Right-Hemisphere Auditory Cortex Is Dominant for Coding Syllable Patterns in Speech

Cortical analysis of speech has long been considered the domain of left-hemisphere auditory areas. A recent hypothesis poses that cortical processing of acoustic signals, including speech, is mediated bilaterally based on the component rates inherent to the speech signal. In support of this hypothesis, previous studies have shown that slow temporal features (3–5 Hz) in nonspeech acoustic signals lateralize to right-hemisphere auditory areas, whereas rapid temporal features (20–50 Hz) lateralize to the left hemisphere. These results were obtained using nonspeech stimuli, and it is not known whether right-hemisphere auditory cortex is dominant for coding the slow temporal features in speech known as the speech envelope. Here we show strong right-hemisphere dominance for coding the speech envelope, which represents syllable patterns and is critical for normal speech perception. Right-hemisphere auditory cortex was 100% more accurate in following contours of the speech envelope and had a 33% larger response magnitude while following the envelope compared with the left hemisphere. Asymmetries were evident regardless of the ear of stimulation despite dominance of contralateral connections in ascending auditory pathways. Results provide evidence that the right hemisphere plays a specific and important role in speech processing and support the hypothesis that acoustic processing of speech involves the decomposition of the signal into constituent temporal features by rate-specialized neurons in right- and left-hemisphere auditory cortex.

[1]  H. Gleason An introduction to descriptive linguistics , 1961 .

[2]  C. Wernicke Der aphasische Symptomenkomplex , 1974 .

[3]  P. Ladefoged A course in phonetics , 1975 .

[4]  D S Beasley,et al.  Intelligibility of time-compressed sentential stimuli. , 1980, Journal of speech and hearing research.

[5]  M. Scherg,et al.  Evoked dipole source potentials of the human auditory cortex. , 1986, Electroencephalography and clinical neurophysiology.

[6]  D. P. Phillips,et al.  Acquired word deafness, and the temporal grain of sound representation in the primary auditory cortex , 1990, Behavioural Brain Research.

[7]  S. Rosen Temporal information in speech: acoustic, auditory and linguistic aspects. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  P. Tallal,et al.  Neurobiological Basis of Speech: A Case for the Preeminence of Temporal Processing , 1993, Annals of the New York Academy of Sciences.

[9]  R. Plomp,et al.  Effect of temporal envelope smearing on speech reception. , 1994, The Journal of the Acoustical Society of America.

[10]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[11]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[12]  T. Carrell,et al.  Auditory Neurophysiologic Responses and Discrimination Deficits in Children with Learning Problems , 1996, Science.

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

[14]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[15]  P. Chauvel,et al.  Specialization of left auditory cortex for speech perception in man depends on temporal coding. , 1999, Cerebral cortex.

[16]  D B Koch,et al.  Acoustic-phonetic approach toward understanding neural processes and speech perception. , 1999, Journal of the American Academy of Audiology.

[17]  M. Dorman,et al.  Neurophysiologic correlates of cross-language phonetic perception. , 2000, The Journal of the Acoustical Society of America.

[18]  Takayuki Arai,et al.  The effect of polarity inversion of speech on human perception and data hiding as an application , 2000, 2000 IEEE International Conference on Acoustics, Speech, and Signal Processing. Proceedings (Cat. No.00CH37100).

[19]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[20]  Jos J Eggermont,et al.  Neuronal responses in cat primary auditory cortex to natural and altered species-specific calls , 2000, Hearing Research.

[21]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[23]  Nina Kraus,et al.  Aging Affects Hemispheric Asymmetry in the Neural Representation of Speech Sounds , 2000, The Journal of Neuroscience.

[24]  R. Zatorre,et al.  Spectral and temporal processing in human auditory cortex. , 2001, Cerebral cortex.

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

[26]  E Ahissar,et al.  Speech comprehension is correlated with temporal response patterns recorded from auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  C. Schreiner,et al.  Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. , 2002, Journal of neurophysiology.

[28]  R. Zatorre,et al.  Structure and function of auditory cortex: music and speech , 2002, Trends in Cognitive Sciences.

[29]  J. Eggermont,et al.  Maturation of human central auditory system activity: separating auditory evoked potentials by dipole source modeling , 2002, Clinical Neurophysiology.

[30]  David Poeppel,et al.  The analysis of speech in different temporal integration windows: cerebral lateralization as 'asymmetric sampling in time' , 2003, Speech Commun..

[31]  J. Eggermont,et al.  Maturation of human central auditory system activity: the T-complex , 2003, Clinical Neurophysiology.

[32]  P. Matthews,et al.  Defining a left-lateralized response specific to intelligible speech using fMRI. , 2003, Cerebral cortex.

[33]  Joseph S Gati,et al.  Overlapping neural regions for processing rapid temporal cues in speech and nonspeech signals☆ , 2003, NeuroImage.

[34]  T Wüstenberg,et al.  Evidence for rapid auditory perception as the foundation of speech processing: a sparse temporal sampling fMRI study , 2004, The European journal of neuroscience.

[35]  Krista L. Johnson,et al.  Learning impaired children exhibit timing deficits and training-related improvements in auditory cortical responses to speech in noise , 2004, Experimental Brain Research.

[36]  J. C. Krause,et al.  Acoustic properties of naturally produced clear speech at normal speaking rates. , 1996, The Journal of the Acoustical Society of America.

[37]  Nina Kraus,et al.  Correlation between brainstem and cortical auditory processes in normal and language-impaired children. , 2004, Brain : a journal of neurology.

[38]  A. Boemio,et al.  Hierarchical and asymmetric temporal sensitivity in human auditory cortices , 2005, Nature Neuroscience.

[39]  Martin Meyer,et al.  Spectro-temporal processing during speech perception involves left posterior auditory cortex , 2005, Neuroreport.

[40]  N. Kraus,et al.  Brainstem Timing: Implications for Cortical Processing and Literacy , 2005, The Journal of Neuroscience.

[41]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[42]  J. Jerger Clear speech. , 2005, Journal of the American Academy of Audiology.

[43]  David A. Medler,et al.  Cerebral Cortex doi:10.1093/cercor/bhi040 Cerebral Cortex Advance Access published February 9, 2005 , 2022 .

[44]  M. Schönwiesner,et al.  Hemispheric asymmetry for spectral and temporal processing in the human antero‐lateral auditory belt cortex , 2005, The European journal of neuroscience.

[45]  Nina Kraus,et al.  Auditory Brainstem Timing Predicts Cerebral Asymmetry for Speech , 2006, The Journal of Neuroscience.

[46]  J. Rauschecker,et al.  Multiple stages of auditory speech perception reflected in event-related FMRI. , 2007, Cerebral cortex.

[47]  J. Eggermont,et al.  Spatial representation of neural responses to natural and altered conspecific vocalizations in cat auditory cortex. , 2007, Journal of neurophysiology.

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

[49]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.