Primary auditory cortex of cats: feature detection or something else?

Abstract.Neurons in sensory cortices are often assumed to be “feature detectors”, computing simple and then successively more complex features out of the incoming sensory stream. These features are somehow integrated into percepts. Despite many years of research, a convincing candidate for such a feature in primary auditory cortex has not been found. We argue that feature detection is actually a secondary issue in understanding the role of primary auditory cortex. Instead, the major contribution of primary auditory cortex to auditory perception is in processing previously derived features on a number of different timescales. We hypothesize that, as a result, neurons in primary auditory cortex represent sounds in terms of auditory objects rather than in terms of feature maps. According to this hypothesis, primary auditory cortex has a pivotal role in the auditory system in that it generates the representation of auditory objects to which higher auditory centers assign properties such as spatial location, source identity, and meaning.

[1]  C J Darwin,et al.  Grouping in pitch perception: evidence for sequential constraints. , 1995, The Journal of the Acoustical Society of America.

[2]  E D Young,et al.  WHY DO CATS NEED A DORSAL COCHLEAR NUCLEUS? , 1996, Journal of basic and clinical physiology and pharmacology.

[3]  J. C. Middlebrooks,et al.  Binaural response-specific bands in primary auditory cortex (AI) of the cat: Topographical organization orthogonal to isofrequency contours , 1980, Brain Research.

[4]  Xiaoqin Wang,et al.  Temporal and rate representations of time-varying signals in the auditory cortex of awake primates , 2001, Nature Neuroscience.

[5]  R. Fay,et al.  Speech Processing in the Auditory System , 2010, Springer Handbook of Auditory Research.

[6]  M. W. Spitzer,et al.  Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity. , 1998, Journal of neurophysiology.

[7]  R K Clifton Breakdown of echo suppression in the precedence effect. , 1987, The Journal of the Acoustical Society of America.

[8]  William Bialek,et al.  Adaptive Rescaling Maximizes Information Transmission , 2000, Neuron.

[9]  A M Aertsen,et al.  Reverse-correlation methods in auditory research , 1983, Quarterly Reviews of Biophysics.

[10]  Guang-Di Chen,et al.  Responses of Chinchilla Inferior Colliculus Neurons to Amplitude-Modulated Tones with Different Envelopes , 2002, Journal of the Association for Research in Otolaryngology.

[11]  I. Nelken,et al.  Responses to linear and logarithmic frequency‐modulated sweeps in ferret primary auditory cortex , 2000, The European journal of neuroscience.

[12]  Gerald Langner,et al.  Processing of frequency-modulated stimuli in the chick auditory cortex analogue: evidence for topographic representations and possible mechanisms of rate and directional sensitivity , 1992, Journal of Comparative Physiology A.

[13]  B. Delgutte,et al.  Neural correlates of the pitch of complex tones. I. Pitch and pitch salience. , 1996, Journal of neurophysiology.

[14]  Shihab A. Shamma,et al.  Ripple Analysis in Ferret Primary Auditory Cortex. II. Topographic and Columnar Distribution of Ripple Response Parameters , 1994 .

[15]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's posterior auditory field. , 1994, Journal of neurophysiology.

[16]  C Trahiotis,et al.  Lateralization of bands of noise: effects of bandwidth and differences of interaural time and phase. , 1989, The Journal of the Acoustical Society of America.

[17]  Andrew J. King,et al.  Linear processing of spatial cues in primary auditory cortex , 2001, Nature.

[18]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's anterior auditory field. , 1994, Journal of neurophysiology.

[19]  A. de Cheveigné,et al.  The auditory system as a separation machine , 2001 .

[20]  Mounya Elhilali,et al.  The enigma of cortical responses: Slow yet precise , 2005 .

[21]  S A Shamma,et al.  Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. , 2001, Journal of neurophysiology.

[22]  Tom C. T. Yin,et al.  Neural Mechanisms of Encoding Binaural Localization Cues in the Auditory Brainstem , 2002 .

[23]  Ben M Clopton,et al.  Spectrotemporal receptive fields of neurons in cochlear nucleus of guinea pig , 1991, Hearing Research.

[24]  Liam Paninski,et al.  Convergence properties of three spike-triggered analysis techniques , 2003, NIPS.

[25]  Israel Nelken,et al.  Responses of auditory-cortex neurons to structural features of natural sounds , 1999, Nature.

[26]  Nova Scotia,et al.  Response timing constraints on the cortical representation of sound time structure , 1990 .

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

[28]  Stephen McAdams,et al.  Auditory signal processing : physiology, psychoacoustics, and models , 2005 .

[29]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. II: Organization of response properties along the ‘isofrequency’ dimension , 1992, Hearing Research.

[30]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

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

[32]  R. Frisina Subcortical neural coding mechanisms for auditory temporal processing , 2001, Hearing Research.

[33]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

[34]  L. Carney,et al.  Temporal coding of resonances by low-frequency auditory nerve fibers: single-fiber responses and a population model. , 1988, Journal of neurophysiology.

[35]  D. P. Phillips,et al.  Timing of spike discharges in cat auditory cortex neurons: Implications for encoding of stimulus periodicity , 1989, Hearing Research.

[36]  B. Delgutte,et al.  Neural correlates of the pitch of complex tones. II. Pitch shift, pitch ambiguity, phase invariance, pitch circularity, rate pitch, and the dominance region for pitch. , 1996, Journal of neurophysiology.

[37]  R. K. Clifton,et al.  Dynamic processes in the precedence effect. , 1991, The Journal of the Acoustical Society of America.

[38]  E D Young,et al.  Comparative analysis of spectro-temporal receptive fields, reverse correlation functions, and frequency tuning curves of auditory-nerve fibers. , 1994, The Journal of the Acoustical Society of America.

[39]  C. Schreiner,et al.  Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps , 2004, Experimental Brain Research.

[40]  John H. Casseday,et al.  The Inferior Colliculus: A Hub for the Central Auditory System , 2002 .

[41]  H. Tokuno,et al.  Central visual pathways in the mole () , 1989 .

[42]  M. W. Spitzer,et al.  Responses of inferior colliculus neurons to time-varying interaural phase disparity: effects of shifting the locus of virtual motion. , 1993, Journal of neurophysiology.

[43]  Brian H Scott,et al.  Context-Dependent Adaptive Coding of Interaural Phase Disparity in the Auditory Cortex of Awake Macaques , 2002, The Journal of Neuroscience.

[44]  C Trahiotis,et al.  Across-frequency interaction in lateralization of complex binaural stimuli. , 1994, The Journal of the Acoustical Society of America.

[45]  A Fishbach,et al.  Auditory edge detection: a neural model for physiological and psychoacoustical responses to amplitude transients. , 2001, Journal of neurophysiology.

[46]  Ad Aertsen,et al.  Statistical and dimensional analysis of the neural representation of the acoustic biotope of the frog , 1982, Journal of Medical Systems.

[47]  A. Aertsen,et al.  The Spectro-Temporal Receptive Field , 1981, Biological Cybernetics.

[48]  M. Merzenich,et al.  Optimizing sound features for cortical neurons. , 1998, Science.

[49]  I. Winter,et al.  The representation of steady-state vowel sounds in the temporal discharge patterns of the guinea pig cochlear nerve and primarylike cochlear nucleus neurons. , 1986, The Journal of the Acoustical Society of America.

[50]  Peter Heil,et al.  A unifying basis of auditory thresholds based on temporal summation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[51]  A. Aertsen,et al.  A comparison of the Spectro-Temporal sensitivity of auditory neurons to tonal and natural stimuli , 1981, Biological Cybernetics.

[52]  S. Shamma Speech processing in the auditory system. I: The representation of speech sounds in the responses of the auditory nerve. , 1985, The Journal of the Acoustical Society of America.

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

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

[55]  A. Aertsen,et al.  Spectro-temporal receptive fields of auditory neurons in the grassfrog , 1980, Biological Cybernetics.

[56]  R. B. Gardner,et al.  Vowel quality changes produced by surrounding tone sequences , 1989, Perception & Psychophysics.

[57]  A. Grinvald,et al.  Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[58]  P. Heil,et al.  Auditory cortical onset responses revisited. II. Response strength. , 1997, Journal of neurophysiology.

[59]  R. Patterson,et al.  The temporal representation of the delay of iterated rippled noise in the ventral cochlear nucleus of the guinea‐pig , 2001, The Journal of physiology.

[60]  T N Buell,et al.  Restarting the adapted binaural system. , 1990, The Journal of the Acoustical Society of America.

[61]  M. Cynader,et al.  Sensitivity of cat primary auditory cortex (Al) neurons to the direction and rate of frequency modulation , 1985, Brain Research.

[62]  Christoph E Schreiner,et al.  Functional architecture of auditory cortex , 2002, Current Opinion in Neurobiology.

[63]  Kunio Murakami,et al.  Intracellular characterization of suppressive responses in supragranular pyramidal neurons of cat primary auditory cortex in vivo. , 2002, Cerebral cortex.

[64]  Steven Greenberg,et al.  Physiology of the Cochlear Nuclei , 1992 .

[65]  I. Nelken,et al.  Responses of Neurons in Cat Primary Auditory Cortex to Bird Chirps: Effects of Temporal and Spectral Context , 2002, The Journal of Neuroscience.

[66]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I: Effects of variation of stimulus parameters , 1992, Hearing Research.

[67]  Lee M. Miller,et al.  Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. , 2002, Journal of neurophysiology.

[68]  Philip H Smith,et al.  Temporal and Binaural Properties in Dorsal Cochlear Nucleus and Its Output Tract , 1998, The Journal of Neuroscience.

[69]  J. Eggermont Representation of a voice onset time continuum in primary auditory cortex of the cat. , 1995, The Journal of the Acoustical Society of America.

[70]  M. Sachs,et al.  Effects of nonlinearities on speech encoding in the auditory nerve. , 1979, The Journal of the Acoustical Society of America.

[71]  Li I. Zhang,et al.  Topography and synaptic shaping of direction selectivity in primary auditory cortex , 2003, Nature.

[72]  L. Paninski Convergence Properties of Some Spike-Triggered Analysis Techniques , 2002 .

[73]  Jonathan Z. Simon,et al.  Robust Spectrotemporal Reverse Correlation for the Auditory System: Optimizing Stimulus Design , 2000, Journal of Computational Neuroscience.

[74]  K. Sen,et al.  Spectral-temporal Receptive Fields of Nonlinear Auditory Neurons Obtained Using Natural Sounds , 2022 .

[75]  E D Young,et al.  Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus. II. Predicting responses with the use of nonlinear models. , 1997, Journal of neurophysiology.

[76]  Christopher J. Plack,et al.  Temporal integration in pitch perception, in Physiological and Psychophysical Bases of Auditory Function , 2001 .

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

[78]  Christoph E Schreiner,et al.  Spectrotemporal structure of receptive fields in areas AI and AAF of mouse auditory cortex. , 2003, Journal of neurophysiology.

[79]  Alon Fishbach,et al.  Neural model for physiological responses to frequency and amplitude transitions uncovers topographical order in the auditory cortex. , 2003, Journal of neurophysiology.

[80]  P. Heil,et al.  Auditory cortical onset responses revisited. I. First-spike timing. , 1997, Journal of neurophysiology.

[81]  N. C. Singh,et al.  Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli , 2001 .