Dance expertise modulates visual sensitivity to complex biological movements

ABSTRACT Motor resonance processes that occur when observing an individual perform an action may be modulated by acquired visuomotor expertise. We used the event‐related potential (EEG/ERP) technique to investigate the ability to automatically recognize a subtle difference between very similar novel contemporary dance movements. Twelve professional dancers and twelve non‐dancers were shown 212 pairs of videos of complex whole‐body movements that lasted 3 s. The second of each pair was the repetition of the previous movement or a slight variation of it (deviance). The participants were engaged in a secondary attentional task. Modulation of a larger centro‐parietal N400 effect and a reduction of the Late Positivity amplitude (repetition suppression effect) were identified in response to deviant stimuli only in the dancers. Source reconstruction (swLORETA) showed activations in biological motion, body and face processing related areas, and fronto‐parietal and limbic systems. The current findings provide evidence that acquired dance expertise modifies the ability to visually code whole‐body complex movements. HIGHLIGHTSDancers and controls were shown novel dance moves during electroencephalography.A N400 and a reduction of Late Positivity to deviant stimuli were found in dancers.Source reconstruction showed activity in mirror system and superior temporal gyrus.

[1]  Daniel M. Smith.  Neurophysiology of action anticipation in athletes: A systematic review , 2016, Neuroscience & Biobehavioral Reviews.

[2]  F. Manes,et al.  N400 ERPs for actions: building meaning in context , 2013, Front. Hum. Neurosci..

[3]  T W Picton,et al.  N2 and automatic versus controlled processes. , 1986, Electroencephalography and clinical neurophysiology. Supplement.

[4]  Alison J. Wiggett,et al.  Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas. , 2007, Journal of neurophysiology.

[5]  Frank E. Pollick,et al.  Experience in judging intent to harm modulates parahippocampal activity: An fMRI study with experienced CCTV operators , 2014, Cortex.

[6]  E. Procyk,et al.  Brain activity during observation of actions. Influence of action content and subject's strategy. , 1997, Brain : a journal of neurology.

[7]  A. Proverbio,et al.  When neurons do not mirror the agent's intentions: Sex differences in neural coding of goal-directed actions , 2010, Neuropsychologia.

[8]  H. Kashima,et al.  A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion , 2006, Neuropsychologia.

[9]  Emily S. Cross,et al.  Additive Routes to Action Learning: Layering Experience Shapes Engagement of the Action Observation Network , 2015, Cerebral cortex.

[10]  Jonathan R. Folstein,et al.  Influence of cognitive control and mismatch on the N2 component of the ERP: a review. , 2007, Psychophysiology.

[11]  Salvatore Maria Aglioti,et al.  Somatotopic mapping of piano fingering errors in sensorimotor experts: TMS studies in pianists and visually trained musically naives. , 2014, Cerebral cortex.

[12]  J. DeSouza,et al.  Lateral occipitotemporal cortex (LOTC) activity is greatest while viewing dance compared to visualization and movement: learning and expertise effects , 2016, Experimental Brain Research.

[13]  Mika Koivisto,et al.  Event-related brain potential correlates of visual awareness , 2010, Neuroscience & Biobehavioral Reviews.

[14]  Phillip J. Holcomb,et al.  Two Neurocognitive Mechanisms of Semantic Integration during the Comprehension of Visual Real-world Events , 2008, Journal of Cognitive Neuroscience.

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

[16]  Paul E. Downing,et al.  Representation of Action in Occipito-temporal Cortex , 2011, Journal of Cognitive Neuroscience.

[17]  A. Schleicher,et al.  Motor cortex and hand motor skills: Structural compliance in the human brain , 1997, Human brain mapping.

[18]  Done-Sik Yoo,et al.  Neural correlates related to action observation in expert archers , 2011, Behavioural Brain Research.

[19]  Henry Railo,et al.  Tracking the processes behind conscious perception: A review of event-related potential correlates of visual consciousness , 2011, Consciousness and Cognition.

[20]  Melvyn A. Goodale,et al.  Repetition suppression in occipital–temporal visual areas is modulated by physical rather than semantic features of objects , 2008, NeuroImage.

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

[22]  M. Roth,et al.  Lateral occipitotemporal cortex and action representation , 2014, Neuropsychologia.

[23]  L. Bonini.  The Extended Mirror Neuron Network , 2017, The Neuroscientist.

[24]  M. Iacoboni,et al.  Golf putt outcomes are predicted by sensorimotor cerebral EEG rhythms , 2008, The Journal of physiology.

[25]  Alice Mado Proverbio,et al.  RP and N400 ERP components reflect semantic violations in visual processing of human actions , 2009, Neuroscience Letters.

[26]  Steven Brown,et al.  The neuroscience of dance. , 2008, Scientific American.

[27]  T W Picton,et al.  The P300 Wave of the Human Event‐Related Potential , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[29]  N. Virji-Babul,et al.  Neural correlates of action understanding in infants: influence of motor experience , 2012, Brain and behavior.

[30]  G. Rizzolatti,et al.  The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations , 2010, Nature Reviews Neuroscience.

[31]  Lutz Jäncke,et al.  Structural neuroplasticity in the sensorimotor network of professional female ballet dancers , 2009, Human brain mapping.

[32]  Hajime Asama,et al.  The body and objects represented in the ventral stream of the parieto-premotor network , 2016, Neuroscience Research.

[33]  Aina Puce,et al.  Electrophysiology and brain imaging of biological motion. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[35]  Scott T. Grafton,et al.  Body language in the brain: constructing meaning from expressive movement , 2015, Front. Hum. Neurosci..

[36]  Emily S. Cross,et al.  The Impact of Aesthetic Evaluation and Physical Ability on Dance Perception , 2011, Front. Hum. Neurosci..

[37]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[38]  M. Bradley,et al.  Affective picture processing: the late positive potential is modulated by motivational relevance. , 2000, Psychophysiology.

[39]  Yoshiro Okubo,et al.  Enhanced activation in the extrastriate body area by goal‐directed actions , 2008, Psychiatry and clinical neurosciences.

[40]  Phillip Wolff,et al.  Causal reasoning with forces , 2015, Front. Hum. Neurosci..

[41]  R. Zatorre,et al.  Early Musical Training and White-Matter Plasticity in the Corpus Callosum: Evidence for a Sensitive Period , 2013, The Journal of Neuroscience.

[42]  J. Mazziotta,et al.  Grasping the Intentions of Others with One's Own Mirror Neuron System , 2005, PLoS biology.

[43]  Donatella Spinelli,et al.  Neural correlates of fast stimulus discrimination and response selection in top-level fencers , 2006, Neuroscience Letters.

[44]  B. Bertenthal,et al.  Does Perception of Biological Motion Rely on Specific Brain Regions? , 2001, NeuroImage.

[45]  Peter A Tass,et al.  swLORETA: a novel approach to robust source localization and synchronization tomography , 2007, Physics in medicine and biology.

[46]  E. Hahn,et al.  Exploring the time course of N170 repetition suppression: a preliminary study. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[47]  G. Króliczak,et al.  Left extrastriate body area is sensitive to the meaning of symbolic gesture: evidence from fMRI repetition suppression , 2016, Scientific Reports.

[48]  Virginia B. Penhune,et al.  Dance and music training have different effects on white matter diffusivity in sensorimotor pathways , 2016, NeuroImage.

[49]  Robert Oostenveld,et al.  The five percent electrode system for high-resolution EEG and ERP measurements , 2001, Clinical Neurophysiology.

[50]  Phillip J Holcomb,et al.  Semantic integration in videos of real-world events: an electrophysiological investigation. , 2003, Psychophysiology.

[51]  B. Röder,et al.  Sensitive periods for the functional specialization of the neural system for human face processing , 2013, Proceedings of the National Academy of Sciences.

[52]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[53]  Alison J. Wiggett,et al.  Patterns of fMRI Activity Dissociate Overlapping Functional Brain Areas that Respond to Biological Motion , 2006, Neuron.

[54]  Kathryn H. Yoo,et al.  Assessing human mirror activity with EEG mu rhythm: A meta-analysis. , 2016, Psychological bulletin.

[55]  Emily S. Cross,et al.  Neurocognitive control in dance perception and performance. , 2012, Acta psychologica.

[56]  K. Laland,et al.  The evolution of dance , 2016, Current Biology.

[57]  Shingo Oda,et al.  Tapping Speed Asymmetry in Drummers for Single-Hand Tapping with a Stick , 2006, Perceptual and motor skills.

[58]  Falisha J. Karpati,et al.  Dance and music share gray matter structural correlates , 2017, Brain Research.

[59]  Kara D. Federmeier,et al.  Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). , 2011, Annual review of psychology.

[60]  Lutz Jäncke,et al.  Hand Skill Asymmetry in Professional Musicians , 1997, Brain and Cognition.

[61]  Frank Haist,et al.  Functional development of the brain's face-processing system. , 2017, Wiley interdisciplinary reviews. Cognitive science.

[62]  J. Ford,et al.  ERPs to response production and inhibition. , 1985, Electroencephalography and clinical neurophysiology.

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

[64]  P. Haggard,et al.  Experts see it all: configural effects in action observation , 2010, Psychological research.

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

[66]  M. Heil,et al.  Expertise in dance modulates alpha/beta event‐related desynchronization during action observation , 2008, The European journal of neuroscience.

[67]  S. M. Aglioti,et al.  Electrocortical signatures of detecting errors in the actions of others: An EEG study in pianists, non-pianist musicians and musically naïve people , 2016, Neuroscience.

[68]  Leslie G. Ungerleider,et al.  Temporal dynamics of face repetition suppression , 2006, Brain Research Bulletin.

[69]  R. Adorni,et al.  Who needs a referee? How incorrect basketball actions are automatically detected by basketball players' brain , 2012, Scientific Reports.

[70]  Rudolf von Laban,et al.  Laban's principles of dance and movement notation , 1975 .

[71]  A. Saygin.  Superior temporal and premotor brain areas necessary for biological motion perception. , 2007, Brain : a journal of neurology.

[72]  E Macaluso,et al.  Action anticipation beyond the action observation network: a functional magnetic resonance imaging study in expert basketball players , 2012, The European journal of neuroscience.

[73]  M. Ridding,et al.  Reduced interhemispheric inhibition in musicians , 2000, Experimental Brain Research.

[74]  Kevin A. Pelphrey,et al.  Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception , 2004, Journal of Cognitive Neuroscience.

[75]  Karl J. Friston,et al.  Predictive coding: an account of the mirror neuron system , 2007, Cognitive Processing.

[76]  Jose L. Contreras-Vidal,et al.  Neural decoding of expressive human movement from scalp electroencephalography (EEG) , 2014, Front. Hum. Neurosci..

[77]  Joana C Carmo,et al.  Understanding and Imitating Unfamiliar Actions: Distinct Underlying Mechanisms , 2012, PloS one.

[78]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[79]  Patric Bach,et al.  Communicating hands: ERPs elicited by meaningful symbolic hand postures , 2004, Neuroscience Letters.

[80]  Paola Cesari,et al.  Fooling the kickers but not the goalkeepers: behavioral and neurophysiological correlates of fake action detection in soccer. , 2013, Cerebral cortex.

[81]  M. Kutas,et al.  Reading senseless sentences: brain potentials reflect semantic incongruity. , 1980, Science.

[82]  Martin Wiesmann,et al.  Expertise reduces neural cost but does not modulate repetition suppression , 2010, Cognitive neuroscience.

[83]  Miao‐kun Sun,et al.  Trends in cognitive sciences , 2012 .

[84]  T. Brandt,et al.  Structural and functional plasticity of the hippocampal formation in professional dancers and slackliners , 2010, Hippocampus.

[85]  R. Zatorre,et al.  Modulation of Functional Connectivity in Auditory‐Motor Networks in Musicians Compared with Nonmusicians , 2016, Cerebral cortex.

[86]  Peter E. Keller,et al.  Captured by motion: Dance, action understanding, and social cognition , 2011, Brain and Cognition.

[87]  Caroline Catmur,et al.  Understanding intentions from actions: Direct perception, inference, and the roles of mirror and mentalizing systems , 2015, Consciousness and Cognition.

[88]  E A Franz,et al.  Experience-Dependent Effects in Unimanual and Bimanual Reaction Time Tasks in Musicians , 2007, Journal of motor behavior.

[89]  Giacomo Rizzolatti,et al.  The mirror-neuron system and action recognition , 2003 .

[90]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[91]  F. Binkofski,et al.  The mirror neuron system and action recognition , 2004, Brain and Language.

[92]  M. Iacoboni,et al.  “Neural efficiency” of experts’ brain during judgment of actions: A high-resolution EEG study in elite and amateur karate athletes , 2010, Behavioural Brain Research.

[93]  P. Haggard,et al.  Constructing Visual Perception of Body Movement with the Motor Cortex , 2015, Cerebral cortex.

[94]  S. Cochin,et al.  Observation and execution of movement: similarities demonstrated by quantified electroencephalography , 1999, The European journal of neuroscience.

[95]  A. de Rugy,et al.  Different mechanisms contributing to savings and anterograde interference are impaired in Parkinson's disease , 2013, Front. Hum. Neurosci..

[96]  G. Rizzolatti,et al.  I Know What You Are Doing A Neurophysiological Study , 2001, Neuron.

[97]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[98]  Alice Mado Proverbio,et al.  Observation of Static Pictures of Dynamic Actions Enhances the Activity of Movement-Related Brain Areas , 2009, PloS one.

[99]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[100]  A. Mark Williams,et al.  The role of cortical sensorimotor oscillations in action anticipation , 2017, NeuroImage.

[101]  L. Minati,et al.  Throwing the banana away and keeping the peel: Neuroelectric responses to unexpected but physically feasible action endings , 2013, Brain Research.

[102]  Vincent M. Reid,et al.  N400 involvement in the processing of action sequences , 2008, Neuroscience Letters.

[103]  Paul E. Downing,et al.  An event-related potential component sensitive to images of the human body , 2006, NeuroImage.

[104]  Emilio Maggio,et al.  Observation and Execution , 2012, Advanced Bimanual Manipulation.

[105]  IT "Deficit" , 1997, Science.

[106]  P. Downing,et al.  The neural basis of visual body perception , 2007, Nature Reviews Neuroscience.

[107]  Christine E. Watson,et al.  The specificity of action knowledge in sensory and motor systems , 2014, Front. Psychol..

[108]  Masayuki Endo,et al.  Corrigendum: Efficient amplification of self-gelling polypod-like structured DNA by rolling circle amplification and enzymatic digestion , 2015, Scientific Reports.

[109]  A. Ben Hamida,et al.  Spatial Resolution Improvement of EEG Source Reconstruction Using swLORETA , 2015, IEEE Transactions on NanoBioscience.

[110]  Scott T. Grafton,et al.  Action outcomes are represented in human inferior frontoparietal cortex. , 2008, Cerebral cortex.

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

[112]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

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

[114]  Michael J. Martinez,et al.  Cerebral Cortex doi:10.1093/cercor/bhj057 Cerebral Cortex Advance Access published October 12, 2005 The Neural Basis of Human Dance , 2022 .

[115]  Hans Herzog,et al.  Activation differences in observation of hand movements for imitation or velocity judgement , 2008, Behavioural Brain Research.

[116]  Parashkev Nachev,et al.  The Neuroanatomical Correlates of Training-Related Perceptuo-Reflex Uncoupling in Dancers , 2013, Cerebral cortex.

[117]  Jiro Gyoba,et al.  Event-related potentials during the evaluation of the appropriateness of cooperative actions , 2009, Neuroscience Letters.

[118]  Wolfgang Klimesch,et al.  EEG Correlates of Action Observation in Humans , 2008, Brain Topography.

[119]  M. Treviño,et al.  Noradrenergic ‘Tone’ Determines Dichotomous Control of Cortical Spike-Timing-Dependent Plasticity , 2012, Scientific Reports.

[120]  M M Mesulam,et al.  An electrophysiological index of stimulus unfamiliarity. , 2000, Psychophysiology.

[121]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[122]  Emily S. Cross,et al.  Dynamic Modulation of the Action Observation Network by Movement Familiarity , 2015, The Journal of Neuroscience.

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

[124]  W. Prinz,et al.  N400-like negativities in action perception reflect the activation of two components of an action representation , 2009, Social neuroscience.