brain research 1558 (2014) 33–43

Available online at www.sciencedirect.com

www.elsevier.com/locate/brainres

Research Report

Functional organization of intrinsic connectivity

networks in Chinese-chess experts

Xujun Duana,1, Zhiliang Longa,1, Huafu Chena,n, Dongmei Liangb,c,

Lihua Qiud, Xiaoqi Huangd, Timon Cheng-Yi Liub,n, Qiyong Gongd
a
Key Laboratory for NeuroInformation of Ministry of Education, School of Life Science and Technology,
University of Electronic Science and Technology of China, Chengdu 610054, PR China
b
School of Physical Education & Sports Exercise, South China Normal University, University Town, Guangzhou 510006,
PR China
c
Center for Studies of Psychological Application, School of Psychology, South China Normal University, Guangzhou
510631, PR China
d
Huaxi MR Research Center, Department of Radiology, West China Hospital of Sichuan University, 610041, PR China

art i cle i nfo ab st rac t

Article history: The functional architecture of the human brain has been extensively described in terms of
Accepted 17 February 2014 functional connectivity networks, detected from the low-frequency coherent neuronal
Available online 22 February 2014 fluctuations during a resting state condition. Accumulating evidence suggests that the

Keywords: overall organization of functional connectivity networks is associated with individual

Chess expert differences in cognitive performance and prior experience. Such an association raises the

Resting-state fMRI question of how cognitive expertise exerts an influence on the topological properties of

Functional connectivity network large-scale functional networks. To address this question, we examined the overall

Graph theoretical analysis organization of brain functional networks in 20 grandmaster and master level Chinese-

Small-world topology chess players (GM/M) and twenty novice players, by means of resting-state functional
connectivity and graph theoretical analyses. We found that, relative to novices, functional
connectivity was increased in GM/Ms between basal ganglia, thalamus, hippocampus, and
several parietal and temporal areas, suggesting the influence of cognitive expertise on
intrinsic connectivity networks associated with learning and memory. Furthermore, we
observed economical small-world topology in the whole-brain functional connectivity
networks in both groups, but GM/Ms exhibited significantly increased values of normalized
clustering coefficient which resulted in increased small-world topology. These findings
suggest an association between the functional organization of brain networks and
individual differences in cognitive expertise, which might provide further evidence of
the mechanisms underlying expert behavior.
& 2014 Elsevier B.V. All rights reserved.

n
Corresponding authors.
E-mail addresses: chenhf@uestc.edu.cn (H. Chen), liutcy@scnu.edu.cn (T.-Y. Liu).
1
Xujun Duan and Zhiliang Long contributed equally to this work.

http://dx.doi.org/10.1016/j.brainres.2014.02.033
0006-8993 & 2014 Elsevier B.V. All rights reserved.
34 brain research 1558 (2014) 33–43
1. Introduction
Task-free spontaneous neural activity has been proposed to
play an important part in maintaining ongoing representa-
tions of conscious activity in the resting brain, and it
demonstrates temporal coherence between brain regions that
are anatomically connected or functionally related (Biswal
et al., 1995; Raichle, 2010; Zhang and Raichle, 2010). Recently,
assessments of brain intrinsic functional connectivity were
conducted in order to investigate the level of integration of
brain systems at a resting state when no task is being
performed (Greicius et al., 2003). Along with intrinsic func-
tional connectivity analyses, graph theoretical approaches
have also emerged as powerful tools to explore brain organi-
zation on the level of large-scale functional networks
(Bullmore and Sporns, 2009; He and Evans, 2010). It is well
accepted that functional connections of brain networks are
organized in a highly efficient small-world manner, charac-
terized by a high level of neighborhood clustering and a short
average distance of nodes within the overall network (Achard
et al., 2006; Sporns et al., 2004).
Small-world attributes have been found in brain func-
tional networks measured from electroencephalography,
magnetoencephalography, functional magnetic resonance
imaging (Bassett and Bullmore, 2006; Ferri et al., 2007; Liao
et al., 2011a; Smit et al., 2008; Supekar et al., 2009), as well as
in brain anatomical networks using structural magnetic
resonance imaging and diffusion tensor imaging (Fan et al.,
2011; Gong et al., 2009; Hagmann et al., 2007; He et al., 2007).
There is increasing evidence that the small-world organiza-
tion of brain networks can be affected by normal aging
(Achard and Bullmore, 2007) and brain diseases, such as
schizophrenia (Liu et al., 2008; Wang et al., 2012; Yu et al.,
2011), Alzheimer's disease (Sanz-Arigita et al., 2010; Stam
et al., 2007), attention-deficit/hyperactivity disorder (Wang
et al., 2009b), and epilepsy (Liao et al., 2010; Ponten et al.,
2007; Wang et al., 2010). However, it has also been suggested
that learning and training can enhance functional organiza-
tion on the level of large-scale brain networks. For instance,
Voss et al. (2010) found that 1-year intervention trial of
aerobic training improved the aging brain's resting functional
connectivity as well as network efficiency in higher-level
cognitive networks, providing important evidence for
exercise-induced functional plasticity in large-scale brain
systems. A recent study conducted by Albert et al. (2009)
showed that motor learning modulated resting state net-
works in a positive manner, and another study performed by
Lewis et al. (2009) demonstrated that visual perceptual
learning modified the interaction and organization between
functional networks. Moreover, several recent studies also
suggested that the level of global communication efficiency of
the brain network is positively associated with individual
differences in cognitive performance. For instance, van den
Heuvel et al. (2009) demonstrated a strong negative relation-
ship between the normalized characteristic path length of the
resting-state brain network and intelligence quotient, sug-
gesting a positive association between the global efficiency of
functional brain networks and intellectual performance.
Another study performed by Li et al. (2009) showed that
people with higher intelligence tend to have greater global
efficiency of the brain anatomical network. This evidence
suggests an association between large-scale organization of
brain networks and individual differences in cognitive per-
formance as well as prior experiences. Such an association
raises the question of how cognitive expertise exerts
an influence on the topological properties of functional
networks.
The board game chess involves many aspects of high level
cognition and requires sophisticated problem solving skills
(Atherton et al., 2003), thus providing a good opportunity to
study the mechanisms underlying cognitive expertise (Wan
et al., 2011). In early psychological studies, researchers found
that, compared with novices, world-class grandmasters
searched much deeper and wider, using more efficient search
processes and more complex evaluation functions to assess
their decisions when detecting the best moves (Charness,
1981; Reynolds, 1982). Relative to local-club players, grand-
masters tended to search at similar depth or width, but
generated moves faster, reached a decision faster, and the
best next-move was always generated in the very beginning
of their search (Connors et al., 2011; De Groot, 1946; Gobet and
Charness, 2006; Lassiter, 2000). Several brain imaging techni-
ques have been employed to study chess skills. In general,
these studies indicated that frontal and posterior parietal
areas, which are known to be involved in top-down orienting
of attention, perception and working memory, are engaged in
chess playing (Amidzic et al., 2001; Atherton et al., 2003;
Bilalic et al., 2010; Campitelli et al., 2005; Gobet and Charness,
2006; Nichelli et al., 1994; Onofrj et al., 1995). There is also
some evidence demonstrating different brain activation pat-
terns between experts and amateurs (or novices) while
performing tasks related to chess. For instance, Amidzic
et al. (2001) found that, compared to amateur players, highly
skilled chess grandmasters had more bursts of gamma band
activity in the brain regions associated with expert memory
retrieval during matches. In more recent research, Wan et al.
(2011) studied the neural basis of intuitive best next-move
generation in Japanese chess experts, and indicated that the
superior capability of board game experts largely depends on
quick automatic processing skills which are mediated by the
caudate nucleus. In our previous studies we studied the
morphological differences of the caudate nucleus between
chess experts and novices due to the important role of this
region in chess skills. We found that the caudate nuclei of
chess experts were significantly smaller relative to those of
novice controls but exhibit increased connections with
widely distributed brain regions in spontaneous oscillatory
activity (Duan et al., 2012a, 2012b). These findings suggest
that chess grandmasters may differ from novices in brain
functional organization of both local connections and global
topologies. However, almost nothing is currently known
about the influence of high-level cognitive expertise on
large-scale intrinsic functional connectivity, not to mention
the global topological properties of the brain networks. In the
current study, we hypothesize that superior chess experts
might differ with novices on: (1) the functional connectivity of
intrinsic brain networks, especially connections associated
with learning and memory systems such as basal ganglia
and medial temporal lobe, due to the important roles of these
 brain research 1558 (2014) 33–43 35

regions in chess expertise; (2) the global topological properties
of the whole-brain functional networks, according to prior
evidence that learning and practice can enhance the func-
tional organization on the level of large-scale brain networks.
To test this hypothesis, we used resting-state functional
magnetic resonance imaging (rs-fMRI) to construct brain
functional networks of a group of grandmaster and master
level Chinese-chess players (GM/M) and a group of novice
players. The whole brain was divided into 90 cortical and
subcortical regions, and functional connectivity was estimated
between the mean time series of each pair of brain regions
according to temporal correlation. The differences in whole-
brain functional connectivity between GM/Ms and novices
were assessed by network-based statistic (NBS) approaches.
Furthermore, the whole-brain interregional correlation
matrices were thresholded to generate a set of undirected
weighted graphs to construct brain functional networks.
Finally, the topological properties of the networks were char-
acterized by graph theoretical approaches, and the differences
between these two groups were further statistically evaluated.
2. Results
2.1. Increased functional connectivity in GM/Ms
We firstly employed one sample t test to identify functional
connections significantly existed between pairs of nodes in
GM/Ms and novices. For a Bonferroni correction of po0.001,
1350 connections survived in novices, while 2184 connections
survived in GM/Ms.
To further localize specific pairs of brain regions in which
the functional connectivity was altered in GM/Ms, we used a
network based statistic (NBS) approach proposed by Zalesky
et al. (2010). The NBS identified a significantly enhanced sub-
network of connections in GM/Ms comparing with novices,
primarily comprising the basal ganglia, thalamus, medial
temporal lobe, and several temporal and parietal areas
(p¼ 0.0259, permutation testing; Fig. 1, Table 1). No signifi-
cantly decreased functional connectivity was found in GM/Ms
compared to novices. Results were visualized with the Brain-
Net Viewer (http://www.nitrc.org/projects/bnv/).
2.2. Enhanced small-world organization in GM/Ms
The functional connectivity networks corresponding to both
groups represented a clear small-world organization for a
defined range of sparsity (S) thresholds, expressed by γ41
and λ  1. The evaluation of the integrated AUC values
revealed that GM/Ms had significantly higher values of
small-worldness index (s) and normalized weighted cluster-
ing coefficient (γ) relative to novices (permutation testing,
po0.05). Since there were no significant differences in nor-
malized weighted characteristic path length (λ), we assume
that the increased s were attributable to the increased γ.

Fig. 1 – Statistically significant increased functional connectivity strength in GM/Ms compared to novice controls. Nodes are
located based on their centroid stereotaxic coordinates and color coded according to the six anatomical subregions listed in
Table 2, and further mapped onto the cortical surfaces at five views: lateral view of left hemisphere (upper left), lateral view of
right hemisphere (upper right), medial view of left hemisphere (lower left), medial view of right hemisphere (lower right), and
superior view (middle). Undirected edges have different thickness according to significnace of functional connectivity
differences.
36 brain research 1558 (2014) 33–43

Table 1 – Increased functional connectivity strength in GM/Ms compared with novices revealed by NBS.

Region 1 Region 2 t

Abbreviation Category Abbreviation Category

Increased connections in network 1, p ¼ 0.0259, corrected

PUT.L Subcortical THA.L Subcortical 3.69
PUT.R Subcortical HIP.R Medial temporal 3.32
PAL.R Subcortical HIP.R Medial temporal 3.51
HIP.L Medial temporal ROL.L Parietal-(pre)motor 3.36
HIP.L Medial temporal ROL.R Parietal-(pre)motor 3.53
HIP.L Medial temporal MTG.R Temporal 3.39
HIP.R Medial temporal ROL.R Parietal-(pre)motor 3.38
HIP.R Medial temporal PHIP.R Medial temporal 3.34
HIP.R Medial temporal FG.L Occipital 3.42
HIP.R Medial temporal SMG.R Parietal-(pre)motor 3.35
THA.L Subcortical ROL.L Parietal-(pre)motor 4.13
THA.L Subcortical ROL.R Parietal-(pre)motor 3.57
THA.L Subcortical INS.L Temporal 3.41
THA.L Subcortical FG.L Occipital 3.53
THA.L Subcortical SMG.L Parietal-(pre)motor 3.68

Besides λ, there were no significant differences in the AUC
values of Sw , Eglobal and Elocal between the two groups (Fig. 2).
3. Discussion
This is the first study, to our knowledge, to investigate the
effect of high-level cognitive expertise in whole brain func-
tional networks and their topological characteristics. We
found that functional connectivity was increased in GM/Ms
between basal ganglia, thalamus, medial temporal regions
and several parietal and temporal areas, relative to novices.
We further found that whole brain functional networks
exhibited economical small-world topology in both groups,
but GM/Ms exhibited significantly increased values of small-
world topology which might be attributable to the increased
normalized clustering coefficient. These findings suggest that
cognitive expertise has a positive influence on the functional
sub-networks center around the brain regions associated
with the expertise as well as the global topology of the
whole-brain network, which might in turn facilitate within-
network communication for expert behavior.
3.1. Enhanced functional connectivity in GM/Ms
In the present study, comparison of the functional connec-
tivity networks between the two groups revealed that GM/Ms
produced significantly stronger connectivity than the novices
mostly between the basal ganglia, thalamus, medial temporal
regions and several parietal and temporal areas (Fig. 1,
Table 1). It has been suggested that the basal ganglia,
thalamus, medial temporal regions and their anatomically
adjacent cortical and subcortical structures constitute the
limbic system, which plays an important role in learning and
memory. Specifically, the thalamus is a critical component of
the frontal cortical-basal ganglia-thalamic circuits that med-
iate motivation, planning and cognition for the development
and expression of goal-directed behaviors (Haber and
Calzavara, 2009). Notably, the thalamus sends a massive
projection directly to the basal ganglia, which is considered
to be particularly critical for learning of new complex beha-
viors (Graybiel, 2005; Pasupathy and Miller, 2005). The basal
ganglia itself is associated with reinforcement-based trial and
error learning, as well as the formation and execution of
habit, or the so-called stimulus-response association
(Graybiel, 2005; Yin et al., 2008). Specific activation of the
basal ganglia in professional chess players was detected
during intuitive generation of the best next-move, consistent
with the important role of basal ganglia in quick automatic-
processing cognitive skills (Wan et al., 2011). In chess experts,
chunks (i.e. the units of perception in chess patterns) are
stored in long-term memory in an accessible form, which
give access to information with respect to what move to play
and what plan to follow (Chase and Simon, 1973; Ericsson and
Kintsch, 1995; Gobet and Simon, 1998). Thus perception of
chunks automatically evokes the idea of the best next-move
or best series of moves (de Groot and Gobet, 1996; Wan et al.,
2011). This idea is similar to the formation of stimulus-
response associations, which might also be related to the
strong reciprocal connections between the basal ganglia and
medial temporal lobe (Dickerson et al., 2011; Voermans et al.,
2004). Previous studies have confirmed that the basal ganglia
and medial temporal lobe form interacting memory systems,
which contribute to skill and knowledge acquisition as well
as habit formation, especially during the early phases of
learning, relying on both procedural and declarative memory
systems (Poldrack et al., 2001; Poldrack and Rodriguez, 2004).
Previous brain imaging studies have investigated the task-
evoked brain activation differences between chess experts
and novices (or amateurs), and demonstrated substantial
differences in brain activation in the striatum, medial tem-
poral lobe and other related regions in response to both
domain-specific and domain-general tasks associated with
memory, decision making, perception and problem-solving
(Bilalic et al., 2011; Bukach et al., 2006; Campitelli et al., 2005,
2007; Wan et al., 2011). Those findings are of critical impor-
tance to the neural basis of chess expertise but also raise
another question on whether those activation differences are
 brain research 1558 (2014) 33–43 37

Fig. 2 – Between-group differences in overall topological characteristics of functional connectivity networks. The barplot
indicates the statistical differences of the area under the curve (AUC) over a range of thresholds of 0.1oSo0.48 between
groups. The asterisk (*) indicates a significance level of po0.05 (permutation testing). Notes: r, small-world topology; γ,
normalized clustering coefficient; λ, normalized characteristic shortest path length; Sw, total connection strength; Elocal,
local efficiency; Eglobal, global efficiency.

limited to specific task paradigms, or do they reflect a more
fundamental differences on the functional architecture repre-
sented by spontaneous activity? In the present study, we
found that, compared with novices, GM/Ms produced signifi-
cantly stronger functional connectivity between the basal
ganglia, thalamus, medial temporal regions and several
parietal and temporal areas, reflecting that long-term and
intensive practice of chess expertise modulates spontaneous
neural activity in circuitries associated with learning and
memory.
Accumulating evidence suggests that spontaneous activity
patterns recorded at rest reflects the fundamental functional-
anatomic organization of the brain, which might be asso-
ciated with individual differences in cognitive performance
and prior experience (Fox et al., 2007; Greicius et al., 2003;
Lewis et al., 2009; Mennes et al., 2010). Recently, functional
connectivity methods based on spontaneous activity have
emerged as powerful tools to investigate the level of integra-
tion of brain systems at a resting state when no task was
performed (Greicius et al., 2003). Task-free spontaneous
neural activity has been proposed to play an important part
in maintaining the ongoing representations of conscious
activity in the resting brain, and it demonstrates temporal
coherence between brain regions that are anatomically con-
nected or functionally related through co-activation in
response to task performance (Biswal et al., 1995; Raichle,
2010; Zhang and Raichle, 2010). Previous evidence from
resting-state studies has consistently demonstrated that
prior experience (i.e. the history of network activation)
changes resting functional connectivity in a behaviorally
specific manner (Hampson et al., 2006a, 2006b; Lewis et al.,
2009). For instance, Hampson et al. (2006b) demonstrated that
functional connectivity of the reading circuit co-varied with
individual differences in reading abilities. In another study,
they investigated the functional connectivity between key
nodes of the default mode network both during a working
memory task and at rest, and found that performance on the
working memory task was positively correlated with the
strength of these functional connections not only during
the working memory task, but also at rest (Hampson et al.,
2006a). Therefore, increased intrinsic connectivity in the
functional circuits related to the basal ganglia, thalamus,
and medial temporal regions might reflect the long-term and
frequent engagement of these circuits in chess practice and
skill learning, and the enhanced connection in turn facilitates
the communication within the network.
Although chess playing involves many aspects of high
level cognition including attention, execution, visuo-spatial
perception and working memory (Amidzic et al., 2001; Onofrj
et al., 1995; van der Maas and Wagenmakers, 2005), we
did not see much between-group differences of functional
connectivity in brain regions involved in those cognitive
38 brain research 1558 (2014) 33–43
processes, such as the prefrontal–parietal system. One pos-
sible explanation is that, as early psychological studies
suggested, high-level chess skill did not reside in differences
in short-term memory capacity, but in the number of chunks
held in long-term memory (Chase and Simon, 1973; Gobet
and Charness, 2006). Therefore, we assume that long-term
procedural and declarative memory systems which consist of
basal ganglia and medial temporal lobe rather than working-
memory systems exhibited significant difference between
GM/Ms and novices are of a certain amount of plausibility.
3.2. Enhanced small-world organization in GM/Ms
Recent resting-state fMRI studies suggest that functional
connectivity networks exhibit a highly efficient small-world
topology, characterized by a high level of neighborhood
clustering and a short average distance of nodes within the
overall network (Achard et al., 2006; Achard and Bullmore,
2007; Bassett and Bullmore, 2006; van den Heuvel et al., 2008).
In agreement with previous findings, we also observed the
features of small-world architecture in the functional brain
networks in both groups of GM/Ms and novices, supporting
the standpoint that brain networks might have been evolved
to maximize cost efficiency of parallel information proces-
sing, i.e., high efficiency of parallel information transfer at
low cost (Achard and Bullmore, 2007; Sporns et al., 2004).
Although both GM/M and novice groups had economical
small-world properties as elucidated earlier, the topological
properties of small-world topology and normalized clustering
coefficient were significantly increased in GM/Ms.
It has been suggested that the small-world structure
reflects an optimal network organization, which is associated
with individual differences in cognitive performance. For
instance, people with short normalized characteristic path
length of the resting-state brain network tend to have higher
intelligence quotient scores, suggesting a positive association
between the global efficiency of functional brain networks
and intellectual performance (van den Heuvel et al., 2009).
Similar results have been reported for brain anatomical net-
works constructed from diffusion tensor imaging (Li et al.,
2009). It has also been suggested that learning and training
can enhance topological organization of brain networks. For
instance, Voss et al. (2010) found that aerobic training
improved the aging brain's resting functional connectivity
as well as network efficiency in higher-level cognitive net-
works. In the present study, the normalized clustering coeffi-
cient (γ) showed significantly higher values in GM/Ms,
implying relatively intense local connectedness of the brain
functional networks in GM/Ms. As revealed by functional
connectivity analysis in the first section, GM/Ms produced
significantly stronger connectivity mainly in the long-term
procedural and declarative memory systems which consist of
basal ganglia and medial temporal lobe, demonstrating the
long-term and intensive involvement of those circuits in
chess practice and high-level cognitive skill learning. Since
the clustering coefficient quantifies the extent of local inter-
connectivity or cliquishness in network (Onnela et al., 2005;
Watts and Strogatz, 1998), enhanced functional connectivity
in the related systems might thus result in an increase of
normalized clustering coefficient. Furthermore, compared
with novices, the small-world index s also showed signifi-
cantly larger values in GM/Ms, which might be caused by the
increased value of normalized clustering coefficient, but it
also reflects the influences of high-level cognitive expertise in
global topologic characteristics.
4. Conclusions
We investigated whole brain functional connectivity net-
works and their topological properties in two groups of GM/
Ms and novices. Our results demonstrate an increased func-
tional connectivity between the basal ganglia, thalamus,
medial temporal regions and several parietal and temporal
areas in GM/Ms compared to novices, which suggests an
effect of cognitive expertise on learning and memory systems
in GM/Ms. Furthermore, both groups showed a clear small-
world property on the whole-brain functional connectivity
networks, but GM/Ms exhibited significantly increased values
of small-world topology which might be attributable to the
increased normalized clustering coefficient. Our findings
highlight the influence of high-level cognitive expertise on
topological organization of large-scale functional networks by
improving the brain’s resting functional connectivity as well
as global network characteristics, which might in turn be
beneficial for specific expert behavior.
5. Experimental procedures
5.1. Participants
Two groups of subjects were recruited and studied. The first
group consisted of twenty grandmaster and master level
Chinese-chess players (GM/M) (seven female, aged 25.4576.13
years) who had a mean period of 11.877.7 years of tournament
and training practice and scored between 2200 and 2600 on
Elo's chess-skill rating scale (Elo, 1978). All of them were
recruited from the First National Intelligence Games held in
Chengdu, China. The second group consisted of twenty well-
matched novice players (seven female, aged 27.2077.84 years)
who knew the rules and simple strategies of playing Chinese
chess. All subjects were right-handed and had no history of
psychiatric or neurological disorders. Both groups were tested
by Raven's Standard Progressive Matrices, and the two groups
did not differ on observation skills and clear-thinking ability
according to the test (p¼ 0.63, t¼  0.44). The present study was
approved by the local Institutional Review Board of the West
China Hospital of Sichuan University, and informed written
consent was obtained from all subjects.
5.2. Data acquisition and preprocessing
Scanning was performed on a 3T Siemens Trio system (Erlan-
gen, German) at the MR Research Center of West China
Hospital of Sichuan University, Chengdu, China. Functional
images covering the whole brain were acquired axially using a
T2n-weighted gradient-echo echo-planar pulse sequence (TR,
2000 ms; TE, 30 ms; flip angle¼901; voxel size¼ 3.75  3.75  5
mm3; 5 mm thickness without gap, 30 axial slices), during
 brain research 1558 (2014) 33–43
which subjects were instructed to relax with their eyes open
and focus on a cross-hair centered in the screen. For each
subject, the resting-state fMRI scanning lasted 410 seconds,
with 205 volumes recorded in total.
The first 5 volumes were discarded for magnetization
stabilization, and the remaining 200 consecutive volumes
were used for data analysis. Image preprocessing was per-
formed using SPM8 software package (http://www.fil.ion.ucl.
ac.uk/spm). After slice timing adjustment and realignment
for head motion correction, any data affected by head motion
of over 1 mm or rotation of more than 11 was excluded (no
subject was excluded in the present study). We also evaluated
group differences in translation and rotation of head motion
according to the following formula (Liao et al., 2011b; Liu
et al., 2008):
Head motion rotation
1 L qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
¼ ¼ ∑ jxi xi  1 j2 þ jyi yi  1 j2 þ jzi  zi  1 j2
L 1 i¼2
where L is the length of the time series (L ¼ 200 in this study),
xi , yi , and zi are translations/rotations at the ith time point in
the x, y, and z directions, respectively. The results showed
that there were no significant group differences between
GM/Ms and novices in head motion (two sample two-tailed
t-test, t¼ 0.642, p¼ 0.525) and rotation (two sample two-tailed
t-test, t¼ 0.657, p¼0.515). The realigned images were spatially
normalized into a standard stereotaxic space at 333 mm3,
using the Montreal Neurological Institute (MNI) echo-planar
imaging (EPI) template. In order to avoid introducing artificial
local spatial correlation, no spatial smoothing was applied, as
previously suggested (Achard et al., 2006; Achard and Bullmore,
2007; Salvador et al., 2005; Wang et al., 2009a).
5.3. Functional connectivity network construction
Nodes and edges between nodes are two fundamental ele-
ments in a network. To determine the nodes of brain func-
tional connectivity networks, we used the automated
anatomical labeling (AAL) algorithm (Tzourio-Mazoyer et al.,
2002) to parcellate the whole brain into 90 non-cerebellar
anatomical regions of interest (45 regions of interest for each
hemisphere), with each representing a node in the network.
Anatomic labels of nodes are presented in Table 2.
To determine the edges between pairs of nodes, we
conducted the following procedures. For each subject, the
representative time series in each region of interest was
obtained by averaging fMRI time series across all voxels in
the region of interest. Several sources of spurious variance,
along with their temporal derivatives, were removed from the
data through linear regression: six parameters obtained by
rigid body correction of head motion, averaged signals from
CSF, and averaged signals from white matter. To reduce the
effect of low-frequency drift and high-frequency noise, tem-
poral band-pass filtering (0.01–0.08 Hz) was then performed.
Finally, a square N  N (where N ¼90 is the number of regions
of interest) correlation matrix (i.e. functional connectivity
matrix) was obtained for each subject by computing Pearson
correlation coefficients between the preprocessed time series
of every pair of regions of interest. Of note, both positive and
negative correlation coefficients were entered into the
39
correlation matrices. A Fisher's r-to-z transformation was
applied to the correlation matrices to improve the normality
of the correlation coefficients (Liao et al., 2010; Liu et al., 2008).
5.4. Network-based statistic
In this study, network-based statistic (NBS) was used to
evaluate connected sub-networks consisting of enhanced
functional connections in GM/Ms. Before the NBS, one sample
t test was employed to test the hypothesis that functional
connectivity strength between specific pairs of nodes were
significantly larger than zero in both groups of GM/Ms and
novices (Bai et al., 2012). Here, we used a rigorous threshold to
control false positive connections by Bonferroni correction
with po0.001. The resulting functional connections in GM/Ms
and novices were then combined to build a connection mask,
which was used for the following NBS analysis.
The NBS procedure was implemented as follows: a pri-
mary threshold (here, t¼3.3) was used for each connection
within the connection mask to define a set of suprathreshold
functional connections evident in GM/Ms. The connected
components within the set of suprathreshold connections
and the component size (numbers of connections) were
determined. To evaluate the significance of each connected
components, we performed nonparametric permutation test
(5000 permutations) to generate a null distribution of the
component size. Specifically, for each permutation, we ran-
domly assigned participants to one of the two groups with
the same size as the origin groups of GM/Ms and novices. The
same threshold (t¼3.3) was then applied to connections in
the connection mask to determine the set of significantly
increased connections in GM/Ms, and the maximum compo-
nent size was computed. We then assigned a p value to each
connected component by computing the proportion of null
distribution values exceeding the original component size.
The connected components with the p value lower than 0.05
were considered as significant. A detailed description of the
NBS methodology is given by Zalesky et al. (2010).
5.5. Graph–theory analysis
5.5.1. Threshold selection
To investigate the topological properties of brain functional
networks, each correlation matrix was thresholded into a set
of weighted graphs (i.e. networks), by selecting the strongest
connections until the desired sparsity was reached. In those
graphs nodes represented brain regions and edges repre-
sented undirected connections. In this study, connection
sparsity S was adopted as a threshold measurement. S was
defined as the ratio of the existing edges to the maximum
possible number of edges in a network. The sparsity thresh-
old ensured that all resultant networks had the same number
of nodes and edges, and enabled us to compare the between-
group differences in relative network organization (Achard
and Bullmore, 2007). Instead of selecting a single threshold,
we applied a threshold range of 0.1oSo0.48 with an interval
of 0.01 to each weighted matrix. The minimum threshold
(S¼ 0.1) was computed according to the criterion that the
average degree over all nodes of each thresholded network
was larger than 2 log(N), where N denotes the number of
40 brain research 1558 (2014) 33–43

Table 2 – Anatomical subregions and corresponding abbreviated regional labels.

Region name Abbreviation

LH RH

Medial temporal
Amygdala AMYG.L AMYG.R
Hippocampus HIP.L HIP.R
Parahippocampalgyrus PHIP.L PHIP.R
Middle temporal gyrus: temporal pole MTGp.L MPGp.R
Superior temporal gyrus: temporal pole STGp.L STGp.R

Frontal
Anterior cingulate gyrus ACC.L ACC.R
Gyrus rectus REG.L REG.R
Inferior frontal gyrus, opercular part IFGoper.L IFGoper.R
Inferior frontal gyrus, orbital IFGorb.L IFGorb.R
Inferior frontal gyrus, triangular IFGtri.L IFGtri.R
Middle frontal gyrus MFG.L MFG.R
Middle frontal gyrus, orbital MFGorb.L MFGorb.R
Superior frontal gyrus SFG.L SFG.R
Superior frontal gyrus, medial SFGmed.L SFGmed.R
Superior frontal gyrus, medial orbital SFGmorb.L SFGmorb.R
Superior frontal gyrus, orbital SFGorb.L SFGorb.R

Occipital
Calcarine fissure CAL.L CAL.R
Cuneus CUN.L CUN.R
Fusiform gyrus FG.L FG.R
Inferior occipital gyrus IOG.L IOG.R
Lingual gyrus LING.L LING.R
Middle occipital gyrus MOG.L MOG.R
Superior occipital gyrus SOG.L SOG.R

Parietal-(pre)motor
Angular gyrus ANG.L ANG.R
Inferior parietal gyrus IPG.L IPG.R
Superior parietal gyrus SPG.L SPG.R
Median cingulate gyri MCC.L MCC.R
Posterior cingulate gyrus PCC.L PCC.R
Paracentral lobule PCL.L PCL.R
Postcentralgyrus PoCG.L PoCG.R
Precentralgyrus PreCG.L PreCG.R
Precuneus PCUN.L PCUN.R
Supplementary motor area SMA.L SMA.R
Supramarginalgyrus SMG.L SMG.R
Rolandic operculum ROL.L ROL.R

Subcortical
Caudate nucleus CAU.L CAU.R
Olfactory cortex OLF.L OLF.R
Pallidum PAL.L PAL.R
Putamen PUT.L PUT.R
Thalamus THA.L THA.R

Temporal
Heschlgyrus HES.L HES.R
Inferior temporal gyrus ITG.L ITG.R
Insula INS.L INS.R
Middle temporal gyrus MTG.L MTG.R
Superior temporal gyrus STG.L STG.R

nodes. The maximum threshold (S ¼0.48) was adopted based of 0.1oSo0.48 guaranteed that the thresholded network had
on the criterion that the average small-worldness scalar estimable small-worldness and control of spurious edges
(s, see below for definition) of thresholded network across possibly. The following network analysis was repeatedly
subjects was larger than 1.1. The generated threshold range performed on this defined threshold range.
 brain research 1558 (2014) 33–43
5.5.2. Network characteristics
For brain networks at each sparsity threshold S, we computed
global network characteristics including (1) small-world para-
meters involving weighted clustering coefficient Cw , weighted
characteristic path length Lw , normalized weighted clustering
coefficient γ, normalized weighted characteristic path length
λ, and small-worldness s; (2) network efficiency involving
local efficiency Elocal and global efficiency Eglobal ; and (3) total
connection strength Sw .
Small-world properties were originally proposed by Watts
and Strogatz (1998). The Cw of a network was expressed as the
average of clustering coefficients across all nodes in the
network: Cw ¼ 1=N∑i A N Cwi , where N denotes the numbers of
nodes, and Cw i denotes the clustering coefficient of a node i,
which was defined as the likelihood that the neighborhoods
of node i were connected to each other or not:
1
Cw
i ¼ ∑ ðw w w Þ1=3
ki ðki 1Þ j;h A N ij ih jh
where ki is the number of edges connecting to node i, and wij
is the correlation weight between node i and node j. The Cw
quantifies the extent of local interconnectivity or cliquish-
ness in network (Onnela et al., 2005; Watts and Strogatz,
1998).
The path length between node i and node j was defined as
the sum of edge length along this path. For weighted func-
tional connectivity networks in this study, we computed the
reciprocal of edge weight, 1=wij as the length of each
weighted edge. The path length Lij was defined as the length
of path for node i and node j with the shortest length:
Lw
ij ¼ ∑auv A gi-j 1=wuv , where gi-j is the shortest weighted path
w
w
between i and j. The weighted characteristic path length Lw of
a network, which was measured by a ‘harmonic mean’ length
between pairs to overcome the problem of possibly discon-
nected network components (Newman, 2003; Rubinov and
Sporns, 2010; Stam et al., 2009):
1 In the present study, S1 ¼ 0:1, Sn ¼ 0:48, and ΔS ¼ 0:01. The
Lw ¼
1=ðNðN 1ÞÞ∑N ∑N 1=Lw
i ¼ 1 jai ij
A real world would be considered small world if it has
similar path length but higher clustering coefficient than
random network, which is γ ¼ Cw =Cw random 41, λ ¼ Lw =
w w
Lrandom  1 (Watts and Strogatz, 1998), where Crandom and
Lw
random are the mean weighted clustering coefficient and
weighted characteristic path length of 100 matched random
networks that preserve the same number of nodes, edges,
and degree distribution as the real network. These two
measures are summarized into a scalar metric, small-world-
ness, s ¼ γ=λ, which is typically larger than 1 in the case of
small-world organization (Achard et al., 2006; Humphries
et al., 2006).
The global efficiency of a network, Eglobal , was defined by
the inverse of the harmonic mean of the path length between
each pair of nodes, which is expressed as follows:
1 1
Eglobal ¼ ∑ Natural Science Foundation of China (81301279, 61035006,
NðN 1Þ i a j A N Lij
where N is the number of nodes in a network. The global
efficiency is a measure of parallel information transformation
(Achard and Bullmore, 2007).
41
The local efficiency of a network, Elocal , is defined as the
average of local efficiency of each node, that is
1
Elocal ¼ ∑E ðG Þ;
N i A G global i
where Eglobal ðGi Þ is the global efficiency of the neighborhood
subgraph Gi of the node i. The local efficiency can be under-
stood as a measure of fault tolerance of the network,
indicating how well each subgraph exchanges information
when the index node is eliminated (Achard and Bullmore,
2007).
The total connection strength (Sw ) of a network was
computed as the average of nodal connection strength (Sw i )
for all nodes in the network:
1
Sw ¼ ∑ Sw
N iAN i
where N is the number of nodes in network, and Sw i was
defined as the sum of the weights of all connections of node i,
which is Sw
i ¼ ∑j A N wij .
5.5.3. Statistical analysis
To evaluate the between-group differences in overall topolo-
gical characteristics, we calculated the area under the curve
(AUC) over the whole range of thresholds of 0.1oSo0.48. The
AUC provides a summarized scalar for topological character-
ization of brain networks independent of single threshold
selection (Achard and Bullmore, 2007; He et al., 2009). The
integrated AUC of network metric Y, which was computed
over the threshold range of S1 to Sn with interval of ΔS, was
expressed as follows:
n1  
Y AUC ¼ ∑ YðSk Þ þ YðSkþ1 Þ ΔS=2
k¼1
AUC metric has been used in previous studies and considered
to be able to sensitively detect the topological differences
between groups (Zhang et al., 2011).
Subsequently, nonparametric permutation testing was
applied to test between-group differences of the integrated
AUC metrics using the above permutation framework. The
differences of each graph characteristics with the p value
lower than 0.05 were considered as significant.
Acknowledgments
We thank Heather Shapiro of University of California at Davis
for help with English editing. We are also grateful for the
interest and participation of all the Chinese-chess grand-
masters and masters, as well as the control volunteers. This
work was supported by 973 Project (2012CB517901), the
61125304, 81030027, and 81227002), the Specialized Research
Fund for the Doctoral Program of Higher Education of China
(20120185110028), and the Postdoctoral Science Foundation of
China (2012M511824).
42 brain research 1558 (2014) 33–43
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