo & Casco, 1999; Scholte, Jolij, Fahrenfort &
Lamme, 2008).
Behavioural investigations can also be informative on
connectivity processes involved in segmentation. In the
well-established contour integration task (Kovacs &
Julesz, 1993), the focus has been on the process of
integration of visual elements, an important aspect of
segmentation. Stimuli in this task contain Gabor ele-
ments forming a contour, which needs to be detected in a
background with a varying amount of randomly posi-
tioned and oriented Gabor elements (noise) (Figure 2,
where contours are circular; Kovacs & Julesz, 1993;
Kovacs, 2000; Hadad, Maurer & Lewis, 2010). Due to
the distance between Gabors, integration of elements
into a contour is proposed to depend on recurrent
connections (e.g. Angelucci, Levitt, Walton, Hupe,
Bullier & Lund, 2002; Gilbert, 1998; Kovacs, Kozma,
Feher & Benedek, 1999; Stettler, Das, Bennett & Gilbert,
2002; Zhang & von der Heydt, 2010). The level of noise
in which adults can detect the contour, providing insight
into their recurrent connectivity, is well investigated
(Kovacs & Julesz, 1993; Hess, Hayes & Field, 2003).
Thus, both ERP and behavioural research have increased
our understanding of recurrent connectivity in the adult
visual cortex.
In children, behavioural research suggests that visual
segmentation improves until 13 years of age (Sireteanu &
Rieth, 1992; Kovacs, 2000; Hadad et al., 2010), but the
specific changes in underlying mechanisms are less well
understood. ERPs evoked by textured stimuli have only
been investigated in infants (Arcand, Tremblay,
Vannasing, Ouimet, Roy, Fallaha, Lepore, Lassonde &
McKerral, 2007).1 In the first year of life, the modulation
of brain activity evoked by checkered versus homogeneous
stimuli changes with age, but still differs from adults at
1 year of age. It is unknown which developmental changes
1
This process was studied in 13-year-old children as well (Kemner,
Lamme, Kovacs & van Engeland, 2007), but not in a developmental
perspective since results were not compared to adults.

in brain functioning related to visual segmentation are
present after this age.
The aim of the current study was to investigate the
developmental trajectory of ERP reflections of visual
segmentation in children from 7 to 18 years of age in a
texture segmentation task using the homogeneous and
checkered stimuli (Figure 1), as described above. In
addition, we investigated behavioural performance using
the contour integration task, aiming to replicate the
previously reported developmental trajectory (Kovacs,
2000; Hadad et al., 2010), and investigate possible
improvements in this task after 13 years of age. Fur-
thermore, our goal was to compare the developmental
trajectories of behavioural and ERP measurements.
Stimuli in both tasks are thought to require recurrent
connectivity, and we therefore hypothesize a parallel
developmental trajectory of both measurements.
Using the texture segmentation and contour integra-
tion tasks, we will be able to uncover the developmental
trajectory of the neurocognitive mechanisms underlying
visual segmentation. This is imperative to better appre-
ciate the biological basis of developmental transitions in
processing of relatively complex visual information. In
addition, increased knowledge of the typical develop-
mental trajectory of visual segmentation and recurrent
connectivity can help in gaining insight into disorders
such as autism spectrum disorder, schizophrenia, and
Williams syndrome where development of these visual
processes seems to go astray (Gervan, Gombos &
Kovacs, 2012; Kemner et al., 2007;Silverstein, Keane,
Barch, Carter, Gold, Kovacs, MacDonald, Ragland &
Strauss, 2012; Vandenbroucke, Scholte, van Engeland,
Lamme & Kemner, 2008, 2009).
Methods
Participants
A total of 111 children took part in the study, divided
into six age groups: 7–8 years (n = 9), 9–10 years
(n = 14), 11–12 years (n = 15), 13–14 years (n = 28),
15–16 years (n = 30), and 17–18 years (n = 15). The last
group (17–18-year-olds) is also referred to as ‘adults’
throughout the results and discussion sections. All
children were male, and there were no significant
Table 1 Average age in years and total IQ (standard error) per age group
Group 7–8 9–10 11–12
Age 8.3 (.23) 10.1 (.14) 11.9 (.15)
IQ 112.3 (4.5) 112.7 (3.3) 112.3 (3.1)
© 2013 John Wiley & Sons Ltd
Development of visual segmentation 3
differences between groups on IQ, as measured using a
shortened version of the Wechsler Intelligence Scale for
Children, revised Dutch version (WISC-RN). Average
age and IQ of the groups are summarized in Table 1.
Children were recruited from elementary and high
schools in and around Utrecht and Someren (The
Netherlands). The medical ethical committee of the
University Medical Center Utrecht approved the study,
in accordance with the Declaration of Helsinki. All
parents or caretakers gave written informed consent
prior to participation, after explanation of the procedure.
Tasks and procedures are equal to those previously
described in Kemner et al. (2007).
Contour integration task
A card version of the contour integration task was used
(Kovacs et al., 1999; Kovacs, 2000). A contour integra-
tion card contains multiple Gabor elements, forming a
closed circular figure (contour) embedded in a back-
ground of randomly positioned and oriented distracters
(orientation; Figure 2). The contour had a random
position to avoid stereotyped responding. Each Gabor
element had a carrier spatial frequency of 5 c/deg at a
viewing distance of 50 cm, and a luminance contrast of
about 95%, printed on white paper. All cards had fixed
inter-element spacing along the contour of 8 wavelengths
(8k) of the carrier, center-to-center (1.6°). Participants
were asked to identify the contour by pointing out the
full path of the circle, which was scored as correct if they
were able to indicate the total contour at the correct
location and as fail if they either could not point out any
contour or pointed out noise (only one closed contour
was present per card). The difficulty of the task depends
on the relative noise density (D) of the stimulus. D is
defined as the ratio of average noise spacing over
contour spacing, and varied between 0.5 and 1.2 in steps
of 0.05. A maximum of 15 cards per set was presented in
a decreasing order of D, and thus in an increasing order
of difficulty. The last card on which the contour was
correctly identified defined the threshold. A simple
staircase procedure was applied to measure the thresh-
old, in which progression was allowed if a card was
missed, but a reversal occurred when the following card
was missed as well. The task was terminated when the
contour on a specific card could not be detected twice.
13–14 15–16 17–18
14.2 (.10) 16.0 (.10) 17.7 (.18)
104.9 (2.7) 109.5 (2.3) 106.4 (3.0)
4 Carlijn van den Boomen et al.

Texture segmentation task eye-movements) (Gratton, Coles & Donchin, 1983).

Epochs with additional amplitude artifacts were removed.
To investigate the differential activation evoked by
These artifacts were defined by a voltage change of more
checkered (textured) versus homogeneous stimuli, a
than 50 lV per sampling point, a voltage difference of less
texture segmentation task was performed. Stimuli con-
than 3 lV per 200 ms, or amplitudes below 100 or above
sisted of 45- or 135-degree oriented black line segments,
100 lV. ERP were averaged separately for the checker-
randomly positioned on a white background (total 450
board and homogeneous stimuli. Next, subtracting the
line segments; 100% luminance contrast). The lines were
ERP evoked by the homogeneous from that evoked by the
organized either into homogeneous (eight different stim-
checkered stimuli created a difference wave that selectively
uli) or into checkered stimuli (also eight different stimuli;
extracts the neural signals related to image segmentation
see Figure 1 for an example) such that local modulations
while discarding any signals related to the processing of
are, on average, equally distributed between the two types
lower-level features such as the line segments and their
of stimuli, but that stimuli are presented in a homoge-
orientation. The electrode of interest was Oz, which was
neous or checkered fashion, thus modulating the amount
determined based on previous research (e.g. Lamme et al.,
of segmentation independently of the changes in orienta-
1992) and was confirmed by visual inspection of ERP
tion that occur on each transition from one stimulus to the
patterns in other electrodes (Figure 3) and topographies
next (see Lamme et al., 1992, for a full explanation of this
of the activity (Figure 4). These figures showed that for all
balancing of local modulation). Stimuli subtended
age groups the segmentation activity is present at the Oz
17.5 9 13 degrees of visual angle at a viewing distance
electrode, and that the pattern of segmentation is not
of 57 cm. Homogeneous and checkered stimuli were
substantially different from Oz at other electrodes (if
alternated every 500 ms (2 Hz). The basic sequence
present). All pre-processing steps were carried out using
consisted of the 16 stimuli presented in a fixed order.
Brain Vision Analyzer (Brain Products GmbH, Munich,
A total of 800 stimuli were presented (400 per condition)
Germany).
on a Dell Latitude D610 laptop. Participants performed
In the difference wave, two peaks were of interest for the
an oddball task on Pokemon cartoons presented at
analyses: first the typical texture negativity (TN;
random timepoints during the task. Stimuli were previ-
Figure 5), described in previous research. Secondly,
ously described by Lamme et al. (1992) and the task has
ERP waveforms of the younger children revealed an
previously been described by Kemner et al. (2007).
additional positive peak. This peak was present before the
TN, and is referred to as the texture positivity (TP;
EEG recordings and analyses Figure 5) in the current paper. The texture positivity was
semi-manually scored as the most positive point (global
Electroencephalographic activity was recorded from 32
maximum) directly preceding texture negativity (i.e. peak
electrodes using a Biosemi Active Two EEG system
was automatically detected, but manually corrected if the
(Biosemi, Amsterdam, The Netherlands). Electrodes
criterion of preceding the texture negativity was not
were positioned at standard EEG recording locations
satisfied). Scoring was performed semi-manually to pre-
according to the international 10/20 system. Vertical
vent mis-detection of possible positive peaks following the
EOG was recorded from electrodes placed above and
TN. Texture negativity was automatically scored as the
below the left eye, and horizontal EOG from electrodes
most negative point (global maximum) between 130 and
placed at the outer canthi of the eyes. An additional
190 ms post-stimulus. Peak amplitude and latency of
electrode was placed at the right mastoid for offline
both the TP and the TN were exported for further
re-referencing purposes. During recording, EEG was
analyses. Four one-way analyses of variance (ANOVA)
sampled at a rate of 2048 Hz. Two electrodes in the cap,
were carried out using PASW 18 (SPSS Inc., Chicago, IL,
the CMS (common Mode Sense) and DRL (driven Right
USA), with latency and amplitude of the TP and the TN
Leg) provided an ‘active ground’.
as the dependent variables, and age as the between-
Raw data were re-referenced offline to the right mastoid.
subjects factor. For all reported analyses, the alpha value
Then data were re-sampled to 512 Hz, and filtered with a
was set at .05 and all post-hoc analyses are comparisons of
high-pass filter of 1 Hz, a low-pass filter of 30 Hz and a
an age group with its following age group (e.g. 7–8- with
notch filter of 50 Hz. In order to compute ERPs, epochs of
9–10-year-old children), performed by univariate analyses
50 ms pre-stimulus (baseline) to 400 ms post-stimulus
with repeated contrasts. These tests were performed with
were extracted from the continuous data. Ocular artifacts
two-way analyses for ERPs, and one-way analyses for the
were removed from the EEG with a regression analysis
contour task due to the specific hypothesis of an
based on eye movements detected by vertical EOG
improvement with age (Hadad et al., 2010; Kovacs, 2000).
(blinks) and horizontal EOG electrodes (horizontal

© 2013 John Wiley & Sons Ltd

 Development of visual segmentation 5

Figure 3 Grand averages of ERPs at occipital and parietal electrodes, evoked by checkerboard and homogeneous stimuli, and the
difference wave between stimuli, for the age groups investigated. Black and grey lines are placed at latency of P1 and N2 peaks,
respectively, in the oldest age group (17–18 years). The figure shows that the pattern of segmentation as represented in the difference
wave is not substantially different at other electrodes than Oz, which was chosen as electrode of interest for analyses.

107) = 8.3, p < .001). Younger children detected con-

tours in fewer cards as compared to older children. Post-
hoc analyses revealed a significant difference between
7–8- and 9–10- (contrast estimate = 1.5; p < .05), and
between 11–12- and 13–14-year-old children (contrast
estimate = 1.0; p < .05). Performance values (mea-
sured in D-threshold) are depicted in Figure 6e.

EEG

Figure 4 Activity maps representing the distribution of the Texture positivity

difference in brain activity between checkered and
homogeneous stimuli over the 32 EEG electrodes. Maps are
plotted per age group at the moment of maximum peak
amplitude for the Texture Positivity (TP) and the Texture
Negativity (TN).
Performance on the contour integration task was
analysed in a one-way analysis of variance (ANOVA),
with number of correct-detected cards as dependent
variable, and age as between-subjects factor.
Results
Contour integration test
Analyses revealed a significant effect of age on the
number of cards with correctly detected contours (F(5,
A main effect of age on latency of the texture positivity
(F(5, 105) = 8.0; p < .001) indicated that younger chil-
dren showed longer latencies than older children. Post-
hoc analyses revealed a significant difference between
11–12- and 13–14-year-old children (contrast esti-
mate = 23.6; p < .001). Latency values are depicted in
Figure 6a. However, the TP peak amplitude was close to
zero in 13–18-year-old children, which could affect peak
detection and thus latency analyses. To provide further
support for a latency change between 11–12 and
13–14 years, ERP peaks evoked by checkerboard and
homogeneous images, rather than difference waves, were
studied as well. The TP peak originated from the
difference in activity evoked by checkerboard versus
homogeneous stimuli at the P1 peak, which was larger
than zero in all age groups (Figure 3). Additional
analyses were performed confirming an effect of age on
latency of the P1 peak (checkerboard: F(5, 105) = 5.6;

© 2013 John Wiley & Sons Ltd

6 Carlijn van den Boomen et al.

(a) (b)

Figure 5 Difference waves of grand averages evoked by (c) (d)

checkerboard versus homogeneous stimuli for the age groups
investigated. Peaks of interest are the texture positivity (TP) and
the texture negativity (TN).

p < .001; homogeneous: F(5, 105) = 6.8; p < .001). Post-

hoc analyses revealed a significant difference between
11–12- and 13–14-year-old children (checkerboard: con-
trast estimate = 7.5; p < .05; homogeneous: contrast
estimate = 12.7; p < .001). Post-hoc analyses showed
that for the checkerboard stimuli, the P1 latency also
decreased between 7–8 and 9–10 years (contrast esti-
mate = 10.1; p < .05). (e)
A main effect of age on amplitude of the texture
positivity (F(5, 105) = 9.4, p < .001) indicated that
younger children showed larger amplitudes than older
children. Post-hoc analyses revealed a significant differ-
ence between 7–8- and 9–10-year-old children (contrast
estimate = 2.3; p < .001). Amplitude values are depicted
in Figure 6b.

Texture negativity
A main effect of age on latency of the texture negativity
(F(5, 105) = 5.7, p < .001) indicated that younger chil-
dren showed longer latencies than older children. Post-
hoc analyses revealed a significant difference between
11–12- and 13–14-year-old children (contrast esti-
mate = 9.1; p < .05). Latency values are depicted in
Figure 6c.
A main effect of age on amplitude of the texture
negativity (F(5, 105) = 3.0, p < .05) indicated that youn-
ger children showed less negative amplitudes than older
children. Post-hoc analyses revealed a significant differ-
ence between 7–8- and 9–10-year-old children (contrast
estimate = 2.7; p < .01). Amplitude values are depicted
in Figure 6d.
The current data are not suitable for determining with
certainty whether changes in the TP and the TN reflect
Figure 6 Average values per age group on (a) Texture
positivity amplitude; (b) Texture positivity latency; (c) Texture
negativity amplitude; (d) Texture negativity latency; (e)
Contour integration performance. Asterisks show significant
differences between age groups.
independent processes, and it is possible that the changes
in latency and amplitude of the TP influence those of the
TN. The age differences in the TN could therefore be due
to differences in the TP. To examine whether this was the
case, we investigated whether the effects of age on the TN
latency and amplitude are still present when taking the
TP latency and amplitude as a covariate. Covariance
analyses (one-tailed testing) showed that the effects of
age on texture negativity amplitude were no longer
present when corrected for texture positivity amplitude

© 2013 John Wiley & Sons Ltd


(F(5, 104) = .67; p > .05). There was still a linear effect
of age on texture negativity latency when corrected for
texture positivity latency (Contrast estimate = 9.985;
p < .05).
Conclusion and discussion
The current study aimed to investigate the development
of ERP reflections of visual segmentation, a process that
is crucial to higher-order processes, to provide informa-
tion on the development of specific neural mechanisms
involved and relate this to behavioural performance. We
revealed a parallel development of both ERP and
behaviour over childhood and adolescence.
More specifically, we measured the ability to behavio-
urally detect a circle (contour) among increasing values
of relative noise density (D), referred to as contour
integration. The lower the D-value, the more difficult it is
to integrate contours. This task showed that the D-value
at which a contour can be detected decreased with age,
with the largest changes from 7–8 to 9–10, and from
11–12 to 13–14 years of age. In the latter group,
performance was almost equal to adults. It should be
noted that the absence of significant change between
9–10- and 11–12-year-old children does not necessarily
imply no change at all between these ages, and that for
instance a lack of power could have affected the results.
Development until late childhood in this task is in
accordance with previous findings (Kovacs et al., 1999;
Kovacs, 2000). Based on multiple studies using animals
and computational models (e.g. Angelucci et al., 2002;
Gilbert, 1998; Stettler et al., 2002; Zhang & von der
Heydt, 2010) it has previously been proposed that
contour integration among increasing noise levels (i.e.
decreasing D-levels) requires increasing activation in
recurrent connections between neurons (e.g. Hess &
Field, 1999; Kovacs et al., 1999). The lower performance
in young children thus implies an immaturity of recur-
rent connectivity.
In the texture segmentation task we investigated the
difference in brain activity evoked by checkered versus
homogeneous stimuli in order to explore the specific
developmental changes in neural mechanisms underlying
visual segmentation, especially the maturation of recur-
rent connectivity. Visual segmentation is reflected in a
negative peak (texture negativity or TN) in the so-called
difference wave between ERPs evoked by checkered
versus homogeneous stimuli (e.g. Lamme et al., 1992;
Bach & Meigen, 1992, 1998; Caputo & Casco, 1999;
Scholte et al., 2008). Results of the current study showed
a negative deflection in all age groups, with increasing
negativity from 7–8 to 9–10 years of age. At a later age,
© 2013 John Wiley & Sons Ltd
Development of visual segmentation 7
from 11–12 to 13–14 years of age, the latency of the TN
was decreasing. Moreover, the results showed that in
younger children the difference wave contained an
additional positive difference (Textured Positivity, TP)
preceding the TN. This peak was most apparent in the
7–8-year-old children, and showed a large decrease in
amplitude until 9–10 years of age, after which the
amplitude was close to zero lV. The latency of the TP
showed a large decrease from 11–12 to 13–14 years of
age. The TP and TN thus both show large changes in
amplitude from 7–8 to 9–10, and in latency from 11–12
to 13–14 years of age, when the ERP pattern resembled
that of adults. The ERP results imply that there are two
stages in development. The first is a transition from an
early-in-time process involved in visual segmentation in
younger children (represented by the TP) to a later-in-
time process in older children (represented by the TN).
Subsequently, there is a general increase in speed of
processing, represented by the shorter latencies of the TP
and TN with increasing age.
Based on ERP and behavioural measurements, no
solid conclusions can be drawn regarding the underlying
mechanisms of the developmental trajectory that is
revealed. We here propose a possible mechanism con-
tributing to the observed changes. Although we did not
directly measure functional connectivity in the brain,
considering the processes theoretically involved in visual
segmentation we could hypothesize that the first devel-
opmental stage is related to increasing involvement of
feedback processes with age, and the second to increased
speed of processing due to myelinization (see discussion
below).
With respect to the increasing role of feedback
processes in visual segmentation with age, we separately
considered the possible role of horizontal and feedback
connectivity. The former mediates detection of borders;
the latter facilitates the grouping of elements of a figure
that is represented by the borders in higher areas such as
IT (Roelfsema et al., 2002). Horizontal and feedback
connectivity are together involved in the generation of
the difference wave, and thus in the TP and TN peaks.
We speculate that each of these types of connectivity is
more prominently involved in the generation of one of
the ERP peaks: horizontal connectivity in generation
of the TP peak, and feedback connectivity mainly in that
of the TN peak. This distinction is based on the order of
the peaks and processes involved: the TP, horizontal
connectivity, and border processing precede the TN,
feedback connectivity, and grouping, respectively (Lam-
me, Rodriguez-Rodriguez & Spekreijse, 1999; Lamme &
Roelfsema, 2000). Evidence for a functional distinction
between early and late segmentation-related activity also
comes from EEG studies in adults. In these studies,
8 Carlijn van den Boomen et al.
stimuli with varying amounts of borders and groups or
figures were presented. Results showed an early activity
related to border processing and later activity related to
grouping (Caputo & Casco, 1999; Scholte et al., 2008).
The ascription of the prominent involvement of hori-
zontal versus feedback connectivity in the generation of
the TP versus TN peaks implies a relative decrease of
horizontal and increase of feedback connectivity
involved during the first developmental stage between
7–8 and 9–10 years. A possible mechanism contributing
to this change is synaptic pruning, resulting in a decrease
of horizontal connections. The second developmental
stage, characterized by decreasing latency, could possibly
be related to increased myelinization of connections.
Myelinization results in increased speed of processing,
which is reflected in decreasing latencies of the ERP
peaks involved in visual segmentation. It has been
previously shown that myelinization continues until late
childhood in the visual cortex (Paus, Collins, Evans,
Leonard, Pike & Zijdenbos, 2001).
Two developmental stages were observed in the
behavioural contour integration task as well. However,
before generalizing the hypothesized changes in recur-
rent connectivity from the ERP to the behavioural task,
the specific types of connectivity possibly involved in
each of the tasks should be considered. For both tasks,
the involvement of feedback connectivity has been
suggested. Therefore, the proposed increasing role of
feedback connectivity over development could underlie
developmental changes in the ERP and behavioural
tasks. However, a distinction has been made regarding
the involvement of specific horizontal connections in
each of the tasks. Structurally, a subdivision can be made
into short- (<0.5 mm) and long-range (<5 mm) horizon-
tal connectivity (Gilbert & Wiesel, 1985; Rockland &
Lund, 1983; Wielaard & Sajda, 2006). Functionally,
short-range connections are thought to be involved in
discriminating nearby stimuli with different orientations,
whereas long-range connections are involved in connect-
ing further-away stimuli with similar orientations (e.g.
Das & Gilbert, 1999; Wielaard & Sajda, 2006; Angelucci
et al., 2002). Contour integration probably relies mainly
on long-range connections, which are increasingly
required in larger distances between contour elements
and in increasing noise levels (Hess & Field, 1999;
Kovacs, 2000). The checkered stimuli in the ERP task
contain borders, which are plausibly processed using
short-range horizontal connectivity, although this has
not been specifically investigated. Due to this distinction,
the decreasing role of horizontal connectivity, proposed
in the ERP task, cannot be generalized to the behavio-
ural contour integration task. Instead, the current results
suggest that short-range connectivity decreases and
© 2013 John Wiley & Sons Ltd
long-range connectivity increases with age. Thus, we
hypothesize that both feedback and long-range horizon-
tal connectivity become increasingly involved during the
first developmental stage that was described in the
present study. The potential cause of the second devel-
opmental stage, i.e. myelinization, could be generalized
to explain the decreased thresholds in the contour
integration task because myelinization would increase
speed of processing in both feedback and long-range
horizontal connectivity, which might lead to faster and
possibly better or more efficient processing.
Altogether, based on the proposed underlying processes
of visual segmentation we speculate that the developmen-
tal changes in ERPs and behavioural performance
between 7–8 and 9–10 years of age can be related to a
relatively increased involvement of long-range horizontal
and feedback connectivity as compared to short-range
horizontal connectivity. This stage would reflect a qual-
itative change in processes. The second stage, from 11–12
to 13–14 years of age, characterized by decreasing latency
of ERP peaks and improved behavioural performance,
could be related to myelinization and would thus involve a
quantitative change. These results match with the previ-
ously reported decrease in short-range functional connec-
tivity within, and increase in long-range functional
connectivity between, areas over the whole brain during
infancy and childhood (e.g. Supekar, Musen & Menon,
2009; Vakorin, Lippe & McIntosh, 2011). Based on the
current results we speculate that these specific changes in
connectivity also occur within the visual cortex, and are
specifically related to behavioural maturation. Future
research is required to investigate this hypothesis.
We here propose changes in specific recurrent connec-
tions as underlying mechanisms of developmental dif-
ferences in visual segmentation, but acknowledge that
this mechanism cannot explain all the results of the
current and previous studies.2 The proposed mechanisms
of change, i.e. pruning and myelinization, cannot fully
explain the observed changes in peak amplitude and
latency. Pruning of connections, as is now proposed to
contribute to the decreasing TP peak, is not restricted to
horizontal connections but occurs in feedback connec-
tions as well. This would result in a decrease in the TN
peak amplitude, which is not observed in the current
data. Future research is required to investigate to what
extent pruning occurs in different neuronal connections
and whether this can explain the changes in TP and
TN peaks. In addition, although myelinization in the
occipital cortex continues throughout childhood (Paus
2
An anonymous reviewer substantially contributed to the following
discussion.

et al., 2001), it is unlikely to change so considerably
between 11–12 and 13–14 years of age as to fully explain
the current results. Furthermore, the current interpreta-
tion does not fully match previous findings, in that it
implies at least a lower contribution of horizontal
connections in older than younger children. These
connections are, however, also present and contributing
to segmentation in older children and adults (Lamme
et al., 1998). However, some changes in (long-range)
connectivity over childhood have been previously
reported (Supekar et al., 2009; Vakorin et al., 2011)
and are proposed to affect segmentation processes
(Kovacs, 2000). Although it is very unlikely that
horizontal and feedback mechanisms function com-
pletely differently in younger children compared to
adults, some changes in the behavioural outcome have
been proposed (Kovacs, 2000). Thus, it is still under
debate to what extent and via which mechanisms
connectivity develops throughout childhood in the visual
cortex, and to what extent this can explain developmen-
tal changes in segmentation.
Moreover, other possible interpretations of ERP results
and limitations in the comparison of tasks should be
noted. First, the presence of the TN in the youngest age
group, and the subsequent development in older children
could be influenced by that of the TP. For example, the
negativity defined as the TN could in the youngest age
group represent a fading of activity in neurons generating
the TP, which would lead to the conclusion that the TN is
absent. Another possibility could be that all changes
observed in the TN are due to that in the TP, and that
neurons generating the TN are thus as active in all age
groups. Covariance analyses on developmental changes
observed in the TP and TN did however reject this last
possibility, showing that changes in the TN occur
independently of those in the TP. Overall, it can still be
concluded that the TP is more prominent in younger
children, whereas the TN does resemble more adult-like
characteristics in older children. Another limiting aspect
includes factors such as structural changes in cortical
folding that influence the position of neurons and thus
whether their activity can be recorded using EEG, which
could affect the peak amplitudes (Luck, 2005). Moreover,
in the comparison between ERP and behavioural results it
should be kept in mind that this represents a correlation
rather than a causal relation and that other aspects, such as
attention and motivation, affect each of the measurements
in a different way (for an extensive discussion, see Boon,
Suttle & Dain, 2007; van den Boomen et al., 2012).
Therefore, the current results should be interpreted with
caution.
In conclusion, the current study revealed a parallel
development of behavioural and ERP measurements
© 2013 John Wiley & Sons Ltd
Development of visual segmentation 9
underlying visual segmentation between 7–8 and
13–14 years of age in the same children, and a more
specific difference between two developmental stages is
demonstrated by the ERP results. The underlying
mechanisms, proposed to be specific aspects of recurrent
connectivity in the visual cortex, have matured at 13–14
years of age.
Acknowledgements
The authors would like to thank Emmie van Schaffelaar
for her contribution to the data collection, and Sascha
Morel and the lab groups of Chantal Kemner and Frans
Verstraten for discussion and comments. We also thank
two anonymous reviewers for their thoughtful com-
ments. C. van den Boomen and C. Kemner are
supported by a VICI Grant from the Dutch Organiza-
tion for Scientific Research (NWO) granted to C.
Kemner. V.A.F. Lamme is supported by an Advanced
Investigator Grant (DEFCON1) from the European
Research Council (ERC).
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Received: 18 July 2012
Accepted: 9 May 2013