Spatial Stream Segregation by Auditory Cortical Neurons

In a complex auditory scene, a “cocktail party” for example, listeners can disentangle multiple competing sequences of sounds. A recent psychophysical study in our laboratory demonstrated a robust spatial component of stream segregation showing ∼8° acuity. Here, we recorded single- and multiple-neuron responses from the primary auditory cortex of anesthetized cats while presenting interleaved sound sequences that human listeners would experience as segregated streams. Sequences of broadband sounds alternated between pairs of locations. Neurons synchronized preferentially to sounds from one or the other location, thereby segregating competing sound sequences. Neurons favoring one source location or the other tended to aggregate within the cortex, suggestive of modular organization. The spatial acuity of stream segregation was as narrow as ∼10°, markedly sharper than the broad spatial tuning for single sources that is well known in the literature. Spatial sensitivity was sharpest among neurons having high characteristic frequencies. Neural stream segregation was predicted well by a parameter-free model that incorporated single-source spatial sensitivity and a measured forward-suppression term. We found that the forward suppression was not due to post discharge adaptation in the cortex and, therefore, must have arisen in the subcortical pathway or at the level of thalamocortical synapses. A linear-classifier analysis of single-neuron responses to rhythmic stimuli like those used in our psychophysical study yielded thresholds overlapping those of human listeners. Overall, the results indicate that the ascending auditory system does the work of segregating auditory streams, bringing them to discrete modules in the cortex for selection by top-down processes.

[1]  E. C. Cherry Some Experiments on the Recognition of Speech, with One and with Two Ears , 1953 .

[2]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[3]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

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

[5]  T. Imig,et al.  Binaural columns in the primary field (A1) of cat auditory cortex , 1977, Brain Research.

[6]  J. C. Middlebrooks,et al.  Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  M. Merzenich,et al.  Role of cat primary auditory cortex for sound-localization behavior. , 1984, Journal of neurophysiology.

[8]  N A Macmillan,et al.  Detection theory analysis of group data: estimating sensitivity from average hit and false-alarm rates. , 1985, Psychological bulletin.

[9]  T. Imig,et al.  Single-unit selectivity to azimuthal direction and sound pressure level of noise bursts in cat high-frequency primary auditory cortex. , 1990, Journal of neurophysiology.

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

[11]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[12]  Douglas Johnson,et al.  Stream Segregation and Peripheral Channeling , 1991 .

[13]  D. M. Green,et al.  Characterization of external ear impulse responses using Golay codes. , 1992, The Journal of the Acoustical Society of America.

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

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

[16]  W. Ritter,et al.  An investigation of the auditory streaming effect using event-related brain potentials. , 1999, Psychophysiology.

[17]  R A Reale,et al.  Directional sensitivity of neurons in the primary auditory (AI) cortex of the cat to successive sounds ordered in time and space. , 2000, Journal of neurophysiology.

[18]  J. C. Middlebrooks,et al.  Coding of Sound-Source Location by Ensembles of Cortical Neurons , 2000, The Journal of Neuroscience.

[19]  Mitchell Steinschneider,et al.  Neural correlates of auditory stream segregation in primary auditory cortex of the awake monkey , 2001, Hearing Research.

[20]  W. Teder-Sälejärvi,et al.  Preattentive evaluation of multiple perceptual streams in human audition , 2003, Neuroreport.

[21]  Georg M Klump,et al.  Primitive auditory stream segregation: a neurophysiological study in the songbird forebrain. , 2004, Journal of neurophysiology.

[22]  C. Schreiner,et al.  Thalamocortical transformation of responses to complex auditory stimuli , 2004, Experimental Brain Research.

[23]  Stephen G Lomber,et al.  Cortical control of sound localization in the cat: unilateral cooling deactivation of 19 cerebral areas. , 2004, Journal of neurophysiology.

[24]  J. Arezzo,et al.  Auditory stream segregation in monkey auditory cortex: effects of frequency separation, presentation rate, and tone duration. , 2004, The Journal of the Acoustical Society of America.

[25]  A. Zador,et al.  Synaptic Mechanisms of Forward Suppression in Rat Auditory Cortex , 2005, Neuron.

[26]  J. Rauschecker,et al.  Perceptual Organization of Tone Sequences in the Auditory Cortex of Awake Macaques , 2005, Neuron.

[27]  J. C. Middlebrooks,et al.  Auditory Prosthesis with a Penetrating Nerve Array , 2007, Journal for the Association for Research in Otolaryngology.

[28]  J. Rauschecker,et al.  The role of auditory cortex in the formation of auditory streams , 2007, Hearing Research.

[29]  E. C. Cmm,et al.  on the Recognition of Speech, with , 2008 .

[30]  D. Pressnitzer,et al.  Perceptual Organization of Sound Begins in the Auditory Periphery , 2008, Current Biology.

[31]  Antje Ihlefeld,et al.  Disentangling the effects of spatial cues on selection and formation of auditory objects. , 2008, The Journal of the Acoustical Society of America.

[32]  Ewan A. Macpherson,et al.  Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex , 2008, Hearing Research.

[33]  John C Middlebrooks,et al.  Auditory cortex phase locking to amplitude-modulated cochlear implant pulse trains. , 2008, Journal of neurophysiology.

[34]  Lee M. Miller,et al.  Populations of auditory cortical neurons can accurately encode acoustic space across stimulus intensity , 2009, Proceedings of the National Academy of Sciences.

[35]  M. A. Bee,et al.  Neural adaptation to tone sequences in the songbird forebrain: patterns, determinants, and relation to the build-up of auditory streaming , 2010, Journal of Comparative Physiology A.

[36]  Mounya Elhilali,et al.  Competing Streams at the Cocktail Party: Exploring the Mechanisms of Attention and Temporal Integration , 2010, The Journal of Neuroscience.

[37]  Alexander Gutschalk,et al.  Activity associated with stream segregation in human auditory cortex is similar for spatial and pitch cues. , 2010, Cerebral cortex.

[38]  Andrew J. King,et al.  Cortical Representation of Auditory Space , 2011 .

[39]  John C. Middlebrooks,et al.  Auditory Cortex Spatial Sensitivity Sharpens During Task Performance , 2010, Nature Neuroscience.

[40]  Cyrus P. Billimoria,et al.  Competing Sound Sources Reveal Spatial Effects in Cortical Processing , 2012, PLoS biology.

[41]  Mitchell Steinschneider,et al.  Neural mechanisms of rhythmic masking release in monkey primary auditory cortex: implications for models of auditory scene analysis. , 2012, Journal of neurophysiology.

[42]  John C. Middlebrooks,et al.  Specialization for Sound Localization in Fields A1, DZ, and PAF of Cat Auditory Cortex , 2013, Journal of the Association for Research in Otolaryngology.

[43]  John C. Middlebrooks,et al.  Stream segregation with high spatial acuity. , 2012, The Journal of the Acoustical Society of America.

[44]  A. Gutschalk,et al.  Role of pattern, regularity, and silent intervals in auditory stream segregation based on inter-aural time differences , 2013, Experimental Brain Research.