Broca’s Area: Linking Perception and Production in Language and Actions

A distinction between action perception and production has always been emphasized by traditional accounts of brain function. The goal of this review is to show that this simple distinction seems no longer valid. Broca’s area in particular seems to be important for both perception and production of language and action. Functional imaging studies suggest that Broca’s area is active both when people produce and perceive syntactically complex sentences and while they produce and perceive complex actions. Lesions in this area disrupt the capacity to produce syntactically correct sentences and to perceive sentences in which syntax is essential. From an action-perspective, lesions to Broca’s area disrupt the capacity to produce goal-directed actions and to perceive the actions of others. Furthermore, the property and location of mirror neurons in the monkey might provide the reason why Broca’s area in humans has a dual function in production and perception.

[1]  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.

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

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

[4]  D. V. von Cramon,et al.  Neurocognition of auditory sentence comprehension: event related fMRI reveals sensitivity to syntactic violations and task demands. , 2000, Brain research. Cognitive brain research.

[5]  O. Hauk,et al.  Neurophysiological distinction of action words in the fronto‐central cortex , 2004, Human brain mapping.

[6]  Christian Keysers,et al.  The anthropomorphic brain: The mirror neuron system responds to human and robotic actions , 2007, NeuroImage.

[7]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[8]  Salvatore Maria Aglioti,et al.  The Sound of Actions in Apraxia , 2008, Current Biology.

[9]  D. V. Cramon,et al.  Predicting Perceptual Events Activates Corresponding Motor Schemes in Lateral Premotor Cortex: An fMRI Study , 2002, NeuroImage.

[10]  Läsion im ventrolateralen prämotorischen Kortex beeinträchtigt die Greiffunktion , 2003 .

[11]  C. Keysers,et al.  Empathy and the Somatotopic Auditory Mirror System in Humans , 2006, Current Biology.

[12]  Y. Grodzinsky Trace Deletion, Θ-Roles, and Cognitive Strategies , 1995, Brain and Language.

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

[14]  A. Pick,et al.  Die agrammatischen Sprachstörungen , 1913 .

[15]  P Hagoort,et al.  A neural correlate of syntactic encoding during speech production , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  H. Freund,et al.  Tactile apraxia: unimodal apractic disorder of tactile object exploration associated with parietal lobe lesions. , 2001, Brain : a journal of neurology.

[17]  N. Geschwind Language and the brain. , 1972, Scientific American.

[18]  M. Makuuchi Is Broca's area crucial for imitation? , 2005, Cerebral cortex.

[19]  Ria De Bleser,et al.  Morphological Processing in Italian Agrammatic Speakers: Eight Experiments in Lexical Morphology , 1996, Brain and Language.

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

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

[22]  Vittorio Gallese,et al.  Listening to Action-related Sentences Activates Fronto-parietal Motor Circuits , 2005, Journal of Cognitive Neuroscience.

[23]  R. Passingham,et al.  Broca's area and the origins of human vocal skill. , 1981, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  Christian Keysers,et al.  Aplasics Born without Hands Mirror the Goal of Hand Actions with Their Feet , 2007, Current Biology.

[25]  A. Damasio,et al.  Nouns and verbs are retrieved with differently distributed neural systems. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[26]  R. Passingham The frontal lobes and voluntary action , 1993 .

[27]  Maria Teresa Guasti,et al.  Comprehension of reversible active and passive sentences in agrammatism , 2001 .

[28]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

[29]  Brian MacWhinney,et al.  Cross-linguistic research in aphasia: An overview , 1991, Brain and Language.

[30]  F Lhermitte,et al.  [Description and scanographic study of Leborgne's brain. Broca's discovery]. , 1980, Revue neurologique.

[31]  Volkmar Glauche,et al.  The human action recognition system and its relationship to Broca’s area: an fMRI study , 2003, NeuroImage.

[32]  R. Seitz,et al.  Learning of Sequential Finger Movements in Man: A Combined Kinematic and Positron Emission Tomography (PET) Study , 1992, The European journal of neuroscience.

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

[34]  A. Pick,et al.  Die Agrammatischen Sprachstörungen: Studien zur Psychologischen Grundlegung der Aphasielehre , 1913 .

[35]  T. Hendler,et al.  The Neural Reality of Syntactic Transformations , 2003, Psychological science.

[36]  R. Passingham,et al.  The Preparation, Execution and Suppression of Copied Movements in the Human Brain , 1996 .

[37]  R. Schubotz,et al.  Dynamic patterns make the premotor cortex interested in objects: influence of stimulus and task revealed by fMRI. , 2002, Brain research. Cognitive brain research.

[38]  S. F. Cappa,et al.  Action and object processing in aphasia: From nouns and verbs to the effect of manipulability , 2007, Brain and Language.

[39]  Christian Keysers,et al.  Testing Simulation Theory with Cross-Modal Multivariate Classification of fMRI Data , 2008, PloS one.

[40]  S. Aglioti,et al.  Neural Underpinnings of Gesture Discrimination in Patients with Limb Apraxia , 2008, The Journal of Neuroscience.

[41]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[42]  Yosef Grodzinsky,et al.  Neural correlates of syntactic movement: converging evidence from two fMRI experiments , 2004, NeuroImage.

[43]  Lewis P. Shapiro,et al.  Verb processing during sentence comprehension in aphasia , 1990, Brain and Language.

[44]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[45]  G. Rizzolatti,et al.  Localization of grasp representations in humans by PET: 1. Observation versus execution , 1996, Experimental Brain Research.

[46]  Y. Grodzinsky The neurology of syntax: Language use without Broca's area , 2000, Behavioral and Brain Sciences.

[47]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

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

[49]  G. Bonin,et al.  Pattern of the cerebral isocortex , 1961 .

[50]  J. Mazziotta,et al.  Modulation of cortical activity during different imitative behaviors. , 2003, Journal of neurophysiology.

[51]  K. Amunts,et al.  Broca's region , 2006 .

[52]  C. Keysers,et al.  Towards a unifying neural theory of social cognition. , 2006, Progress in brain research.

[53]  J. Müller,et al.  Of the brain. , 1837 .

[54]  E. Cabanis,et al.  Paul Broca's historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. , 2007, Brain : a journal of neurology.

[55]  G. Rizzolatti,et al.  Congruent Embodied Representations for Visually Presented Actions and Linguistic Phrases Describing Actions , 2006, Current Biology.

[56]  A. Caramazza,et al.  On the Basis for the Agrammatic's Difficulty in Producing Main Verbs , 1984, Cortex.

[57]  R. E Passingham,et al.  Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study , 2003, NeuroImage.

[58]  A. Campbell Histological Studies on the Localisation of Cerebral Function , 2009 .

[59]  R. Knight,et al.  Cortical Networks Underlying Mechanisms of Time Perception , 1998, The Journal of Neuroscience.

[60]  R. Bastiaanse,et al.  Spontaneous speech in Italian agrammatic aphasia: A focus on verb production , 2008 .

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

[62]  L. Fogassi,et al.  Audiovisual mirror neurons and action recognition , 2003, Experimental Brain Research.

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

[64]  E. Renzi,et al.  Imitating gestures. A quantitative approach to ideomotor apraxia. , 1980, Archives of neurology.

[65]  R. J. Seitz,et al.  A parieto-premotor network for object manipulation: evidence from neuroimaging , 1999, Experimental Brain Research.

[66]  D. V. von Cramon,et al.  Functional organization of the lateral premotor cortex: fMRI reveals different regions activated by anticipation of object properties, location and speed. , 2001, Brain research. Cognitive brain research.

[67]  H. Gräfin von Einsiedel,et al.  The role of lateral premotor-cerebellar-parietal circuits in motor sequence control: a parametric fMRI study. , 2002, Brain research. Cognitive brain research.

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

[69]  Jens Frahm,et al.  Equivalent Responses to Lexical and Nonlexical Visual Stimuli in Occipital Cortex: A Functional Magnetic Resonance Imaging Study , 1997, NeuroImage.

[70]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[71]  A. Caramazza,et al.  Dissociation of algorithmic and heuristic processes in language comprehension: Evidence from aphasia , 1976, Brain and Language.

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

[73]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

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

[75]  D. V. Cramon,et al.  Functional–anatomical concepts of human premotor cortex: evidence from fMRI and PET studies , 2003, NeuroImage.

[76]  A. Goldman,et al.  Mirror neurons and the simulation theory of mind-reading , 1998, Trends in Cognitive Sciences.

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

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

[79]  Antonia F. de C. Hamilton,et al.  Action Understanding Requires the Left Inferior Frontal Cortex , 2006, Current Biology.

[80]  R. Adolphs,et al.  NEURAL CORRELATES OF CONCEPTUAL KNOWLEDGE FOR ACTIONS , 2003, Cognitive neuropsychology.

[81]  O. Foerster,et al.  THE MOTOR CORTEX IN MAN IN THE LIGHT OF HUGHLINGS JACKSON'S DOCTRINES , 1936 .

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

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

[84]  M. Erb,et al.  Overt sentence production in event-related fMRI , 2005, Neuropsychologia.

[85]  R. Berndt,et al.  Retrieval of nouns and verbs in agrammatism and anomia , 1990, Brain and Language.

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

[87]  D. Yves von Cramon,et al.  A Blueprint for Target Motion: fMRI Reveals Perceived Sequential Complexity to Modulate Premotor Cortex , 2002, NeuroImage.

[88]  S. Bookheimer,et al.  Form and Content Dissociating Syntax and Semantics in Sentence Comprehension , 1999, Neuron.

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

[90]  R. Hari,et al.  Temporal dynamics of cortical representation for action. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Elizabeth Bates,et al.  Action comprehension in aphasia: linguistic and non-linguistic deficits and their lesion correlates , 2004, Neuropsychologia.

[92]  J. Grèzes,et al.  What is “mirror” in the premotor cortex? A review , 2008, Neurophysiologie Clinique/Clinical Neurophysiology.

[93]  Peter Hagoort,et al.  A PET study of cerebral activation patterns induced by verb inflection , 1997 .

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

[95]  J. Jaeger A POSITRON EMISSION TOMOGRAPHIC STUDY OF REGULAR AND IRREGULAR VERB MORPHOLOGY IN ENGLISH , 1996 .

[96]  A D Friederici,et al.  Syntactic Working Memory and the Establishment of Filler-Gap Dependencies: Insights from ERPs and fMRI , 2001, Journal of psycholinguistic research.

[97]  C. Luzzatti,et al.  Linguistic theory and morphosyntactic impairments in German and Italian aphasics , 1996, Journal of Neurolinguistics.