Premotor cortex mediates perceptual performance

Articulatory goals have long been proposed to mediate perception. Examples include direct realist and constructivist (analysis by synthesis) theories of speech perception. Although the activity in brain regions involved with action production has been shown to be present during action observation (Mirror Neuron System), the relationship of this activity to perceptual performance has not been clearly demonstrated at the event level. To this end we used functional magnetic resonance imaging fMRI and magnetoencephalography MEG to measure brain activity for correct and incorrect trials of an auditory phonetic identification in noise task. FMRI analysis revealed activity in the premotor cortex including the neighboring frontal opercular part of Broca's area (PMC/Broca's) for both perception and production tasks involving the same phonetic stimuli (potential mirror system site) that was significantly greater for correct over incorrect perceptual identification trials. Time-frequency analysis of single trials conducted over MEG current localized to PMC/Broca's using a hierarchical variational Bayesian source analysis technique revealed significantly greater event-related synchronization ERS and desynchronization ERD for correct over incorrect trials in the alpha, beta, and gamma frequency range prior to and after stimulus presentation. Together, these fMRI and MEG results are consistent with the hypothesis that articulatory processes serve to facilitate perceptual performance, while further dispelling concerns that activity found in ventral PMC/Broca's (mirror system) is merely a product of covert production of the perceived action. The finding of performance predictive activity prior to stimulus onset as well as activity related to task difficulty instead of information available in stimulation are consistent with constructivist and contrary to direct realist theories of perception.

[1]  M. Kawato,et al.  Attentional shifts towards an expected visual target alter the level of alpha-band oscillatory activity in the human calcarine cortex. , 2005, Brain research. Cognitive brain research.

[2]  Ernst Niebur,et al.  High-frequency gamma activity (80–150Hz) is increased in human cortex during selective attention , 2008, Clinical Neurophysiology.

[3]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[4]  Keiichi Tajima,et al.  Neural processes involved with perception of non-native durational contrasts , 2006, Neuroreport.

[5]  K. Linkenkaer-Hansen,et al.  Prestimulus Oscillations Enhance Psychophysical Performance in Humans , 2004, The Journal of Neuroscience.

[6]  Masa-aki Sato,et al.  Hierarchical Bayesian estimation for MEG inverse problem , 2004, NeuroImage.

[7]  G. Edelman Neural Darwinism: The Theory Of Neuronal Group Selection , 1989 .

[8]  G. Rizzolatti,et al.  Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons , 2002, Science.

[9]  David A. Medler,et al.  Neural correlates of sensory and decision processes in auditory object identification , 2004, Nature Neuroscience.

[10]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[11]  P. McGuire,et al.  Cortical substrates for the perception of face actions: an fMRI study of the specificity of activation for seen speech and for meaningless lower-face acts (gurning). , 2001, Brain research. Cognitive brain research.

[12]  Stephen J. Anderson,et al.  Elsevier Editorial System(tm) for Brain Research Manuscript Draft Response Letter Reviewer Number 1 Attentional Changes in Pre-stimulus Oscillatory Activity within Early Visual Cortex Are Predictive of Human Visual Performance , 2007 .

[13]  Marco Iacoboni,et al.  Beyond a Single Area: Motor Control and Language Within a Neural Architecture Encompassing Broca's Area , 2006, Cortex.

[14]  Jeffery A. Jones,et al.  Multisensory Integration Sites Identified by Perception of Spatial Wavelet Filtered Visual Speech Gesture Information , 2004, Journal of Cognitive Neuroscience.

[15]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[16]  Lori L. Holt,et al.  Reflections on mirror neurons and speech perception , 2009, Trends in Cognitive Sciences.

[17]  J. Schoffelen,et al.  Prestimulus Oscillatory Activity in the Alpha Band Predicts Visual Discrimination Ability , 2008, The Journal of Neuroscience.

[18]  Takashi Hanakawa,et al.  Song and speech: Brain regions involved with perception and covert production , 2006, NeuroImage.

[19]  Frank H. Guenther,et al.  An fMRI investigation of syllable sequence production , 2006, NeuroImage.

[20]  R. Brubaker Models for the perception of speech and visual form: Weiant Wathen-Dunn, ed.: Cambridge, Mass., The M.I.T. Press, I–X, 470 pages , 1968 .

[21]  D. Wolpert,et al.  Mental state inference using visual control parameters. , 2005, Brain research. Cognitive brain research.

[22]  J. Sarvas Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[23]  Marco Iacoboni,et al.  Neural responses to non-native phonemes varying in producibility: Evidence for the sensorimotor nature of speech perception , 2006, NeuroImage.

[24]  Jean-Luc Schwartz,et al.  Parieto-frontal gamma band activity during the perceptual emergence of speech forms , 2008, NeuroImage.

[25]  William Matchin,et al.  Broca's Area, Sentence Comprehension, and Working Memory: An fMRI Study , 2008, Frontiers in human neuroscience.

[26]  M. Erb,et al.  fMRI Evaluation of Somatotopic Representation in Human Primary Motor Cortex , 2000, NeuroImage.

[27]  Jeffery A. Jones,et al.  Phonetic perceptual identification by native- and second-language speakers differentially activates brain regions involved with acoustic phonetic processing and those involved with articulatory–auditory/orosensory internal models , 2004, NeuroImage.

[28]  T. Ergenoğlu,et al.  Alpha rhythm of the EEG modulates visual detection performance in humans. , 2004, Brain research. Cognitive brain research.

[29]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[30]  Mikko Sams,et al.  Processing of audiovisual speech in Broca's area , 2005, NeuroImage.

[31]  Michael P. Kaschak,et al.  Grounding language in action , 2002, Psychonomic bulletin & review.

[32]  Claus Lamm,et al.  Predicting the actions of others taps into one's own somatosensory representations—A functional MRI study , 2007, Neuropsychologia.

[33]  R. Schubotz Prediction of external events with our motor system: towards a new framework , 2007, Trends in Cognitive Sciences.

[34]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

[35]  J. Hirsch,et al.  fMRI Evidence for Cortical Modification during Learning of Mandarin Lexical Tone , 2003, Journal of Cognitive Neuroscience.

[36]  A M Liberman,et al.  Perception of the speech code. , 1967, Psychological review.

[37]  Vincent L. Gracco,et al.  A mediating role of the premotor cortex in phoneme segmentation , 2009, Brain and Language.

[38]  Gregor Thut,et al.  Prediction of response speed by anticipatory high‐frequency (gamma band) oscillations in the human brain , 2005, Human brain mapping.

[39]  Sarah-Jayne Blakemore,et al.  The role of motor contagion in the prediction of action , 2005, Neuropsychologia.

[40]  E. Bullmore,et al.  Response amplification in sensory-specific cortices during crossmodal binding. , 1999, Neuroreport.

[41]  Jeremy I. Skipper,et al.  Seeing Voices : How Cortical Areas Supporting Speech Production Mediate Audiovisual Speech Perception , 2007 .

[42]  R. Hari,et al.  Viewing Lip Forms Cortical Dynamics , 2002, Neuron.

[43]  Masa-aki Sato,et al.  Evaluation of hierarchical Bayesian method through retinotopic brain activities reconstruction from fMRI and MEG signals , 2008, NeuroImage.

[44]  M. Sams,et al.  Primary auditory cortex activation by visual speech: an fMRI study at 3 T , 2005, Neuroreport.

[45]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

[46]  Shinobu Masaki,et al.  Learning-induced neural plasticity associated with improved identification performance after training of a difficult second-language phonetic contrast , 2003, NeuroImage.

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

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

[49]  K. Doya,et al.  A unifying computational framework for motor control and social interaction. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  A. Glenberg,et al.  Processing Abstract Language Modulates Motor System Activity , 2008, Quarterly journal of experimental psychology.

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

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

[53]  Karl J. Friston,et al.  The mirror-neuron system: a Bayesian perspective. , 2007, Neuroreport.

[54]  Friedemann Pulvermüller,et al.  Motor cortex maps articulatory features of speech sounds , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Randy L Buckner,et al.  Common and dissociable activation patterns associated with controlled semantic and phonological processing: evidence from FMRI adaptation. , 2005, Cerebral cortex.

[56]  M. Turvey,et al.  The motor theory of speech perception reviewed , 2006, Psychonomic bulletin & review.

[57]  Marco Iacoboni,et al.  The Essential Role of Premotor Cortex in Speech Perception , 2007, Current Biology.

[58]  Marco Iacoboni,et al.  The role of premotor cortex in speech perception: Evidence from fMRI and rTMS , 2008, Journal of Physiology-Paris.

[59]  J Decety,et al.  Is perceptual anticipation a motor simulation? A PET study , 2001, Neuroreport.

[60]  E. Bullmore,et al.  Activation of auditory cortex during silent lipreading. , 1997, Science.

[61]  A. Kok,et al.  Neuroelectrical signs of selective attention to color in boys with attention-deficit hyperactivity disorder. , 2001, Brain research. Cognitive brain research.

[62]  L. Bernstein,et al.  Visual speech perception without primary auditory cortex activation , 2002, Neuroreport.

[63]  R. Campbell,et al.  Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex , 2000, Current Biology.

[64]  Jeffery A. Jones,et al.  Neural processes underlying perceptual enhancement by visual speech gestures , 2003, Neuroreport.

[65]  Christoph S. Herrmann,et al.  Human EEG very high frequency oscillations reflect the number of matches with a template in auditory short-term memory , 2008, Brain Research.

[66]  Jennifer H. Pfeifer,et al.  Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders , 2006, Nature Neuroscience.

[67]  D E Callan,et al.  Single-sweep EEG analysis of neural processes underlying perception and production of vowels. , 2000, Brain research. Cognitive brain research.

[68]  N. A. Borghese,et al.  A functional-anatomical model for lipreading. , 2003, Journal of neurophysiology.

[69]  V M Haughton,et al.  A comparison of functional MR activation patterns during silent and audible language tasks. , 1995, AJNR. American journal of neuroradiology.

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

[71]  K. Amunts,et al.  Broca's region: from action to language. , 2005, Physiology.

[72]  L. Fadiga,et al.  The Motor Somatotopy of Speech Perception , 2009, Current Biology.

[73]  J. Gibson The Ecological Approach to Visual Perception , 1979 .

[74]  M J Brammer,et al.  Dispersed activation in the left temporal cortex for speech-reading in congenitally deaf people , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[75]  Mikko Sams,et al.  Viewing speech modulates activity in the left SI mouth cortex , 2005, NeuroImage.

[76]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[77]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[78]  D. Poeppel,et al.  Speech perception at the interface of neurobiology and linguistics , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[79]  Gerald M. Edelman,et al.  The Remembered Present; A Biological Theory of Consciousness. , 1994 .

[80]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[81]  M. Iacoboni,et al.  Listening to speech activates motor areas involved in speech production , 2004, Nature Neuroscience.

[82]  R. Campbell,et al.  Reading Speech from Still and Moving Faces: The Neural Substrates of Visible Speech , 2003, Journal of Cognitive Neuroscience.

[83]  Steven L. Small,et al.  Listening to talking faces: motor cortical activation during speech perception , 2005, NeuroImage.

[84]  Bruno Rossion,et al.  Category Specificity in Early Perception: Face and Word N170 Responses Differ in Both Lateralization and Habituation Properties , 2008, Frontiers in human neuroscience.

[85]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[86]  F. Garbarini,et al.  At the root of embodied cognition: Cognitive science meets neurophysiology , 2004, Brain and Cognition.

[87]  A. Liberman,et al.  The motor theory of speech perception revised , 1985, Cognition.

[88]  Jeremy I. Skipper,et al.  Speech-associated gestures, Broca’s area, and the human mirror system , 2007, Brain and Language.

[89]  J. Gore,et al.  A comparison of bound and unbound audio-visual information processing in the human cerebral cortex. , 2002, Brain research. Cognitive brain research.

[90]  G. Edelman,et al.  A Universe Of Consciousness: How Matter Becomes Imagination , 2000 .

[91]  C. Fowler An event approach to the study of speech perception from a direct realist perspective , 1986 .