Variability in functional brain networks predicts expertise during action observation

Abstract Observing an action performed by another individual activates, in the observer, similar circuits as those involved in the actual execution of that action. This activation is modulated by prior experience; indeed, sustained training in a particular motor domain leads to structural and functional changes in critical brain areas. Here, we capitalized on a novel graph‐theory approach to electroencephalographic data (Fraiman et al., 2016) to test whether variability in functional brain networks implicated in Tango observation can discriminate between groups differing in their level of expertise. We found that experts and beginners significantly differed in the functional organization of task‐relevant networks. Specifically, networks in expert Tango dancers exhibited less variability and a more robust functional architecture. Notably, these expertise‐dependent effects were captured within networks derived from electrophysiological brain activity recorded in a very short time window (2 s). In brief, variability in the organization of task‐related networks seems to be a highly sensitive indicator of long‐lasting training effects. This finding opens new methodological and theoretical windows to explore the impact of domain‐specific expertise on brain plasticity, while highlighting variability as a fruitful measure in neuroimaging research. HighlightsWe analyzed functional brain networks implicated in motor expertise.Networks showed less variability in highly skilled individuals.Network variability serves as a classifier to identify the level of motor expertise.Network variability is a fruitful measure in neuroimaging research.

[1]  Claudio Galletti,et al.  Functional imaging of the parietal cortex during action execution and observation. , 2009, Cerebral cortex.

[2]  Emmanuele Tidoni,et al.  Action Simulation Plays a Critical Role in Deceptive Action Recognition , 2013, The Journal of Neuroscience.

[3]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[4]  G. Rizzolatti,et al.  Neural Circuits Involved in the Recognition of Actions Performed by Nonconspecifics: An fMRI Study , 2004, Journal of Cognitive Neuroscience.

[5]  Steven L. Miller,et al.  Language Comprehension in Language-Learning Impaired Children Improved with Acoustically Modified Speech , 1996, Science.

[6]  Peter Fransson,et al.  Connecting to Create: Expertise in Musical Improvisation Is Associated with Increased Functional Connectivity between Premotor and Prefrontal Areas , 2014, The Journal of Neuroscience.

[7]  Frank E. Pollick,et al.  Motor Simulation without Motor Expertise: Enhanced Corticospinal Excitability in Visually Experienced Dance Spectators , 2012, PloS one.

[8]  Ellen Poliakoff,et al.  The effect of viewing graspable objects and actions in Parkinson's disease , 2007, Neuroreport.

[9]  Ralf Engbert,et al.  Microsaccades are triggered by low retinal image slip. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Emily S. Cross,et al.  Sensitivity of the action observation network to physical and observational learning. , 2008, Cerebral cortex.

[11]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[12]  M Lotze,et al.  The musician's brain: functional imaging of amateurs and professionals during performance and imagery , 2003, NeuroImage.

[13]  Á. Pascual-Leone,et al.  Impaired motor facilitation during action observation in individuals with autism spectrum disorder , 2005, Current Biology.

[14]  Agustín Ibáñez,et al.  Time to Tango: Expertise and contextual anticipation during action observation , 2014, NeuroImage.

[15]  S. MacDonald,et al.  Neuroscience and Biobehavioral Reviews Review Moment-to-moment Brain Signal Variability: a next Frontier in Human Brain Mapping? , 2022 .

[16]  Steven L. Miller,et al.  Temporal Processing Deficits of Language-Learning Impaired Children Ameliorated by Training , 1996, Science.

[17]  Wichian Sittiprapa,et al.  The Musician's Brain , 2012 .

[18]  胡德文 Large-Scale Functional Brain Network Changes in Taxi Drivers: Evidence From Resting-State fMRI , 2015 .

[19]  C. Gilbert,et al.  The Neural Basis of Perceptual Learning , 2001, Neuron.

[20]  Jonas Richiardi,et al.  Graph analysis of functional brain networks: practical issues in translational neuroscience , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  Emily S. Cross,et al.  Building a motor simulation de novo: Observation of dance by dancers , 2006, NeuroImage.

[22]  Helen E. Savaki,et al.  Observation of action: grasping with the mind's hand , 2004, NeuroImage.

[23]  Nancy Gwinn Time to Tango! , 2004 .

[24]  C. Keysers,et al.  The Observation and Execution of Actions Share Motor and Somatosensory Voxels in all Tested Subjects: Single-Subject Analyses of Unsmoothed fMRI Data , 2008, Cerebral cortex.

[25]  John S. Johnson,et al.  Audience preferences are predicted by temporal reliability of neural processing , 2014, Nature Communications.

[26]  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.

[27]  C. Gilbert,et al.  Top-Down Reorganization of Activity in the Visual Pathway after Learning a Shape Identification Task , 2005, Neuron.

[28]  Yumie Ono,et al.  Frontotemporal oxyhemoglobin dynamics predict performance accuracy of dance simulation gameplay: Temporal characteristics of top-down and bottom-up cortical activities , 2014, NeuroImage.

[29]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[30]  Dennis C. Tkach,et al.  Congruent Activity during Action and Action Observation in Motor Cortex , 2007, The Journal of Neuroscience.

[31]  C. Gilbert,et al.  Brain States: Top-Down Influences in Sensory Processing , 2007, Neuron.

[32]  S. Swinnen,et al.  Functional Organization of the Action Observation Network in Autism: A Graph Theory Approach , 2015, PloS one.

[33]  R. Passingham,et al.  Seeing or Doing? Influence of Visual and Motor Familiarity in Action Observation , 2006, Current Biology.

[34]  Jonathan D. Nelson,et al.  Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery , 2007, NeuroImage.

[35]  R. Passingham,et al.  Action observation and acquired motor skills: an FMRI study with expert dancers. , 2005, Cerebral cortex.

[36]  E. Altenmüller,et al.  The musician's brain as a model of neuroplasticity , 2002, Nature Reviews Neuroscience.

[37]  M. Iacoboni,et al.  Getting a grip on other minds: Mirror neurons, intention understanding, and cognitive empathy , 2006, Social Neuroscience.

[38]  J. Hirsch,et al.  Motor learning and modulation of prefrontal cortex: an fNIRS assessment , 2015, Journal of neural engineering.

[39]  H. Théoret,et al.  Early non‐specific modulation of corticospinal excitability during action observation , 2010, The European journal of neuroscience.

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

[41]  Xin Jin,et al.  Corticostriatal dynamics encode the refinement of specific behavioral variability during skill learning , 2015, eLife.

[42]  Lyle Borg-Graham,et al.  Facilitating the science in computational neuroscience , 2000, Nature Neuroscience.

[43]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

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

[45]  John G Milton,et al.  On the Road to Automatic: Dynamic Aspects in the Development of Expertise , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[46]  G A Cecchi,et al.  Noise in neurons is message dependent. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[47]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[48]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[49]  R. Kliegl,et al.  Human Microsaccade-Related Visual Brain Responses , 2009, The Journal of Neuroscience.

[50]  G. Rizzolatti,et al.  Impairment of actions chains in autism and its possible role in intention understanding , 2007, Proceedings of the National Academy of Sciences.

[51]  C. Urgesi,et al.  Action anticipation and motor resonance in elite basketball players , 2008, Nature Neuroscience.

[52]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Stephan P. Swinnen,et al.  Motor facilitation during action observation: The role of M1 and PMv in grasp predictions , 2016, Cortex.

[54]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[55]  Panagiotis D Bamidis,et al.  Musical expertise is related to altered functional connectivity during audiovisual integration , 2015, Proceedings of the National Academy of Sciences.

[56]  Lubin Wang,et al.  Changes in functional connectivity dynamics associated with vigilance network in taxi drivers , 2016, NeuroImage.