Representation of temporal features of complex sounds by the discharge patterns of neurons in the owl's inferior colliculus.

The spiking pattern evoked in cells of the owl's inferior colliculus by repeated presentation of the same broadband noise was found to be highly reproducible and synchronized with the temporal features of the noise stimulus. The pattern remained largely unchanged when the stimulus was presented from spatial loci that evoke similar average firing rates. To better understand this patterning, we computed the pre-event stimulus ensemble (PESE)-the average of the stimuli that preceded each spike. Computing the PESE by averaging the pressure waveforms produced a noisy, featureless trace, suggesting that the patterning was not synchronized to a particular waveform in the fine structure. By contrast, computing the PESE by averaging the stimulus envelope revealed an average envelope waveform, the "PESE envelope," typically having a peak preceded by a trough. Increasing the overall stimulus level produced PESE envelopes with higher amplitudes, suggesting a decrease in the jitter of the cell's response. The effect of carrier frequency on the PESE envelope was investigated by obtaining a cell's response to broadband noise and either estimating the PESE envelope for each spectral band or by computing a spectrogram of the stimulus prior to each spike. Either method yielded the cell's PESE spectrogram, a plot of the average amplitude of each carrier-frequency component at various pre-spike times. PESE spectrograms revealed surfaces with peaks and troughs at certain frequencies and pre-spike times. These features are collectively called the spectrotemporal receptive field (STRF). The shape of the STRF showed that in many cases, the carrier frequency can affect the PESE envelope. The modulation transfer function (MTF), which describes a cell's ability to respond to time-varying amplitudes, was estimated with sinusoidally amplitude-modulated (SAM) noises. Comparison of the PESE envelope with the MTF in the time and frequency domains showed that the two were closely matched, suggesting that a cell's response to SAM stimuli is largely predictable from its response to a noise-modulated carrier. The STRF is considered to be a model of the linear component of a system's response to dynamic stimuli. Using the STRF, we estimated the degree to which we could predict a cell's response to an arbitrary broadband noise by comparing the convolution of the STRF and the envelope of the noise with the cell's post-stimulus time histogram to the same noise. The STRF explained 18-46% of the variance of a cell's response to broadband noise.

[1]  A. Aertsen,et al.  Prediction of the responses of auditory neurons in the midbrain of the grass frog based on the spectro-temporal receptive field , 1983, Hearing Research.

[2]  R. Plomp,et al.  Effect of temporal envelope smearing on speech reception. , 1994, The Journal of the Acoustical Society of America.

[3]  A. R. Palmer,et al.  Binaural masking level difference effects in single units of the guinea pig inferior colliculus , 1991, Hearing Research.

[4]  Klaus Hartung,et al.  Head-related transfer functions of the barn owl: measurement and neural responses , 1998, Hearing Research.

[5]  L. Carney,et al.  Responses of low-frequency cells in the inferior colliculus to interaural time differences of clicks: excitatory and inhibitory components. , 1989, Journal of neurophysiology.

[6]  C H Keller,et al.  Representation of multiple sound sources in the owl's auditory space map , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  B. Delgutte,et al.  Speech coding in the auditory nerve: V. Vowels in background noise. , 1984, The Journal of the Acoustical Society of America.

[8]  G. Rose A temporal-processing mechanism for all species? , 1986, Brain, behavior and evolution.

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

[10]  N I Durlach,et al.  Intensity perception. XIII. Perceptual anchor model of context-coding. , 1984, The Journal of the Acoustical Society of America.

[11]  A. Møller,et al.  Frequency selectivity of single auditory-nerve fibers in response to broadband noise stimuli. , 1977, The Journal of the Acoustical Society of America.

[12]  B. Delgutte,et al.  Receptive fields and binaural interactions for virtual-space stimuli in the cat inferior colliculus. , 1999, Journal of neurophysiology.

[13]  P. I. M. Johannesma,et al.  Spectro-temporal characteristics of single units in the auditory midbrain of the lightly anaesthetised grass frog (Rana temporaria L.) Investigated with noise stimuli , 1981, Hearing Research.

[14]  D. M. Green,et al.  A panoramic code for sound location by cortical neurons. , 1994, Science.

[15]  A. Møller,et al.  Statistical evaluation of the dynamic properties of cochlear nucleus units using stimuli modulated with pseudorandom noise. , 1973, Brain research.

[16]  G. Klump,et al.  Temporal modulation transfer functions in the barn owl (Tyto alba) , 2002, Journal of Comparative Physiology A.

[17]  Eliot A. Brenowitz The contribution of temporal song cues to species recognition in the red-winged blackbird , 1983, Animal Behaviour.

[18]  C H Keller,et al.  Binaural Cross-Correlation Predicts the Responses of Neurons in the Owl’s Auditory Space Map under Conditions Simulating Summing Localization , 1996, The Journal of Neuroscience.

[19]  M. Konishi,et al.  Space and frequency are represented separately in auditory midbrain of the owl. , 1978, Journal of neurophysiology.

[20]  J. E. Rose,et al.  Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source. , 1966, Journal of neurophysiology.

[21]  E. Lewis,et al.  Predicting the temporal responses of non-phase-locking bullfrog auditory units to complex acoustic waveforms , 1999, Hearing Research.

[22]  T E Hanna,et al.  Discrimination of reproducible noise as a function of bandwidth and duration , 1984, Perception & psychophysics.

[23]  T T Takahashi,et al.  Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl , 1988, The Journal of comparative neurology.

[24]  Alan R. Palmer,et al.  Psychophysical and Physiological Advances in Hearing , 1998 .

[25]  Eric I. Knudsen,et al.  Representation of interaural level difference in the VLVp, the first site of binaural comparison in the barn owl's auditory system , 1994, Hearing Research.

[26]  A. Møller,et al.  Dynamic properties of the responses of single neurones in the cochlear nucleus of the rat. , 1976, The Journal of physiology.

[27]  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.

[28]  H. Wagner,et al.  Representation of interaural time difference in the central nucleus of the barn owl's inferior colliculus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  C. Köppl,et al.  Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. , 1997, Journal of neurophysiology.

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

[31]  R. Adolphs,et al.  Bilateral inhibition generates neuronal responses tuned to interaural level differences in the auditory brainstem of the barn owl , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  M. Ferragamo,et al.  Auditory nerve representation of a complex communication sound in background noise. , 1992, The Journal of the Acoustical Society of America.

[33]  R. Meddis,et al.  A computer model of amplitude-modulation sensitivity of single units in the inferior colliculus. , 1994, The Journal of the Acoustical Society of America.

[34]  James A. Mazer Integration of Parallel Processing Streams in the Inferior Colliculus of the Barn Owl , 1995 .

[35]  J. J. Eggermont,et al.  Quantitative characterisation procedure for auditory neurons based on the spectro-temporal receptive field , 1983, Hearing Research.

[36]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  A. Doupe,et al.  Temporal and Spectral Sensitivity of Complex Auditory Neurons in the Nucleus HVc of Male Zebra Finches , 1998, The Journal of Neuroscience.

[38]  B. Delgutte,et al.  Neural coding of the temporal envelope of speech : Relation to modulation transfer functions , 2001 .

[39]  P Kuyper,et al.  Triggered correlation. , 1968, IEEE transactions on bio-medical engineering.

[40]  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.

[41]  P M Narins,et al.  Noise susceptibility and immunity of phase locking in amphibian auditory-nerve fibers. , 1989, The Journal of the Acoustical Society of America.

[42]  T. Takahashi,et al.  An anatomical substrate for the inhibitory gradient in the VLVp of the owl , 1995, The Journal of comparative neurology.

[43]  T T Takahashi,et al.  Role of commissural projections in the representation of bilateral auditory space in the barn owl's inferior colliculus , 1989, The Journal of comparative neurology.

[44]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[45]  M. Konishi,et al.  Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  William Bialek,et al.  Non-phase locked auditory cells and ‘envelope’ detection , 1993 .

[47]  R. Payne Acoustic location of prey by barn owls (Tyto alba). , 1971, The Journal of experimental biology.

[48]  M. Konishi,et al.  Selectivity for interaural time difference in the owl's midbrain , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  Linda J. Lombardino,et al.  Deficits in auditory temporal and spectral resolution in language-impaired children , 1997, Nature.

[50]  Adrian Rees,et al.  Dynamic properties of the responses of single neurons in the inferior colliculus of the rat , 1986, Hearing Research.

[51]  C. D. Geisler,et al.  Wiener kernel analysis of responses from anteroventral cochlear nucleus neurons , 1984, Hearing Research.

[52]  W E Sullivan Classification of response patterns in cochlear nucleus of barn owl: correlation with functional response properties. , 1985, Journal of neurophysiology.

[53]  D A Bodnar,et al.  Midbrain combinatorial code for temporal and spectral information in concurrent acoustic signals. , 1999, Journal of neurophysiology.

[54]  S F Coble,et al.  Discriminability of bursts of reproducible noise. , 1992, The Journal of the Acoustical Society of America.