Temporal coherence sensitivity in auditory cortex.

Natural sounds often contain energy over a broad spectral range and consequently overlap in frequency when they occur simultaneously; however, such sounds under normal circumstances can be distinguished perceptually (e.g., the cocktail party effect). Sound components arising from different sources have distinct (i.e., incoherent) modulations, and incoherence appears to be one important cue used by the auditory system to segregate sounds into separately perceived acoustic objects. Here we show that, in the primary auditory cortex of awake marmoset monkeys, many neurons responsive to amplitude- or frequency-modulated tones at a particular carrier frequency [the characteristic frequency (CF)] also demonstrate sensitivity to the relative modulation phase between two otherwise identically modulated tones: one at CF and one at a different carrier frequency. Changes in relative modulation phase reflect alterations in temporal coherence between the two tones, and the most common neuronal response was found to be a maximum of suppression for the coherent condition. Coherence sensitivity was generally found in a narrow frequency range in the inhibitory portions of the frequency response areas (FRA), indicating that only some off-CF neuronal inputs into these cortical neurons interact with on-CF inputs on the same time scales. Over the population of neurons studied, carrier frequencies showing coherence sensitivity were found to coincide with the carrier frequencies of inhibition, implying that inhibitory inputs create the effect. The lack of strong coherence-induced facilitation also supports this interpretation. Coherence sensitivity was found to be greatest for modulation frequencies of 16-128 Hz, which is higher than the phase-locking capability of most cortical neurons, implying that subcortical neurons could play a role in the phenomenon. Collectively, these results reveal that auditory cortical neurons receive some off-CF inputs temporally matched and some temporally unmatched to the on-CF input(s) and respond in a fashion that could be utilized by the auditory system to segregate natural sounds containing similar spectral components (such as vocalizations from multiple conspecifics) based on stimulus coherence.

[1]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[2]  I. Nelken,et al.  Population responses to multifrequency sounds in the cat auditory cortex: Four-tone complexes , 1994, Hearing Research.

[3]  X Chen,et al.  Dynamic frequency change among stimulus components: effects of coherence on detectability. , 1992, The Journal of the Acoustical Society of America.

[4]  P. Marler,et al.  Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. , 1980, Science.

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

[6]  M. Merzenich,et al.  Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. , 1973, Journal of neurophysiology.

[7]  D. P. Phillips,et al.  Level-dependent representation of stimulus frequency in cat primary auditory cortex , 2004, Experimental Brain Research.

[8]  Xiaoqin Wang,et al.  Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. , 2002, Journal of neurophysiology.

[9]  R. Carlyon Detecting coherent and incoherent frequency modulation , 2000, Hearing Research.

[10]  B C Moore,et al.  Modulation discrimination interference and auditory grouping. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[11]  J H Grose,et al.  Some factors affecting the magnitude of comodulation masking release. , 1990, The Journal of the Acoustical Society of America.

[12]  C. Schreiner,et al.  Organization of inhibitory frequency receptive fields in cat primary auditory cortex. , 1999, Journal of neurophysiology.

[13]  Three Experiments Concerned with Pitch Perception , 1963 .

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

[15]  C. Darwin,et al.  Spectral integration based on common amplitude modulation , 1985, Perception & psychophysics.

[16]  P. M. Hamilton Noise Masked Thresholds as a Function of Tonal Duration and Masking Noise Band Width , 1955 .

[17]  D. D. Greenwood Critical Bandwidth and the Frequency Coordinates of the Basilar Membrane , 1961 .

[18]  Gerald Langner,et al.  Periodicity coding in the auditory system , 1992, Hearing Research.

[19]  D A Fantini,et al.  Within- versus cross-channel mechanisms in detection of envelope phase disparity. , 1989, The Journal of the Acoustical Society of America.

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

[21]  R P Carlyon Further evidence against an across-frequency mechanism specific to the detection of frequency modulation (FM) incoherence between resolved frequency components. , 1994, The Journal of the Acoustical Society of America.

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

[23]  S. Shamma,et al.  Analysis of dynamic spectra in ferret primary auditory cortex. II. Prediction of unit responses to arbitrary dynamic spectra. , 1996, Journal of neurophysiology.

[24]  D P Phillips,et al.  Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. , 1981, Journal of neurophysiology.

[25]  A. Bregman,et al.  The perceptual segregation of simultaneous auditory signals: Pulse train segregation and vowel segregation , 1989, Perception & psychophysics.

[26]  J. Goldberg,et al.  Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. , 1968, Journal of neurophysiology.

[27]  L. Rosenblum Primate Behavior: Developments in Field and Laboratory Research , 1970 .

[28]  S. S. Stevens,et al.  Critical Band Width in Loudness Summation , 1957 .

[29]  B E Pfingst,et al.  Characteristics of neurons in auditory cortex of monkeys performing a simple auditory task. , 1981, Journal of neurophysiology.

[30]  Paul J. Abbas,et al.  A chronic microelectrode investigation of the tonotopic organization of human auditory cortex , 1996, Brain Research.

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

[32]  R B Gardner,et al.  Grouping of vowel harmonics by frequency modulation: Absence of effects on phonemic categorization , 1986, Perception & psychophysics.

[33]  P. Coleman,et al.  Experiments in hearing , 1961 .

[34]  J. Kaas,et al.  Auditory cortex in the grey squirrel: Tonotopic organization and architectonic fields , 1976, The Journal of comparative neurology.

[35]  N Suga,et al.  Functional properties of auditory neurones in the cortex of echo‐locating bats. , 1965, The Journal of physiology.

[36]  M. Goldstein,et al.  Intracellular study of the cat's primary auditory cortex. , 1972, Brain research.

[37]  S. Shamma,et al.  Ripple Analysis in Ferret Primary Auditory Cortex. I. Response Characteristics of Single Units to Sinusoidally Rippled Spectra , 1994 .

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

[39]  M M Merzenich,et al.  Cochleotopic organization of primary auditory cortex in the cat. , 1973, Brain research.

[40]  A S Bregman,et al.  The perceptual segregation of simultaneous vowels with harmonic, shifted, or random components , 1993, Perception & psychophysics.

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

[42]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

[43]  Leslie G. Ungerleider,et al.  Contextual Modulation in Primary Visual Cortex of Macaques , 2001, The Journal of Neuroscience.

[44]  Joseph W. Hall,et al.  Detection in noise by spectro-temporal pattern analysis. , 1984, The Journal of the Acoustical Society of America.

[45]  Robert P. Carlyon,et al.  Detecting single‐cycle frequency modulation imposed on sinusoidal, harmonic, and inharmonic carriers , 1989 .

[46]  G. Epple,et al.  Comparative studies on vocalization in marmoset monkeys (Hapalidae). , 1968, Folia primatologica; international journal of primatology.

[47]  E. G. Jones,et al.  Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys , 1997, The Journal of comparative neurology.

[48]  C. M. Marin,et al.  Segregation of concurrent sounds. II: Effects of spectral envelope tracing, frequency modulation coherence, and frequency modulation width. , 1991, The Journal of the Acoustical Society of America.

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

[50]  J. Ostwald,et al.  Temporal Coding of Amplitude and Frequency Modulation in the Rat Auditory Cortex , 1995, The European journal of neuroscience.

[51]  S. McAdams Segregation of concurrent sounds. I: Effects of frequency modulation coherence. , 1989, The Journal of the Acoustical Society of America.

[52]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

[53]  G Westheimer,et al.  Dynamics of spatial summation in primary visual cortex of alert monkeys. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Q Summerfield,et al.  The role of frequency modulation in the perceptual segregation of concurrent vowels. , 1995, The Journal of the Acoustical Society of America.

[55]  K. Koffka Principles Of Gestalt Psychology , 1936 .

[56]  R. Carlyon,et al.  Discriminating between coherent and incoherent frequency modulation of complex tones. , 1991, The Journal of the Acoustical Society of America.

[57]  I. Ohzawa,et al.  Asymmetric Suppression Outside the Classical Receptive Field of the Visual Cortex , 1999, The Journal of Neuroscience.

[58]  R. Carlyon,et al.  The psychophysics of concurrent sound segregation. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[59]  M. Merzenich,et al.  Frequency representation in auditory cortex of the common marmoset (Callithrix jacchus jacchus) , 1986, The Journal of comparative neurology.

[60]  D P Phillips,et al.  Effect of tone-pulse rise time on rate-level functions of cat auditory cortex neurons: excitatory and inhibitory processes shaping responses to tone onset. , 1988, Journal of neurophysiology.

[61]  J H Grose,et al.  Detection of frequency modulation (FM) in the presence of a second FM tone. , 1990, The Journal of the Acoustical Society of America.

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

[63]  B C Moore,et al.  Co-modulation masking release: spectro-temporal pattern analysis in hearing. , 1990, British journal of audiology.

[64]  P. Bonding Critical bandwidth in loudness summation in sensorineural hearing loss. , 1979, British journal of audiology.

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

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

[67]  J. E. Rose,et al.  The relations of thalamic connections, cellular structure and evocable electrical activity in the auditory region of the cat , 1949, The Journal of comparative neurology.

[68]  G. Epple The Behavior of Marmoset Monkeys (Callithricidae) , 1975 .

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

[70]  W A Yost,et al.  Across-critical-band processing of amplitude-modulated tones. , 1989, The Journal of the Acoustical Society of America.

[71]  B C Moore,et al.  Across-channel processes in frequency modulation detection. , 1996, The Journal of the Acoustical Society of America.

[72]  G. Békésy,et al.  Experiments in Hearing , 1963 .

[73]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[74]  W A Yost,et al.  Modulation interference in detection and discrimination of amplitude modulation. , 1989, The Journal of the Acoustical Society of America.

[75]  N Suga,et al.  Analysis of frequency‐modulated sounds by auditory neurones of echo‐locating bats. , 1965, The Journal of physiology.

[76]  A S Bregman,et al.  Fusion of simultaneous tonal glides: The role of parallelness and simple frequency relations , 1984, Perception & psychophysics.

[77]  Kourosh Saberi,et al.  A common neural code for frequency- and amplitude-modulated sounds , 1995, Nature.

[78]  H. Jones,et al.  Context-dependent interactions and visual processing in V1 , 1996, Journal of Physiology-Paris.

[79]  Gregory H. Wakefield,et al.  Discrimination of envelope phase disparity , 1987 .

[80]  Eberhard Zwicker,et al.  Direct Comparisons between the Sensations Produced by Frequency Modulation and Amplitude Modulation , 1962 .