Neural correlates of auditory stream segregation in primary auditory cortex of the awake monkey

An important feature of auditory scene analysis is the perceptual organization of sequential sound components, or 'auditory stream segregation'. Auditory stream segregation can be demonstrated by presenting a sequence of high and low frequency tones in an alternating pattern, ABAB. When the tone presentation rate (PR) is slow or the frequency separation (DeltaF) between the tones is small (<10%), a connected alternating sequence ABAB is perceived. When the PR is fast or the DeltaF is large, however, the alternating sequence perceptually splits into two parallel auditory streams, one composed of interrupted 'A' tones, and the other of interrupted 'B' tones. The neurophysiological basis of this perceptual phenomenon is unknown. Neural correlates of auditory stream segregation were examined in A1 of the awake monkey using neuronal ensemble techniques (multiunit activity and current source density). Responses evoked by alternating frequency sequences of tones, ABAB, were studied as a function of PR (5, 10, 20 and 40 Hz). 'A' tones corresponded to the best frequency (BF) of the cortical site, while 'B' tones were situated away from the BF by an amount DeltaF. At slow PRs, 'A' and 'B' tones evoked responses that generated an overall pattern of activity at the stimulus PR. In contrast, at fast PRs, 'B' tone responses were differentially suppressed, resulting in a pattern of activity consisting predominantly of 'A' tone responses at half the PR. The magnitude of 'B' tone response suppression increased with DeltaF. Differential suppression of BF and non-BF tone responses at high PRs can be explained by physiological principles of forward masking. The effect of DeltaF is explained by the hypothesis that responses to tones distant from the BF are more susceptible to suppression by BF tones than responses to tones near the BF. These results parallel human psychoacoustics of auditory stream segregation and suggest a cortical basis for the perceptual phenomenon.

[1]  George Gourevitch.  Detectability of Tones in Quiet and in Noise by Rats and Monkeys , 1970 .

[2]  W. Yost.  Auditory image perception and analysis: The basis for hearing , 1991, Hearing Research.

[3]  Phillips Dp.  Central auditory processing: a view from auditory neuroscience. , 1995, The American journal of otology.

[4]  R. Eckhorn,et al.  Stimulus-dependent modulations of correlated high-frequency oscillations in cat visual cortex. , 1997, Cerebral cortex.

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

[6]  L. V. Noorden.  Temporal coherence in the perception of tone sequences , 1975 .

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

[8]  M Steinschneider,et al.  Complex tone processing in primary auditory cortex of the awake monkey. I. Neural ensemble correlates of roughness. , 2000, The Journal of the Acoustical Society of America.

[9]  B. Moore.  Psychophysical tuning curves measured in simultaneous and forward masking. , 1978, The Journal of the Acoustical Society of America.

[10]  Stuart Anstis,et al.  Adaptation to auditory streaming of frequency-modulated tones. , 1985 .

[11]  J. Rauschecker.  Cortical processing of complex sounds , 1998, Current Opinion in Neurobiology.

[12]  J. Nerbonne,et al.  Three kinetically distinct Ca2+-independent depolarization-activated K+ currents in callosal-projecting rat visual cortical neurons. , 1997, Journal of neurophysiology.

[13]  S. H. Hulse,et al.  Auditory scene analysis by European starlings (Sturnus vulgaris): perceptual segregation of tone sequences. , 1998, The Journal of the Acoustical Society of America.

[14]  R. Metherate,et al.  Facilitation of an NMDA receptor‐mediated EPSP by paired‐pulse stimulation in rat neocortex via depression of GABAergic IPSPs. , 1994, The Journal of physiology.

[15]  Carolyn Drake,et al.  Perceptual attenuation of nonfocused auditory streams , 1997, Perception & psychophysics.

[16]  H. Scheich,et al.  Processing of sound sequences in macaque auditory cortex: response enhancement. , 1999, Journal of neurophysiology.

[17]  W. Jesteadt,et al.  Forward masking as a function of frequency, masker level, and signal delay. , 1982, The Journal of the Acoustical Society of America.

[18]  P. Schwindt,et al.  Two transient potassium currents in layer V pyramidal neurones from cat sensorimotor cortex. , 1991, The Journal of physiology.

[19]  J. Kaas,et al.  Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[20]  J. Lisman.  Bursts as a unit of neural information: making unreliable synapses reliable , 1997, Trends in Neurosciences.

[21]  R. Meddis,et al.  A Computer Model of Auditory Stream Segregation , 1991, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[22]  Michael B. Calford,et al.  Monaural inhibition in cat auditory cortex. , 1995, Journal of neurophysiology.

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

[24]  David B. Moody.  Detection and discrimination of amplitude-modulated signals by macaque monkeys. , 1994, The Journal of the Acoustical Society of America.

[25]  C. Gross,et al.  The Effects of Superior Temporal Cortex Lesions on the Processing and Retention of Auditory Information in Monkeys (Cebus apella) , 1996, The Journal of Neuroscience.

[26]  M. Goldstein,et al.  Cortical coding of repetitive acoustic pulses. , 1972, Brain research.

[27]  A S Bregman,et al.  Allocating attention to frequency regions , 1994, Perception & psychophysics.

[28]  Norman M. Weinberger,et al.  Synaptic potentials and effects of amino acid antagonists in the auditory cortex , 1992, Brain Research Bulletin.

[29]  D. Woods,et al.  Signal clustering modulates auditory cortical activity in humans , 1994, Perception & psychophysics.

[30]  Lawrence Weiskrantz,et al.  Auditory sequence discrimanation in macaca mulatta: The role of the superior temporal cortex , 1976, Neuropsychologia.

[31]  J. Kaas,et al.  Subdivisions of AuditoryCortex and Levels of Processing in Primates , 1998, Audiology and Neurotology.

[32]  C. Nicholson,et al.  Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. , 1975, Journal of neurophysiology.

[33]  M. Beauvois.  The effect of tone duration on auditory stream formation , 1998, Perception & psychophysics.

[34]  I. Nelken,et al.  Population responses to multifrequency sounds in the cat auditory cortex: One- and two-parameter families of sounds , 1994, Hearing Research.

[35]  C. Schreiner,et al.  Time course of forward masking tuning curves in cat primary auditory cortex. , 1997, Journal of neurophysiology.

[36]  Timothy D. Griffiths,et al.  Spatial and temporal auditory processing deficits following right hemisphere infarction , 1997 .

[37]  A. Bregman,et al.  Primary auditory stream segregation and perception of order in rapid sequences of tones. , 1971, Journal of experimental psychology.

[38]  D P Phillips,et al.  Effects of bilateral auditory cortical lesions on gap-detection thresholds in the ferret (Mustela putorius). , 1996, Behavioral neuroscience.

[39]  Ray Meddis,et al.  Computer simulation of auditory stream segregation in alternating‐tone sequences , 1993 .

[40]  H. Vaughan,et al.  A new multielectrode array for the simultaneous recording of field potentials and unit activity. , 1981, Electroencephalography and clinical neurophysiology.

[41]  Richard R Fay,et al.  Auditory stream segregation in goldfish (Carassius auratus) , 1998, Hearing Research.

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

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

[44]  R Hari,et al.  Auditory stream segregation in dyslexic adults. , 1999, Brain : a journal of neurology.

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

[46]  Albert S. Bregman,et al.  The Auditory Scene. (Book Reviews: Auditory Scene Analysis. The Perceptual Organization of Sound.) , 1990 .

[47]  I. Peretz,et al.  Contribution of different cortical areas in the temporal lobes to music processing. , 1998, Brain : a journal of neurology.

[48]  S. Buus,et al.  Effective attenuation of signals in noise under focused attention. , 1991, The Journal of the Acoustical Society of America.

[49]  Timothy D. Griffiths,et al.  Spatial and temporal auditory processing deficits following right hemisphere infarction. A psychophysical study. , 1997 .

[50]  G. A. Miller,et al.  The Trill Threshold , 1950 .

[51]  Michael J. Denham,et al.  A Model of Auditory Streaming , 1995, NIPS.

[52]  M Steinschneider,et al.  Click train encoding in primary auditory cortex of the awake monkey: evidence for two mechanisms subserving pitch perception. , 1998, The Journal of the Acoustical Society of America.

[53]  Mitchell Steinschneider,et al.  Intracranial generators of event-related potentials in the monkey , 1986 .

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

[55]  Shihab A. Shamma,et al.  Patterns of inhibition in auditory cortical cells in awake squirrel monkeys , 1985, Hearing Research.

[56]  J. L. Hollett,et al.  Repetition rate and signal level effects on neuronal responses to brief tone pulses in cat auditory cortex. , 1989, The Journal of the Acoustical Society of America.

[57]  C. Nicholson,et al.  Experimental optimization of current source-density technique for anuran cerebellum. , 1975, Journal of neurophysiology.