Functional organization of intrinsic connectivity networks in Chinese-chess experts

The functional architecture of the human brain has been extensively described in terms of functional connectivity networks, detected from the low-frequency coherent neuronal fluctuations during a resting state condition. Accumulating evidence suggests that the overall organization of functional connectivity networks is associated with individual differences in cognitive performance and prior experience. Such an association raises the question of how cognitive expertise exerts an influence on the topological properties of large-scale functional networks. To address this question, we examined the overall organization of brain functional networks in 20 grandmaster and master level Chinese-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.

[1]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[2]  Thomas Elbert,et al.  Pattern of focal γ-bursts in chess players , 2001, Nature.

[3]  M. Raichle,et al.  Disease and the brain's dark energy , 2010, Nature Reviews Neurology.

[4]  G. Sandini,et al.  Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. , 2009, Brain : a journal of neurology.

[5]  M. Raichle The brain's dark energy. , 2010 .

[6]  S. Rombouts,et al.  Loss of ‘Small-World’ Networks in Alzheimer's Disease: Graph Analysis of fMRI Resting-State Functional Connectivity , 2010, PloS one.

[7]  Yong He,et al.  Topologically Convergent and Divergent Structural Connectivity Patterns between Patients with Remitted Geriatric Depression and Amnestic Mild Cognitive Impairment , 2012, The Journal of Neuroscience.

[8]  A. Graybiel The basal ganglia: learning new tricks and loving it , 2005, Current Opinion in Neurobiology.

[9]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[10]  Qiang Xu,et al.  Small-world directed networks in the human brain: Multivariate Granger causality analysis of resting-state fMRI , 2011, NeuroImage.

[11]  Wei Liao,et al.  Large-Scale Brain Networks in Board Game Experts: Insights from a Domain-Related Task and Task-Free Resting State , 2012, PloS one.

[12]  Keiji Tanaka,et al.  The Neural Basis of Intuitive Best Next-Move Generation in Board Game Experts , 2011, Science.

[13]  Fernand Gobet,et al.  Structure and Stimulus Familiarity: A Study of Memory in Chess-Players with Functional Magnetic Resonance Imaging , 2005, The Spanish Journal of Psychology.

[14]  T. Prescott,et al.  The brainstem reticular formation is a small-world, not scale-free, network , 2006, Proceedings of the Royal Society B: Biological Sciences.

[15]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[16]  Fernand Gobet,et al.  BRAIN LOCALIZATION OF MEMORY CHUNKS IN CHESSPLAYERS , 2007, The International journal of neuroscience.

[17]  T Elbert,et al.  Pattern of focal gamma-bursts in chess players. , 2001, Nature.

[18]  M. Raichle The Brain's Dark Energy , 2006, Science.

[19]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

[20]  K. Worsley,et al.  Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. , 2009, Brain : a journal of neurology.

[21]  S. Haber,et al.  The cortico-basal ganglia integrative network: The role of the thalamus , 2009, Brain Research Bulletin.

[22]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[23]  K. Kaski,et al.  Intensity and coherence of motifs in weighted complex networks. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  Dinggang Shen,et al.  Brain anatomical networks in early human brain development , 2011, NeuroImage.

[25]  Martin Suter,et al.  Small World , 2002 .

[26]  Edwin M. Robertson,et al.  The Resting Human Brain and Motor Learning , 2009, Current Biology.

[27]  Yong He,et al.  Disrupted small-world networks in schizophrenia. , 2008, Brain : a journal of neurology.

[28]  Michelle Hampson,et al.  Connectivity–behavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability , 2006, NeuroImage.

[29]  Jun Li,et al.  Brain Anatomical Network and Intelligence , 2009, NeuroImage.

[30]  Huafu Chen,et al.  Default mode network abnormalities in mesial temporal lobe epilepsy: A study combining fMRI and DTI , 2011, Human brain mapping.

[31]  P. Thiran,et al.  Mapping Human Whole-Brain Structural Networks with Diffusion MRI , 2007, PloS one.

[32]  H. Simon,et al.  Expert chess memory: revisiting the chunking hypothesis. , 1998, Memory.

[33]  G. Lassiter,et al.  The Relative Contributions of Recognition and Search-Evaluation Processes to High-Level Chess Performance: Comment on Gobet and Simon , 2000, Psychological science.

[34]  Justin L. Vincent,et al.  Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior , 2007, Neuron.

[35]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[36]  M. Onofrj,et al.  Non-dominant dorsal-prefrontal activation during chess problem solution evidenced by single photon emission computerized tomography (SPECT) , 1995, Neuroscience Letters.

[37]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[38]  A. D. D. Groot,et al.  Perception and memory in chess: Studies in the heuristics of the prodessional eye , 1996 .

[39]  Liang Wang,et al.  Altered small‐world brain functional networks in children with attention‐deficit/hyperactivity disorder , 2009, Human brain mapping.

[40]  Sheng He,et al.  A functional MRI study of high-level cognition , 2003 .

[41]  E. McAuley,et al.  Frontiers in Aging Neuroscience Aging Neuroscience , 2022 .

[42]  Kaustubh Supekar,et al.  Development of Large-Scale Functional Brain Networks in Children , 2009, NeuroImage.

[43]  B. Balleine,et al.  Reward‐guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico‐basal ganglia networks , 2008, The European journal of neuroscience.

[44]  Vince D. Calhoun,et al.  Altered Topological Properties of Functional Network Connectivity in Schizophrenia during Resting State: A Small-World Brain Network Study , 2011, PloS one.

[45]  Yuan Zhou,et al.  Anatomical insights into disrupted small-world networks in schizophrenia , 2012, NeuroImage.

[46]  N. Charness,et al.  Aging and skilled problem solving. , 1981, Journal of experimental psychology. General.

[47]  Michael Erb,et al.  Mechanisms and neural basis of object and pattern recognition: a study with chess experts. , 2010, Journal of experimental psychology. General.

[48]  Cindy M. Bukach,et al.  Beyond faces and modularity: the power of an expertise framework , 2006, Trends in Cognitive Sciences.

[49]  C. Stam,et al.  Small-world networks and epilepsy: Graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures , 2007, Clinical Neurophysiology.

[50]  Yong He,et al.  Graph theoretical modeling of brain connectivity. , 2010, Current opinion in neurology.

[51]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[52]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[53]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[54]  P. Skudlarski,et al.  Brain Connectivity Related to Working Memory Performance , 2006, The Journal of Neuroscience.

[55]  X. Duan,et al.  Nanoscale morphology, dimensional control, and electrical properties of oligoanilines. , 2010, Journal of the American Chemical Society.

[56]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[57]  R. Poldrack,et al.  How do memory systems interact? Evidence from human classification learning , 2004, Neurobiology of Learning and Memory.

[58]  Huafu Chen,et al.  Altered Functional Connectivity and Small-World in Mesial Temporal Lobe Epilepsy , 2010, PloS one.

[59]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[60]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[61]  R. Kahn,et al.  Efficiency of Functional Brain Networks and Intellectual Performance , 2009, The Journal of Neuroscience.

[62]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[63]  E. Wagenmakers,et al.  A psychometric analysis of chess expertise. , 2005, The American journal of psychology.

[64]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[65]  C. Stam,et al.  Small-world network organization of functional connectivity of EEG slow-wave activity during sleep , 2007, Clinical Neurophysiology.

[66]  Liang Wang,et al.  Parcellation‐dependent small‐world brain functional networks: A resting‐state fMRI study , 2009, Human brain mapping.

[67]  W. Grodd,et al.  Many Faces of Expertise: Fusiform Face Area in Chess Experts and Novices , 2011, The Journal of Neuroscience.

[68]  Jian Li,et al.  Parallel contributions of distinct human memory systems during probabilistic learning , 2011, NeuroImage.

[69]  H. Simon,et al.  Perception in chess , 1973 .

[70]  Sheng He,et al.  A functional MRI study of high-level cognition. I. The game of chess. , 2003, Brain research. Cognitive brain research.

[71]  Cornelis J. Stam,et al.  Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain , 2008, NeuroImage.

[72]  R. I. Reynolds Search heuristics of chess players of different calibers. , 1982, The American journal of psychology.

[73]  K. A. Ericsson,et al.  Long-term working memory. , 1995, Psychological review.

[74]  Pietro Pietrini,et al.  Brain activity in chess playing , 1994, Nature.

[75]  Guillermo Campitelli,et al.  Expertise in Complex Decision Making: The Role of Search in Chess 70 Years After de Groot , 2011, Cogn. Sci..

[76]  C. Stam,et al.  Heritability of “small‐world” networks in the brain: A graph theoretical analysis of resting‐state EEG functional connectivity , 2008, Human brain mapping.

[77]  Yufeng Zang,et al.  Linking inter-individual differences in neural activation and behavior to intrinsic brain dynamics , 2011, NeuroImage.

[78]  Yuan Li,et al.  Reduced caudate volume and enhanced striatal-DMN integration in chess experts , 2012, NeuroImage.

[79]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[80]  Neil Charness,et al.  Expertise in chess , 2006 .

[81]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[82]  Xiaoqi Huang,et al.  Disrupted Brain Connectivity Networks in Drug-Naive, First-Episode Major Depressive Disorder , 2011, Biological Psychiatry.

[83]  C. Stam,et al.  Small-world networks and functional connectivity in Alzheimer's disease. , 2006, Cerebral cortex.

[84]  Guillén Fernández,et al.  Interaction between the Human Hippocampus and the Caudate Nucleus during Route Recognition , 2004, Neuron.

[85]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.