Specialization of left auditory cortex for speech perception in man depends on temporal coding.

Speech perception requires cortical mechanisms capable of analysing and encoding successive spectral (frequency) changes in the acoustic signal. To study temporal speech processing in the human auditory cortex, we recorded intracerebral evoked potentials to syllables in right and left human auditory cortices including Heschl's gyrus (HG), planum temporale (PT) and the posterior part of superior temporal gyrus (area 22). Natural voiced /ba/, /da/, /ga/) and voiceless (/pa/, /ta/, /ka/) syllables, spoken by a native French speaker, were used to study the processing of a specific temporally based acoustico-phonetic feature, the voice onset time (VOT). This acoustic feature is present in nearly all languages, and it is the VOT that provides the basis for the perceptual distinction between voiced and voiceless consonants. The present results show a lateralized processing of acoustic elements of syllables. First, processing of voiced and voiceless syllables is distinct in the left, but not in the right HG and PT. Second, only the evoked potentials in the left HG, and to a lesser extent in PT, reflect a sequential processing of the different components of the syllables. Third, we show that this acoustic temporal processing is not limited to speech sounds but applies also to non-verbal sounds mimicking the temporal structure of the syllable. Fourth, there was no difference between responses to voiced and voiceless syllables in either left or right areas 22. Our data suggest that a single mechanism in the auditory cortex, involved in general (not only speech-specific) temporal processing, may underlie the further processing of verbal (and non-verbal) stimuli. This coding, bilaterally localized in auditory cortex in animals, takes place specifically in the left HG in man. A defect of this mechanism could account for hearing discrimination impairments associated with language disorders.

[1]  A. Liberman,et al.  The role of selected stimulus-variables in the perception of the unvoiced stop consonants. , 1952, The American journal of psychology.

[2]  R. Efron TEMPORAL PERCEPTION, APHASIA AND D'EJ'A VU. , 1963, Brain : a journal of neurology.

[3]  L. Lisker,et al.  A Cross-Language Study of Voicing in Initial Stops: Acoustical Measurements , 1964 .

[4]  H. Lane,et al.  THE MOTOR THEORY OF SPEECH PERCEPTION: A CRITICAL REVIEW. , 1965, Psychological review.

[5]  G. E. Chatrian,et al.  La stéréo-électroencéphalographie dans l'épilepsie. Informations neurophysiopathologiques apportées par l'investigation fonctionnelle stéréotaxique , 1967 .

[6]  P. Tallal,et al.  Defects of Non-Verbal Auditory Perception in Children with Developmental Aphasia , 1973, Nature.

[7]  D. Pisoni,et al.  Reaction times to comparisons within and across phonetic categories , 1974, Perception & psychophysics.

[8]  Sheila Blumstein,et al.  Effects of unilateral brain damage on the processing of speech sounds , 1975, Brain and Language.

[9]  P. Mermelstein,et al.  Speech sounds and features , 1975, Proceedings of the IEEE.

[10]  G. Celesia Organization of auditory cortical areas in man. , 1976, Brain : a journal of neurology.

[11]  S. Blumstein,et al.  Perceptual invariance and onset spectra for stop consonants in different vowel environments , 1976 .

[12]  Eleanor M. Saffran,et al.  An analysis of speech perception in word deafness , 1976, Brain and Language.

[13]  Harold Goodglass,et al.  Phonological factors in auditory comprehension in aphasia , 1977, Neuropsychologia.

[14]  L. Vignolo,et al.  Phonemic Identification Defect in Aphasia , 1977, Cortex.

[15]  J L Miller,et al.  Nonindependence of feature processing in initial consonants. , 1977, Journal of speech and hearing research.

[16]  A. Ades,et al.  Vowels, Consonants, Speech, and Nonspeech. , 1977 .

[17]  Richard E. Pastore,et al.  Common-Factor Model of Categorical Perception. , 1977 .

[18]  Carlo Caltagirone,et al.  Discrimination of voice versus place contrasts in aphasia , 1978, Brain and Language.

[19]  Paula Tallal,et al.  Impairment of auditory perception and language comprehension in dysphasia , 1978, Brain and Language.

[20]  D. Molfese,et al.  Left and right hemisphere involvement in speech perception: Electrophysiological correlates , 1978, Perception & psychophysics.

[21]  D. Moody,et al.  Neural lateralization of species-specific vocalizations by Japanese macaques (Macaca fuscata). , 1978, Science.

[22]  S. Blumstein,et al.  Acoustic invariance in speech production: evidence from measurements of the spectral characteristics of stop consonants. , 1979, The Journal of the Acoustical Society of America.

[23]  R. Efron,et al.  Spectral versus temporal features in dichotic listening , 1979, Brain and Language.

[24]  A. Galaburda,et al.  Cytoarchitectonic organization of the human auditory cortex , 1980, The Journal of comparative neurology.

[25]  S. Blumstein,et al.  Perceptual invariance and onset spectra for stop consonants in different vowel environments. , 1980, The Journal of the Acoustical Society of America.

[26]  K. Stevens Acoustic correlates of some phonetic categories. , 1979, The Journal of the Acoustical Society of America.

[27]  Prof. Dr. Heiko Braak,et al.  Architectonics of the Human Telencephalic Cortex , 1980, Studies of Brain Function.

[28]  P. Tallal,et al.  Rate of acoustic change may underlie hemispheric specialization for speech perception , 1980, Science.

[29]  Mitchell Steinschneider,et al.  Phase-locked cortical responses to a human speech sound and low-frequency tones in the monkey , 1980, Brain Research.

[30]  S. Makeig,et al.  A 40-Hz auditory potential recorded from the human scalp. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[31]  H. Seldon Structure of human auditory cortex. I. Cytoarchitectonics and dendritic distributions , 1981, Brain Research.

[32]  Kenneth N. Stevens,et al.  Constraints Imposed by the Auditory System on the Properties Used to Classify Speech Sounds: Data from Phonology, Acoustics, and Psychoacoustics , 1981 .

[33]  Mitchell Steinschneider,et al.  Speech evoked activity in the auditory radiations and cortex of the awake monkey , 1982, Brain Research.

[34]  Gabriele Miceli,et al.  The processing of speech sounds in a patient with cortical auditory disorder , 1982, Neuropsychologia.

[35]  M. Alexander,et al.  Pure word deafness. Analysis of a case with bilateral lesions and a defect at the prephonemic level. , 1982, Brain : a journal of neurology.

[36]  Julia Dwyer,et al.  The role of duration and rapid temporal processing on the lateral perception of consonants and vowels , 1982, Brain and Language.

[37]  T. V. Stockert On the structure of word deafness and mechanisms underlying the fluctuation of disturbances of higher cortical functions , 1982, Brain and Language.

[38]  P. Kuhl,et al.  Enhanced discriminability at the phonetic boundaries for the place feature in macaques. , 1983, The Journal of the Acoustical Society of America.

[39]  M. Leek,et al.  Lateralization of rapid auditory sequences , 1983, Neuropsychologia.

[40]  Zvi Wollberg,et al.  Responses of cells in the auditory cortex of awake squirrel monkeys to normal and reversed species-specific vocalizations , 1983, Hearing Research.

[41]  William C. Stebbins,et al.  Neural lateralization of vocalizations by Japanese macaques: communicative significance is more important than acoustic structure. , 1984, Behavioral neuroscience.

[42]  B. Delgutte,et al.  Speech coding in the auditory nerve: I. Vowel-like sounds. , 1984, The Journal of the Acoustical Society of America.

[43]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF) , 1986, Hearing Research.

[44]  Voice onset time perception in Japanese aphasic patients , 1986, Brain and Language.

[45]  R Hari,et al.  Evidence for cortical origin of the 40 Hz auditory evoked response in man. , 1987, Electroencephalography and clinical neurophysiology.

[46]  B C Moore,et al.  The shape of the ear's temporal window. , 1988, The Journal of the Acoustical Society of America.

[47]  M. Mendez,et al.  Cortical auditory disorders: clinical and psychoacoustic features. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[48]  B. Yaqub,et al.  Pure word deafness (acquired verbal auditory agnosia) in an Arabic speaking patient. , 1988, Brain : a journal of neurology.

[49]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields , 1988, Hearing Research.

[50]  D B Moody,et al.  Categorical perception of conspecific communication sounds by Japanese macaques, Macaca fuscata. , 1989, The Journal of the Acoustical Society of America.

[51]  K Zilles,et al.  Cerebral asymmetry: MR planimetry of the human planum temporale. , 1989, Journal of computer assisted tomography.

[52]  H. Damasio,et al.  Auditory perception of temporal and spectral events in patients with focal left and right cerebral lesions , 1990, Brain and Language.

[53]  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 .

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

[55]  Joanne L. Miller,et al.  Speech Perception , 1990, Springer Handbook of Auditory Research.

[56]  M. Sachs,et al.  The representations of the steady-state vowel sound /e/ in the discharge patterns of cat anteroventral cochlear nucleus neurons. , 1990, Journal of neurophysiology.

[57]  Jos J. Eggermont,et al.  Rate and synchronization measures of periodicity coding in cat primary auditory cortex , 1991, Hearing Research.

[58]  P. Chauvel,et al.  Localization of the primary auditory area in man. , 1991, Brain : a journal of neurology.

[59]  N. Viemeister,et al.  Temporal integration and multiple looks. , 1991, The Journal of the Acoustical Society of America.

[60]  G. V. Simpson,et al.  Cellular generators of the cortical auditory evoked potential initial component. , 1992, Electroencephalography and clinical neurophysiology.

[61]  J Bancaud,et al.  Clinical semiology of frontal lobe seizures. , 1992, Advances in neurology.

[62]  D. P. Phillips Neural Representation of Stimulus Times in the Primary Auditory Cortex a , 1993, Annals of the New York Academy of Sciences.

[63]  A. Galaburda,et al.  Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. , 1993, Cerebral cortex.

[64]  D. P. Phillips,et al.  Representation of acoustic events in the primary auditory cortex. , 1993, Journal of experimental psychology. Human perception and performance.

[65]  P Tallal,et al.  Functional lateralization for auditory temporal processing in male and female rats. , 1993, Behavioral neuroscience.

[66]  C. Schroeder,et al.  Speech-evoked activity in primary auditory cortex: effects of voice onset time. , 1994, Electroencephalography and clinical neurophysiology.

[67]  Douglas W. Jones,et al.  Gender differences in the normal lateralization of the supratemporal cortex: MRI surface-rendering morphometry of Heschl's gyrus and the planum temporale. , 1994, Cerebral cortex.

[68]  J M Badier,et al.  Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components. , 1994, Electroencephalography and clinical neurophysiology.

[69]  S. Dehaene,et al.  Speed and cerebral correlates of syllable discrimination in infants , 1994, Nature.

[70]  J J Eggermont,et al.  Neural interaction in cat primary auditory cortex II. Effects of sound stimulation. , 1994, Journal of neurophysiology.

[71]  C. Schroeder,et al.  Physiologic Correlates of the Voice Onset Time Boundary in Primary Auditory Cortex (A1) of the Awake Monkey: Temporal Response Patterns , 1995, Brain and Language.

[72]  Steven L. Miller,et al.  Temporal Processing Deficits of Language-Learning Impaired Children Ameliorated by Training , 1996, Science.

[73]  T. Carrell,et al.  Acoustic elements of speechlike stimuli are reflected in surface recorded responses over the guinea pig temporal lobe. , 1996, The Journal of the Acoustical Society of America.

[74]  R. Christopher deCharms,et al.  Primary cortical representation of sounds by the coordination of action-potential timing , 1996, Nature.

[75]  Steven L. Miller,et al.  Language Comprehension in Language-Learning Impaired Children Improved with Acoustically Modified Speech , 1996, Science.

[76]  Alvin M. Liberman,et al.  Speech: A Special Code , 1996 .

[77]  Alan C. Evans,et al.  Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. , 1996, Cerebral cortex.

[78]  Shihab A. Shamma,et al.  Auditory cortex , 1998 .

[79]  Denis Schwartz Localisation des generateurs intra-cerebraux de l'activite meg et eeg : evaluation de la precision spatiale et temporelle (doctorat genie biologique et medical) , 1998 .

[80]  S. H. Auerbach Pure word deafness. Analysis of a case with bilateral lesions and a defect at the prephonemic level , 1999 .