Communication with emblematic gestures: Shared and distinct neural correlates of expression and reception

Emblematic (or symbolic) gestures allow individuals to convey a variety of thoughts and emotions ranging from approval to hostility. The use of such gestures involves the execution of a codified motor act by the addresser and its perception and decoding by the addressee. To examine underlying common and distinct neural correlates, we used fMRI tasks in which subjects viewed video clips of emblematic one‐hand gestures. They were asked to (1) take the perspective of the addresser and imagine executing the gestures (“expression” condition), and to (2) take the perspective of the addressee and imagine being confronted with the gestures (“reception” condition). Common areas of activation were found in inferior frontal, medial frontal, and posterior temporal cortices with left‐hemispheric predominance as well as in the cerebellum. The distinction between regions specifically involved in the expression or reception condition partly resembled the dorsal and ventral stream dichotomy of visual processing with junctions in inferior frontal and medial prefrontal cortices. Imagery of gesture expression involved the dorsal visual stream as well as higher‐order motor areas. In contrast, gesture reception encompassed regions related to semantic processing, and medial prefrontal areas known to be involved in the process of understanding the intentions of others. In conclusion, our results provide evidence for a dissociation in representations of emblematic gesture processing between addresser and addressee in addition to shared components in language‐related areas. Hum Brain Mapp, 2012. © 2011 Wiley Periodicals, Inc.

[1]  R. Leiguarda,et al.  The neural substrate of gesture recognition , 2008, Neuropsychologia.

[2]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C. Keysers,et al.  Integrating simulation and theory of mind: from self to social cognition , 2007, Trends in Cognitive Sciences.

[4]  Melvyn A. Goodale,et al.  Action without perception in human vision , 2008, Cognitive neuropsychology.

[5]  Xenophon Papademetris,et al.  More accurate Talairach coordinates for neuroimaging using non-linear registration , 2008, NeuroImage.

[6]  Tao Wu,et al.  The role of the dorsal stream for gesture production , 2006, NeuroImage.

[7]  R. Seitz,et al.  Value judgments and self-control of action: The role of the medial frontal cortex , 2009, Brain Research Reviews.

[8]  Anne Lacheret,et al.  FMRI study of emotional speech comprehension. , 2006, Cerebral cortex.

[9]  M Hallett,et al.  Gesture subtype-dependent left lateralization of praxis planning: an event-related fMRI study. , 2009, Cerebral cortex.

[10]  A. Braun,et al.  Symbolic gestures and spoken language are processed by a common neural system , 2009, Proceedings of the National Academy of Sciences.

[11]  R. Rumiati,et al.  Imitation of transitive and intransitive actions in healthy individuals , 2009, Brain and Cognition.

[12]  M. Petrides Broca’s Area in the Human and the Nonhuman Primate Brain , 2006 .

[13]  R. Bagby,et al.  The twenty-item Toronto Alexithymia Scale--I. Item selection and cross-validation of the factor structure. , 1994, Journal of psychosomatic research.

[14]  Dr. Stefan Geyer The Microstructural Border Between the Motor and the Cognitive Domain in the Human Cerebral Cortex , 2004, Advances in Anatomy Embryology and Cell Biology.

[15]  Gregory Hickok,et al.  Eight Problems for the Mirror Neuron Theory of Action Understanding in Monkeys and Humans , 2009, Journal of Cognitive Neuroscience.

[16]  F. Binkofski,et al.  Motor functions of the Broca’s region , 2004, Brain and Language.

[17]  C. Frith,et al.  Dissociable neural pathways for the perception and recognition of expressive and instrumental gestures , 2004, Neuropsychologia.

[18]  J. Mazziotta,et al.  The essential role of Broca's area in imitation , 2003, The European journal of neuroscience.

[19]  R. Veit,et al.  Differential cerebral activation during observation of expressive gestures and motor acts , 2006, Neuropsychologia.

[20]  Katrin Amunts,et al.  Broca’s area: Nomenclature, anatomy, typology and asymmetry , 2009, Brain and Language.

[21]  Rupert Lanzenberger,et al.  The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling , 2008, NeuroImage.

[22]  Roel M. Willems,et al.  Complementary Systems for Understanding Action Intentions , 2008, Current Biology.

[23]  A. Braun,et al.  Activation of Broca’s area during the production of spoken and signed language: a combined cytoarchitectonic mapping and PET analysis , 2003, Neuropsychologia.

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

[25]  J. Decety,et al.  From the perception of action to the understanding of intention , 2001, Nature reviews. Neuroscience.

[26]  R. McIntosh,et al.  Two visual streams for perception and action: Current trends , 2009, Neuropsychologia.

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

[28]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[29]  Henrik Walter,et al.  Understanding Intentions in Social Interaction: The Role of the Anterior Paracingulate Cortex , 2004, Journal of Cognitive Neuroscience.

[30]  Allen R. Braun,et al.  Distinguishing the processing of gestures from signs in deaf individuals: An fMRI study , 2009, Brain Research.

[31]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[32]  C D Marsden,et al.  Limb apraxias: higher-order disorders of sensorimotor integration. , 2000, Brain : a journal of neurology.

[33]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

[34]  M. Studdert-Kennedy Hand and Mind: What Gestures Reveal About Thought. , 1994 .

[35]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[36]  Mark Mühlau,et al.  Left inferior parietal dominance in gesture imitation: an fMRI study , 2005, Neuropsychologia.

[37]  A. Meltzoff,et al.  What imitation tells us about social cognition: a rapprochement between developmental psychology and cognitive neuroscience. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[39]  S. Bookheimer Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[40]  M. Iacoboni Imitation, empathy, and mirror neurons. , 2009, Annual review of psychology.

[41]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

[42]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

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

[44]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[45]  D Yves von Cramon,et al.  Motion Class Dependency in Observers' Motor Areas Revealed by Functional Magnetic Resonance Imaging , 2005, The Journal of Neuroscience.

[46]  Rainer Goebel,et al.  Playing Charades in the fMRI: Are Mirror and/or Mentalizing Areas Involved in Gestural Communication? , 2009, PloS one.

[47]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[48]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[49]  Karl J. Friston,et al.  To Smooth or Not to Smooth? Bias and Efficiency in fMRI Time-Series Analysis , 2000, NeuroImage.

[50]  Rüdiger J Seitz,et al.  Functional modularity of the medial prefrontal cortex: involvement in human empathy. , 2006, Neuropsychology.

[51]  J. Mazziotta,et al.  Lateralization of the Human Mirror Neuron System , 2006, The Journal of Neuroscience.

[52]  Timothy E. J. Behrens,et al.  Functional organization of the medial frontal cortex , 2007, Current Opinion in Neurobiology.

[53]  M. Iacoboni,et al.  The self and social cognition: the role of cortical midline structures and mirror neurons , 2007, Trends in Cognitive Sciences.

[54]  S. Goldin-Meadow,et al.  The role of gesture in communication and thinking , 1999, Trends in Cognitive Sciences.

[55]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[56]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[57]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[58]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[59]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[60]  Ellen F. Lau,et al.  A cortical network for semantics: (de)constructing the N400 , 2008, Nature Reviews Neuroscience.