A Supramodal Neural Network for Speech and Gesture Semantics: An fMRI Study

In a natural setting, speech is often accompanied by gestures. As language, speech-accompanying iconic gestures to some extent convey semantic information. However, if comprehension of the information contained in both the auditory and visual modality depends on same or different brain-networks is quite unknown. In this fMRI study, we aimed at identifying the cortical areas engaged in supramodal processing of semantic information. BOLD changes were recorded in 18 healthy right-handed male subjects watching video clips showing an actor who either performed speech (S, acoustic) or gestures (G, visual) in more (+) or less (−) meaningful varieties. In the experimental conditions familiar speech or isolated iconic gestures were presented; during the visual control condition the volunteers watched meaningless gestures (G−), while during the acoustic control condition a foreign language was presented (S−). The conjunction of the visual and acoustic semantic processing revealed activations extending from the left inferior frontal gyrus to the precentral gyrus, and included bilateral posterior temporal regions. We conclude that proclaiming this frontotemporal network the brain's core language system is to take too narrow a view. Our results rather indicate that these regions constitute a supramodal semantic processing network.

[1]  Leonardo Fogassi,et al.  Anterior intraparietal cortex codes complexity of observed hand movements , 2010, Brain Research Bulletin.

[2]  A. Nobre,et al.  The Response of Left Temporal Cortex to Sentences , 2002, Journal of Cognitive Neuroscience.

[3]  A. Braun,et al.  Neural responses to meaningless pseudosigns: Evidence for sign-based phonetic processing in superior temporal cortex , 2011, Brain and Language.

[4]  C. Fiebach,et al.  The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. , 2003, Cerebral cortex.

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

[6]  Angela D. Friederici,et al.  Lateral Inferotemporal Cortex Maintains ConceptualSemantic Representations in Verbal Working Memory , 2007, Journal of Cognitive Neuroscience.

[7]  Spencer D. Kelly,et al.  Gesture, brain, and language , 2007, Brain and Language.

[8]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[9]  Bentin Shlomo Neural correlates of semantic and episodic memory for faces: evidence from multiple frequency bands , 2008 .

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

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

[12]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[13]  K. Willmes,et al.  Neural interaction of speech and gesture: Differential activations of metaphoric co-verbal gestures , 2009, Neuropsychologia.

[14]  A. Damasioa,et al.  Neural systems behind word and concept retrieval , 2004 .

[15]  P. Hagoort On Broca, brain, and binding: a new framework , 2005, Trends in Cognitive Sciences.

[16]  Tilo Kircher,et al.  Social cues, mentalizing and the neural processing of speech accompanied by gestures , 2010, Neuropsychologia.

[17]  J. Decety,et al.  Neural mechanisms subserving the perception of human actions , 1999, Trends in Cognitive Sciences.

[18]  S. Kelly,et al.  Neural correlates of bimodal speech and gesture comprehension , 2004, Brain and Language.

[19]  Tilo Kircher,et al.  Categorical and thematic knowledge representation in the brain: Neural correlates of taxonomic and thematic conceptual relations , 2008, Neuropsychologia.

[20]  G. McCarthy,et al.  Human Brain Mapping 6:1–13(1998) � Functional MRI Studies of Auditory Comprehension , 2022 .

[21]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[22]  Seana Coulson,et al.  Iconic gestures prime related concepts: An ERP study , 2007, Psychonomic bulletin & review.

[23]  Angela D. Friederici,et al.  Gesture Facilitates the Syntactic Analysis of Speech , 2012, Front. Psychology.

[24]  Marco Davare,et al.  Causal Connectivity between the Human Anterior Intraparietal Area and Premotor Cortex during Grasp , 2010, Current Biology.

[25]  R. Adolphs,et al.  Neural systems behind word and concept retrieval , 2004, Cognition.

[26]  S. Krach,et al.  Taxonomic and thematic categories: Neural correlates of categorization in an auditory-to-visual priming task using fMRI , 2009, Brain Research.

[27]  D. Schacter,et al.  Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. , 2000, Brain : a journal of neurology.

[28]  Bernard Mazoyer,et al.  What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis , 2011, NeuroImage.

[29]  Susan Goldin-Meadow,et al.  CNS activation and regional connectivity during pantomime observation: No engagement of the mirror neuron system for deaf signers , 2010, NeuroImage.

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

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

[32]  G. Beattie,et al.  Iconic hand gestures and the predictability of words in context in spontaneous speech. , 2000, British journal of psychology.

[33]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[34]  Angela D. Friederici,et al.  Dynamic assignment of neural resources in auditory comprehension of complex sentences , 2011, NeuroImage.

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

[36]  Roel M. Willems,et al.  When language meets action: the neural integration of gesture and speech. , 2007, Cerebral cortex.

[37]  Thomas C. Gunter,et al.  What Iconic Gesture Fragments Reveal about Gesture–Speech Integration: When Synchrony Is Lost, Memory Can Help , 2011, Journal of Cognitive Neuroscience.

[38]  D. McNeill Gesture and Thought , 2005 .

[39]  Robert Lindenberg,et al.  Supramodal language comprehension: Role of the left temporal lobe for listening and reading , 2007, Neuropsychologia.

[40]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[41]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[42]  L. Buxbaum,et al.  On beyond mirror neurons: internal representations subserving imitation and recognition of skilled object-related actions in humans. , 2005, Brain research. Cognitive brain research.

[43]  Jason B. Mattingley,et al.  Selective attention modulates inferior frontal gyrus activity during action observation , 2008, NeuroImage.

[44]  Tilo Kircher,et al.  Memory Effects of Speech and Gesture Binding: Cortical and Hippocampal Activation in Relation to Subsequent Memory Performance , 2009, Journal of Cognitive Neuroscience.

[45]  Tilo Kircher,et al.  Lion – tiger – stripes: Neural correlates of indirect semantic priming across processing modalities , 2009, NeuroImage.

[46]  G. Orban,et al.  Coding observed motor acts: different organizational principles in the parietal and premotor cortex of humans. , 2010, Journal of neurophysiology.

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

[48]  D. Callan,et al.  Giving speech a hand: Gesture modulates activity in auditory cortex during speech perception , 2009, Human brain mapping.

[49]  Gina R. Kuperberg,et al.  Neuroanatomical distinctions within the semantic system during sentence comprehension: Evidence from functional magnetic resonance imaging , 2008, NeuroImage.

[50]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[51]  M Jeannerod,et al.  Visual pathways for object-oriented action and object recognition: functional anatomy with PET. , 1997, Cerebral cortex.

[52]  S. Sato,et al.  fMRI language task panel improves determination of language dominance , 2004, Neurology.

[53]  Pierre Feyereisen,et al.  The Meaning of Gestures - What Can Be Understood Without Speech , 1988 .

[54]  T. Kircher,et al.  The differentiation of iconic and metaphoric gestures: Common and unique integration processes , 2011, Human brain mapping.

[55]  Tilo Kircher,et al.  How Different Types of Conceptual Relations Modulate Brain Activation during Semantic Priming , 2011, Journal of Cognitive Neuroscience.

[56]  D. Schacter,et al.  A sensory signature that distinguishes true from false memories , 2004, Nature Neuroscience.

[57]  Luca Turella,et al.  Neurofunctional modulation of brain regions by the observation of pointing and grasping actions. , 2009, Cerebral cortex.

[58]  Sotaro Kita,et al.  On-line Integration of Semantic Information from Speech and Gesture: Insights from Event-related Brain Potentials , 2007, Journal of Cognitive Neuroscience.

[59]  Angela D. Friederici,et al.  Cooperation of different neuronal systems during hand sign recognition , 2004, NeuroImage.

[60]  F. Fazio,et al.  Brain processing of native and foreign languages , 1996, NeuroImage.

[61]  G. Rizzolatti,et al.  Neural Circuits Underlying Imitation Learning of Hand Actions An Event-Related fMRI Study , 2004, Neuron.

[62]  Karl J. Friston,et al.  The Trouble with Cognitive Subtraction , 1996, NeuroImage.

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

[64]  Luciano Fadiga,et al.  Hand Actions and Speech Representation in Broca's Area , 2006, Cortex.

[65]  Christian Obermeier,et al.  Exploring the significance of task, timing and background noise on gesture-speech integration (Doctoral dissertation). MPI Series in Human Cognitive and Brain Sciences: Vol. 133 , 2011 .

[66]  Asli Ozyurek,et al.  Gesture, language, and brain , 2007 .

[67]  Thomas C. Gunter,et al.  The Role of Iconic Gestures in Speech Disambiguation: ERP Evidence , 2007, Journal of Cognitive Neuroscience.

[68]  Tilo Kircher,et al.  Automatic processing of semantic relations in fMRI: Neural activation during semantic priming of taxonomic and thematic categories , 2008, Brain Research.

[69]  Jody C Culham,et al.  fMRI Repetition Suppression for Familiar But Not Arbitrary Actions with Tools , 2012, The Journal of Neuroscience.

[70]  Roel M. Willems,et al.  Differential roles for left inferior frontal and superior temporal cortex in multimodal integration of action and language , 2009, NeuroImage.

[71]  Tilo Kircher,et al.  Neural integration of speech and gesture in schizophrenia: Evidence for differential processing of metaphoric gestures , 2013, Human brain mapping.

[72]  Istvan Molnar-Szakacs,et al.  Making the Connection: Polar Sites Are Key to Assembly in Many Immune Receptors , 2006, PLoS biology.

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

[74]  Scott H. Johnson-Frey The neural bases of complex tool use in humans , 2004, Trends in Cognitive Sciences.

[75]  J B Poline,et al.  Brain imaging of language plasticity in adopted adults: can a second language replace the first? , 2001, NeuroImage.

[76]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[77]  A. Meltzoff,et al.  An fMRI study of imitation: action representation and body schema , 2005, Neuropsychologia.

[78]  Ying Choon Wu,et al.  How iconic gestures enhance communication: An ERP study , 2007, Brain and Language.

[79]  D. Shankweiler,et al.  An Event-related Neuroimaging Study Distinguishing Form and Content in Sentence Processing , 2000, Journal of Cognitive Neuroscience.

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

[81]  Thomas C. Gunter,et al.  The benefit of gestures during communication: Evidence from hearing and hearing-impaired individuals , 2012, Cortex.

[82]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[83]  J. Trueswell,et al.  Cognitive control and parsing: Reexamining the role of Broca’s area in sentence comprehension , 2005, Cognitive, affective & behavioral neuroscience.

[84]  Alex Martin,et al.  Neural correlates of semantic and episodic memory retrieval , 1998, Neuropsychologia.

[85]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

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

[87]  Andreas Hennenlotter,et al.  Neural correlates of the processing of co-speech gestures , 2008, NeuroImage.

[88]  Tilo Kircher,et al.  Priming words with pictures: Neural correlates of semantic associations in a cross‐modal priming task using fMRI , 2009, Human brain mapping.

[89]  Weijia Ni,et al.  Sentence complexity and input modality effects in sentence comprehension: an fMRI study , 2004, NeuroImage.

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

[91]  Ying Choon Wu,et al.  Meaningful gestures: electrophysiological indices of iconic gesture comprehension. , 2005, Psychophysiology.

[92]  Cheryl M. Capek,et al.  The signing brain: the neurobiology of sign language , 2008, Trends in Cognitive Sciences.

[93]  M. Corballis Mirror neurons and the evolution of language , 2010, Brain and Language.

[94]  M. Corballis,et al.  From manual gesture to speech: A gradual transition , 2006, Neuroscience & Biobehavioral Reviews.

[95]  P. McGuire,et al.  Engagement of right temporal cortex during processing of linguistic context , 2001, Neuropsychologia.

[96]  Jeremy I. Skipper,et al.  Co‐speech gestures influence neural activity in brain regions associated with processing semantic information , 2009, Human brain mapping.

[97]  Tilo Kircher,et al.  Encoding Social Interactions: The Neural Correlates of True and False Memories , 2011, Journal of Cognitive Neuroscience.

[98]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[99]  Petra Schmalbrock,et al.  An fMRI Study of Semantic Priming: Modulation of Brain Activity by Varying Semantic Distances , 2006, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[100]  M. Corballis From mouth to hand: Gesture, speech, and the evolution of right-handedness , 2003, Behavioral and Brain Sciences.

[101]  P. McGuire,et al.  Neural systems underlying British Sign Language and audio-visual English processing in native users. , 2002, Brain : a journal of neurology.

[102]  A. Jansen,et al.  Neural integration of iconic and unrelated coverbal gestures: A functional MRI study , 2009, Human brain mapping.

[103]  R. Murray,et al.  Neural correlates of formal thought disorder in schizophrenia: preliminary findings from a functional magnetic resonance imaging study. , 2001, Archives of general psychiatry.

[104]  Jonas Obleser,et al.  Integration of iconic gestures and speech in left superior temporal areas boosts speech comprehension under adverse listening conditions , 2010, NeuroImage.