Speaking modifies voice‐evoked activity in the human auditory cortex

The voice we most often hear is our own, and proper interaction between speaking and hearing is essential for both acquisition and performance of spoken language. Disturbed audiovocal interactions have been implicated in aphasia, stuttering, and schizophrenic voice hallucinations, but paradigms for a noninvasive assessment of auditory self‐monitoring of speaking and its possible dysfunctions are rare. Using magnetoencephalograpy we show here that self‐uttered syllables transiently activate the speaker's auditory cortex around 100 ms after voice onset. These phasic responses were delayed by 11 ms in the speech‐dominant left hemisphere relative to the right, whereas during listening to a replay of the same utterances the response latencies were symmetric. Moreover, the auditory cortices did not react to rare vowel changes interspersed randomly within a series of repetitively spoken vowels, in contrast to regular change‐related responses evoked 100–200 ms after replayed rare vowels. Thus, speaking primes the human auditory cortex at a millisecond time scale, dampening and delaying reactions to self‐produced “expected” sounds, more prominently in the speech‐dominant hemisphere. Such motor‐to‐sensory priming of early auditory cortex responses during voicing constitutes one element of speech self‐monitoring that could be compromised in central speech disorders. Hum. Brain Mapping 9:183–191, 2000. © 2000 Wiley‐Liss, Inc.

[1]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[2]  Bernard S. Lee Effects of delayed speech feedback , 1950 .

[3]  A. Starr,et al.  ELECTROMYOGRAPHY OF MIDDLE EAR MUSCLES IN MAN DURING MOTOR ACTIVITIES , 1963, Acta neurologica Scandinavica.

[4]  G. E. Alexander,et al.  Convergence of prefrontal and acoustic inputs upon neurons in the superior temporal gyrus of the awake squirrel monkey , 1976, Brain Research.

[5]  J. D. Newman,et al.  Anatomical and physiological evidence for a relationship between the ‘cingular’ vocalization area and the auditory cortex in the squirrel monkey , 1980, Brain Research.

[6]  S. Blumstein,et al.  Speech production mechanisms in aphasia: A delayed auditory feedback study , 1981, Brain and Language.

[7]  C. Elberling,et al.  Auditory magnetic fields from the human cortex. Influence of stimulus intensity. , 1981, Scandinavian audiology.

[8]  P. Mu¨ller-Preuss,et al.  Inhibition of auditory cortical neurons during phonation , 1981, Brain Research.

[9]  R. Knight,et al.  Bitemporal lesions dissociate auditory evoked potentials and perception. , 1984, Electroencephalography and clinical neurophysiology.

[10]  Andrew C. Papanicolaou,et al.  Brain stem evoked response suppression during speech production , 1986, Brain and Language.

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

[12]  G. V. Simpson,et al.  Generators of middle- and long-latency auditory evoked potentials: implications from studies of patients with bitemporal lesions. , 1987, Electroencephalography and clinical neurophysiology.

[13]  H. Pick,et al.  Inhibiting the Lombard effect. , 1989, The Journal of the Acoustical Society of America.

[14]  K. Lehnertz,et al.  Neuromagnetic evidence of an amplitopic organization of the human auditory cortex. , 1989, Electroencephalography and clinical neurophysiology.

[15]  F. Richer,et al.  Intracerebral amplitude distributions of the auditory evoked potential. , 1989, Electroencephalography and clinical neurophysiology.

[16]  M. Scherg,et al.  A Source Analysis of the Late Human Auditory Evoked Potentials , 1989, Journal of Cognitive Neuroscience.

[17]  R. Hari The neuromagnetic method in the study of the human auditory cortex , 1990 .

[18]  S. Foote,et al.  Intensity-amplitude relationships in monkey event-related potentials: parallels to human augmenting-reducing responses. , 1991, Electroencephalography and clinical neurophysiology.

[19]  M Kajola,et al.  Modified activity of the human auditory cortex during auditory hallucinations. , 1992, The American journal of psychiatry.

[20]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[21]  Risto N t nen Attention and brain function , 1992 .

[22]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[23]  L. Parkkonen,et al.  122-channel squid instrument for investigating the magnetic signals from the human brain , 1993 .

[24]  R. Murray,et al.  Increased blood flow in Broca's area during auditory hallucinations in schizophrenia , 1993, The Lancet.

[25]  R Näätänen,et al.  Phonetic invariance in the human auditory cortex. , 1993, Neuroreport.

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

[27]  D Mrowinski,et al.  Intensity dependence of auditory evoked dipole source activity. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  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.

[29]  N. Kraus,et al.  Nonprimary auditory thalamic representation of acoustic change. , 1994, Journal of neurophysiology.

[30]  T. Carrell,et al.  Discrimination of speech-like contrasts in the auditory thalamus and cortex. , 1994, The Journal of the Acoustical Society of America.

[31]  E. Schröger Automatic detection of frequency change is invariant over a large intensity range. , 1994, Neuroreport.

[32]  C. Schroeder,et al.  Detection of stimulus deviance within primate primary auditory cortex: intracortical mechanisms of mismatch negativity (MMN) generation , 1994, Brain Research.

[33]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[34]  M S Hämäläinen,et al.  Effects of intensity variation on human auditory evoked magnetic fields. , 1995, Acta oto-laryngologica.

[35]  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.

[36]  D. Poeppel,et al.  Task-induced asymmetry of the auditory evoked M100 neuromagnetic field elicited by speech sounds. , 1996, Brain research. Cognitive brain research.

[37]  J. Kalinowski,et al.  Fluent Speech, Fast Articulatory Rate, and Delayed Auditory Feedback: Creating a Crisis for a Scientific Revolution? , 1996, Perceptual and motor skills.

[38]  Alan C. Evans,et al.  Modulation of cerebral blood-flow in the human auditory cortex during speech: role of motor-to-sensory discharges , 1996, NeuroImage.

[39]  R. Ingham,et al.  A PET study of the neural systems of stuttering , 1996, Nature.

[40]  C. Frith,et al.  Functional neuroanatomy of verbal self-monitoring , 1996, NeuroImage.

[41]  Hearing and the development of language and speech. , 1996, Folia phoniatrica et logopaedica : official organ of the International Association of Logopedics and Phoniatrics.

[42]  H. Fukuyama,et al.  Cortical processing mechanism for vocalization with auditory verbal feedback , 1997, Neuroreport.

[43]  Michael I. Jordan,et al.  Sensorimotor adaptation in speech production. , 1998, Science.

[44]  M. Scherg,et al.  Intracerebral Sources of Human Auditory-Evoked Potentials , 1999, Audiology and Neurotology.

[45]  Gabriel Curio,et al.  Differential effects of overt, covert and replayed speech on vowel-evoked responses of the human auditory cortex , 1999, Neuroscience Letters.

[46]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.