FMRI study of emotional speech comprehension.

Little is known about the neural correlates of affective prosody in the context of affective semantic discourse. We used functional magnetic resonance imaging to investigate this issue while subjects performed 1) affective classification of sentences having an affective semantic content and 2) grammatical classification of sentences with neutral semantic content. Sentences of each type were produced half by actors and half by a text-to-speech software lacking affective prosody. Compared with neutral sentences processing, sentences with affective semantic content--with or without affective prosody--led to an increase in activation of a left inferior frontal area involved in the retrieval of semantic knowledge. In addition, the posterior part of the left superior temporal sulcus (STS) together with the medial prefrontal cortex were recruited, although not activated by neutral sentences classification. Interestingly, these areas have been described as implicated during self-reflection or other's mental state inference that possibly occurred during the affective classification task. When affective prosody was present, additional rightward activations of the human-selective voice area and the posterior part of STS were observed, corresponding to the processing of speaker's voice emotional content. Accurate affective communication, central to social interactions, requires the cooperation of semantics, affective prosody, and mind-reading neural networks.

[1]  K. Heilman,et al.  Comprehension of emotional prosody following unilateral hemispheric lesions: Processing defect versus distraction defect , 1987, Neuropsychologia.

[2]  Hanneke E. M. den Ouden,et al.  Thinking about intentions , 2005, NeuroImage.

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

[4]  K. Scherer,et al.  The voices of wrath: brain responses to angry prosody in meaningless speech , 2005, Nature Neuroscience.

[5]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

[6]  E. Ross,et al.  The aprosodias. Functional-anatomic organization of the affective components of language in the right hemisphere. , 1981, Archives of neurology.

[7]  J Ashburner,et al.  Functional neuroimaging of speech perception in six normal and two aphasic subjects. , 1999, The Journal of the Acoustical Society of America.

[8]  Sterling C. Johnson,et al.  The Cerebral Response during Subjective Choice with and without Self-reference , 2005, Journal of Cognitive Neuroscience.

[9]  Michael J. Brammer,et al.  The role of ‘shared representations’ in social perception and empathy: An fMRI study , 2006, NeuroImage.

[10]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[11]  M. Erb,et al.  Dynamic Brain Activation during Processing of Emotional Intonation: Influence of Acoustic Parameters, Emotional Valence, and Sex , 2002, NeuroImage.

[12]  Sterling C. Johnson,et al.  Self-appraisal decisions evoke dissociated dorsal—ventral aMPFC networks , 2006, NeuroImage.

[13]  Andreas Kleinschmidt,et al.  Interaction of Face and Voice Areas during Speaker Recognition , 2005, Journal of Cognitive Neuroscience.

[14]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[15]  M. Mesulam Principles of Behavioral and Cognitive Neurology , 2000 .

[16]  R. Elliott,et al.  The neural response to emotional prosody, as revealed by functional magnetic resonance imaging , 2003, Neuropsychologia.

[17]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[18]  F. Bermpohl,et al.  Cortical midline structures and the self , 2004, Trends in Cognitive Sciences.

[19]  Kevin N. Ochsner,et al.  The neural correlates of direct and reflected self-knowledge , 2005, NeuroImage.

[20]  Scott T. Grafton,et al.  Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking , 2006, Neuropsychologia.

[21]  A. Kleinschmidt,et al.  Modulation of neural responses to speech by directing attention to voices or verbal content. , 2003, Brain research. Cognitive brain research.

[22]  E. Ross,et al.  Lateralization of Affective Prosody in Brain and the Callosal Integration of Hemispheric Language Functions , 1997, Brain and Language.

[23]  E. Bullmore,et al.  Common and Distinct Neural Substrates for Pragmatic, Semantic, and Syntactic Processing of Spoken Sentences: An fMRI Study , 2000, Journal of Cognitive Neuroscience.

[24]  K. Heilman,et al.  Understanding emotional prosody activates right hemisphere regions. , 1996, Archives of neurology.

[25]  Masatoshi Itoh,et al.  Target dependency of brain mechanism involved in dispositional inference: a PET study , 2004, NeuroImage.

[26]  D. V. von Cramon,et al.  FMRI reveals brain regions mediating slow prosodic modulations in spoken sentences , 2002, Human brain mapping.

[27]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[28]  C. Frith,et al.  Movement and Mind: A Functional Imaging Study of Perception and Interpretation of Complex Intentional Movement Patterns , 2000, NeuroImage.

[29]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[30]  B. Renault,et al.  Functional Anatomy of Human Auditory Attention Studied with PET , 1997, NeuroImage.

[31]  D. Bub,et al.  The Neural Substrate for Concrete, Abstract, and Emotional Word Lexica A Positron Emission Tomography Study , 1997, Journal of Cognitive Neuroscience.

[32]  D. Perrett,et al.  Dissociable neural responses to facial expressions of sadness and anger. , 1999, Brain : a journal of neurology.

[33]  A. Liberman,et al.  Parametrically Dissociating Speech and Nonspeech Perception in the Brain Using fMRI , 2001, Brain and Language.

[34]  K. Heilman,et al.  The role of the right hemisphere in emotional communication. , 1991, Brain : a journal of neurology.

[35]  Michel Morel,et al.  « Kali », synthèse vocale à partir du texte : De la conception à la mise en oeuvre , 2001 .

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

[37]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[38]  Hermann Ackermann,et al.  The contribution of the insula to motor aspects of speech production: A review and a hypothesis , 2004, Brain and Language.

[39]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[40]  G Jobard,et al.  Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies , 2003, NeuroImage.

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

[42]  A. Liberman,et al.  On the relation of speech to language , 2000, Trends in Cognitive Sciences.

[43]  D. Poeppel,et al.  The effect of spectral manipulations on the identification of affective and linguistic prosody , 2003, Brain and Language.

[44]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[45]  C. Neil Macrae,et al.  Forming impressions of people versus inanimate objects: Social-cognitive processing in the medial prefrontal cortex , 2005, NeuroImage.

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

[47]  D. Premack,et al.  Does the chimpanzee have a theory of mind? , 1978, Behavioral and Brain Sciences.

[48]  E. Courchesne,et al.  Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. , 2001, Brain : a journal of neurology.

[49]  K. Zilles,et al.  Mind Reading: Neural Mechanisms of Theory of Mind and Self-Perspective , 2001, NeuroImage.

[50]  J. Decety,et al.  A PET Investigation of the Attribution of Intentions with a Nonverbal Task , 2000, NeuroImage.

[51]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[52]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[53]  Alexander Todorov,et al.  Attributions on the brain: Neuro-imaging dispositional inferences, beyond theory of mind , 2005, NeuroImage.

[54]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[55]  Pascal Belin,et al.  Abnormal cortical voice processing in autism , 2004, Nature Neuroscience.

[56]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

[57]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[58]  Evelyn C. Ferstl,et al.  What Does the Frontomedian Cortex Contribute to Language Processing: Coherence or Theory of Mind? , 2002, NeuroImage.

[59]  Y. Samson,et al.  Lateralization of Speech and Auditory Temporal Processing , 1998, Journal of Cognitive Neuroscience.

[60]  Libero Verard,et al.  Fully automatic identification of AC and PC landmarks on brain MRI using scene analysis , 1997, IEEE Transactions on Medical Imaging.

[61]  A. Friederici,et al.  On the lateralization of emotional prosody: An event-related functional MR investigation , 2003, Brain and Language.

[62]  Wolfgang Grodd,et al.  Identification of emotional intonation evaluated by fMRI , 2005, NeuroImage.

[63]  M Erb,et al.  Distinct frontal regions subserve evaluation of linguistic and emotional aspects of speech intonation. , 2004, Cerebral cortex.

[64]  J. Decety,et al.  What you believe versus what you think they believe: a neuroimaging study of conceptual perspective‐taking , 2003, The European journal of neuroscience.

[65]  Vinod Goel,et al.  Neuroanatomical Correlates of Human Reasoning , 1998, Journal of Cognitive Neuroscience.

[66]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

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

[68]  P. Belin,et al.  Thinking the voice: neural correlates of voice perception , 2004, Trends in Cognitive Sciences.

[69]  Pascal Belin,et al.  Is voice processing species-specific in human auditory cortex? An fMRI study , 2004, NeuroImage.

[70]  Yasushi Miyashita,et al.  From Perception to Sentence Comprehension: The Convergence of Auditory and Visual Information of Language in the Left Inferior Frontal Cortex , 2002, NeuroImage.

[71]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[72]  Y. Miyashita,et al.  A syntactic specialization for Broca's area. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Istvan Molnar-Szakacs,et al.  Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline , 2004, NeuroImage.

[74]  L. Tan,et al.  Functional anatomy of syntactic and semantic processing in language comprehension , 2002, Human brain mapping.

[75]  J. Armony,et al.  Priming of non-speech vocalizations in male adults: The influence of the speaker's gender , 2004, Brain and Cognition.

[76]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[77]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[78]  M. Brüne "Theory of mind" in schizophrenia: a review of the literature. , 2005, Schizophrenia bulletin.

[79]  Karl J. Friston,et al.  Hearing and saying. The functional neuro-anatomy of auditory word processing. , 1996, Brain : a journal of neurology.

[80]  Joel R. Meyer,et al.  Modality independence of word comprehension , 2002, Human brain mapping.

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

[82]  Richard S. J. Frackowiak,et al.  Analysis of temporal structure in sound by the human brain , 1998, Nature Neuroscience.

[83]  G. Winocur,et al.  In Search of the Self: A Positron Emission Tomography Study , 1999 .

[84]  P. Mousty,et al.  Brulex: une base de donne 'es lexicales informatise 'e pour le franc?ais e 'crit et parle , 1990 .

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

[86]  E Altenmüller,et al.  The cortical processing of perceived emotion: a DC‐potential study on affective speech prosody , 1997, Neuroreport.

[87]  Reginald B. Adams,et al.  A Comparison of Neural Circuits Underlying Auditory and Visual Object Categorization , 2002, NeuroImage.

[88]  C. Neil Macrae,et al.  The Link between Social Cognition and Self-referential Thought in the Medial Prefrontal Cortex , 2005, Journal of Cognitive Neuroscience.

[89]  Mahzarin R. Banaji,et al.  Encoding-Specific Effects of Social Cognition on the Neural Correlates of Subsequent Memory , 2004, The Journal of Neuroscience.

[90]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

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

[92]  M. Hallett,et al.  Modeling other minds , 1995, Neuroreport.

[93]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[94]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[95]  R. Zatorre,et al.  Adaptation to speaker's voice in right anterior temporal lobe , 2003, Neuroreport.

[96]  R. Schultz Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area , 2005, International Journal of Developmental Neuroscience.

[97]  Sophie K. Scott,et al.  Impaired auditory recognition of fear and anger following bilateral amygdala lesions , 1997, Nature.