Time Course of the Involvement of the Right Anterior Superior Temporal Gyrus and the Right Fronto-Parietal Operculum in Emotional Prosody Perception

In verbal communication, not only the meaning of the words convey information, but also the tone of voice (prosody) conveys crucial information about the emotional state and intentions of others. In various studies right frontal and right temporal regions have been found to play a role in emotional prosody perception. Here, we used triple-pulse repetitive transcranial magnetic stimulation (rTMS) to shed light on the precise time course of involvement of the right anterior superior temporal gyrus and the right fronto-parietal operculum. We hypothesized that information would be processed in the right anterior superior temporal gyrus before being processed in the right fronto-parietal operculum. Right-handed healthy subjects performed an emotional prosody task. During listening to each sentence a triplet of TMS pulses was applied to one of the regions at one of six time points (400–1900 ms). Results showed a significant main effect of Time for right anterior superior temporal gyrus and right fronto-parietal operculum. The largest interference was observed half-way through the sentence. This effect was stronger for withdrawal emotions than for the approach emotion. A further experiment with the inclusion of an active control condition, TMS over the EEG site POz (midline parietal-occipital junction), revealed stronger effects at the fronto-parietal operculum and anterior superior temporal gyrus relative to the active control condition. No evidence was found for sequential processing of emotional prosodic information from right anterior superior temporal gyrus to the right fronto-parietal operculum, but the results revealed more parallel processing. Our results suggest that both right fronto-parietal operculum and right anterior superior temporal gyrus are critical for emotional prosody perception at a relatively late time period after sentence onset. This may reflect that emotional cues can still be ambiguous at the beginning of sentences, but become more apparent half-way through the sentence.

[1]  Angela D. Friederici,et al.  Sex differences in the preattentive processing of vocal emotional expressions , 2005, Neuroreport.

[2]  K. Zilles,et al.  Recognition of emotional prosody and verbal components of spoken language: an fMRI study. , 2000, Brain research. Cognitive brain research.

[3]  I. Wambacq,et al.  Non-voluntary and voluntary processing of emotional prosody: an event-related potentials study , 2004, Neuroreport.

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

[5]  R. Goebel,et al.  The Dynamics of Interhemispheric Compensatory Processes in Mental Imagery , 2005, Science.

[6]  K M Heilman,et al.  Auditory affective agnosia. Disturbed comprehension of affective speech. , 1975, Journal of neurology, neurosurgery, and psychiatry.

[7]  Michael Erb,et al.  Cerebral pathways in processing of affective prosody: A dynamic causal modeling study , 2006, NeuroImage.

[8]  Sean A. Spence,et al.  Descartes' Error: Emotion, Reason and the Human Brain , 1995 .

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

[10]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

[11]  D. Long,et al.  Transcranial Magnetic Stimulation: A Neurochronometrics of Mind , 2004 .

[12]  Jean Vroomen,et al.  Duration and intonation in emotional speech , 1993, EUROSPEECH.

[13]  Wiebo H Brouwer,et al.  Cognitive, physiological, and personality correlates of recurrence of depression. , 2005, Journal of affective disorders.

[14]  M. Erb,et al.  Effects of prosodic emotional intensity on activation of associative auditory cortex , 2006, Neuroreport.

[15]  P. Gorelick,et al.  The aprosodias: further functional-anatomical evidence for the organisation of affective language in the right hemisphere. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[16]  H. Spekreijse,et al.  FigureGround Segregation in a Recurrent Network Architecture , 2002, Journal of Cognitive Neuroscience.

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

[18]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[19]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  Michael Andres,et al.  Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals , 2004, The European journal of neuroscience.

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

[22]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[23]  Nick F. Ramsey,et al.  A stereotactic method for image-guided transcranial magnetic stimulation validated with fMRI and motor-evoked potentials , 2004, NeuroImage.

[24]  Hanna Damasio,et al.  Neural systems for recognition of emotional prosody: a 3-D lesion study. , 2002, Emotion.

[25]  Sonja A. Kotz,et al.  Early emotional prosody perception based on different speaker voices , 2008, Neuroreport.

[26]  K. Heilman,et al.  Discrimination and evocation of affectively intoned speech in patients with right parietal disease , 1977, Neurology.

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

[28]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

[29]  Guy Vingerhoets,et al.  Cerebral hemodynamics during discrimination of prosodic and semantic emotion in speech studied by transcranial doppler ultrasonography. , 2003, Neuropsychology.

[30]  S. Kotz,et al.  Beyond the right hemisphere: brain mechanisms mediating vocal emotional processing , 2006, Trends in Cognitive Sciences.

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

[32]  S. Scott,et al.  Saying it with feeling: neural responses to emotional vocalizations , 1999, Neuropsychologia.

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

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

[35]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[36]  Z. Nahas,et al.  Motor threshold in transcranial magnetic stimulation: a comparison of a neurophysiological method and a visualization of movement method. , 1998, The journal of ECT.

[37]  S. Scott,et al.  Positive Emotions Preferentially Engage an Auditory–Motor “Mirror” System , 2006, The Journal of Neuroscience.

[38]  T. Johnstone,et al.  The voice of emotion: an FMRI study of neural responses to angry and happy vocal expressions. , 2006, Social cognitive and affective neuroscience.

[39]  Anne-Lise Giraud,et al.  Distinct functional substrates along the right superior temporal sulcus for the processing of voices , 2004, NeuroImage.

[40]  A. Anderson,et al.  Perceiving emotion: There’s more than meets the eye , 2000, Current Biology.

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

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

[43]  Guy Vingerhoets,et al.  What is said or how it is said makes a difference: role of the right fronto‐parietal operculum in emotional prosody as revealed by repetitive TMS , 2005, The European journal of neuroscience.

[44]  Wolfgang Grodd,et al.  Cerebral processing of emotional prosody—influence of acoustic parameters and arousal , 2008, NeuroImage.

[45]  T. Crow,et al.  Right hemisphere language functions and schizophrenia: the forgotten hemisphere? , 2005, Brain : a journal of neurology.

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

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

[48]  Mark Hallett,et al.  Locating the Motor Cortex on the MRI with Transcranial Magnetic Stimulation and PET , 1996, NeuroImage.