Neural correlates of the pitch of complex tones. I. Pitch and pitch salience.

1. The temporal discharge patterns of auditory nerve fibers in Dial-anesthetized cats were studied in response to periodic complex acoustic waveforms that evoke pitches at their fundamental frequencies. Single-formant vowels, amplitude-modulated (AM) and quasi-frequency-modulated tones. AM noise, click trains, and other complex tones were utilized. Distributions of intervals between successive spikes ("1st-order intervals") and between both successive and nonsuccessive spikes ("all-order intervals") were computed from spike trains. Intervals from many fibers were pooled to estimate interspike interval distributions for the entire auditory nerve. Properties of these "pooled interspike interval distributions," such as the positions of interval peaks and their relative heights, were examined for correspondence to the psychophysical data on pitch frequency and pitch salience. 2. For a diverse set of complex stimuli and levels, the most frequent all-order interspike interval present in the pooled distribution corresponded to the pitch heard in psychophysical experiments. Pitch estimates based on pooled interval distributions (30-85 fibers, 100 stimulus presentations per fiber) were highly accurate (within 1%) for harmonic stimuli that produce strong pitches at 60 dB SPL. 3. Although the most frequent intervals in pooled all-order interval distributions were very stable with respect to sound intensity level (40, 60, and 80 dB total SPL), this was not necessarily the case for first-order interval distributions. Because the low pitches of complex tones are largely invariant with respect to level, pitches estimated from all-order interval distributions correspond better to perception. 4. Spectrally diverse stimuli that evoke similar low pitches produce pooled interval distributions with similar most-frequent intervals. This suggests that the pitch equivalence of these different stimuli could result from central auditory processing mechanisms that analyze interspike interval patterns. 5. Complex stimuli that evoke strong or "salient" pitches produce pooled interval distributions with high peak-to-mean ratios. Those stimuli that evoke weak pitches produce pooled interval distributions with low peak-to-mean ratios. 6. Pooled interspike interval distributions for stimuli consisting of low-frequency components generally resembled the short-time auto-correlation function of stimulus waveforms. Pooled interval distributions for stimuli consisting of high-frequency components resembled the short-time autocorrelation function of the waveform envelope. 7. Interval distributions in populations of neurons constitute a general, distributed means of encoding, transmitting, and representing information. Existence of a central processor capable of analyzing these interval patterns could provide a unified explanation for many different aspects of pitch perception.

[1]  E. F. Evans,et al.  Pitch and Cochlear Nerve Fibre Temporal Discharge Patterns , 1938 .

[2]  E. Boring.  Sensation and Perception. (Scientific Books: Sensation and Perception in the History of Experimental Psychology) , 1943 .

[3]  E. Boring.  Sensation and Perception. (Scientific Books: Sensation and Perception in the History of Experimental Psychology) , 1943 .

[4]  G. A. Miller,et al.  The Perception of Repeated Bursts of Noise , 1948 .

[5]  Walter A. Rosenblith,et al.  Theory of Hearing , 1950 .

[6]  J. Licklider.  “Periodicity” Pitch and “Place” Pitch , 1954 .

[7]  R. Ritsma.  Existence Region of the Tonal Residue. I , 1962 .

[8]  R W RODIECK,et al.  Some quantitative methods for the study of spontaneous activity of single neurons. , 1962, Biophysical journal.

[9]  Georg v. Békésy,et al.  Hearing Theories and Complex Sounds , 1963 .

[10]  I. Whitfield.  Discharge Patterns of Single Fibers in the Cat's Auditory Nerve , 1966 .

[11]  R. Plomp.  Pitch of complex tones. , 1966, The Journal of the Acoustical Society of America.

[12]  R. W. Rodieck.  Maintained activity of cat retinal ganglion cells. , 1967, Journal of neurophysiology.

[13]  A. M. Mimpen,et al.  The ear as a frequency analyzer. II. , 1964, The Journal of the Acoustical Society of America.

[14]  F. Bilsen,et al.  Some parameters influencing the perceptibility of pitch. , 1970, The Journal of the Acoustical Society of America.

[15]  J. Lettvin,et al.  Multiple meaning in single visual units. , 1970, Brain, behavior and evolution.

[16]  W. M. Siebert,et al.  Frequency discrimination in the auditory system: Place or periodicity mechanisms? , 1970 .

[17]  A R Moller,et al.  The use of correlation analysis in processing neuroelectric data. , 1970, Progress in brain research.

[18]  R A Levine,et al.  Auditory-nerve activity in cats with normal and abnormal cochleas. In: Sensorineural hearing loss. , 1970, Ciba Foundation symposium.

[19]  R. Fay.  Perception of Amplitude‐Modulated Auditory Signals by the Goldfish , 1972 .

[20]  Edwin C. Moxon,et al.  Physiological Considerations in Artificial Stimulation of the Inner Ear , 1972, The Annals of otology, rhinology, and laryngology.

[21]  F. Wightman.  The pattern-transformation model of pitch. , 1973, The Journal of the Acoustical Society of America.

[22]  J. L. Goldstein.  An optimum processor theory for the central formation of the pitch of complex tones. , 1973, The Journal of the Acoustical Society of America.

[23]  F. Wightman.  Pitch and stimulus fine structure. , 1973, The Journal of the Acoustical Society of America.

[24]  E. Terhardt.  Pitch, consonance, and harmony. , 1974, The Journal of the Acoustical Society of America.

[25]  Reinier Plomp,et al.  Aspects of tone sensation , 1976 .

[26]  I. Whitfield,et al.  Perception of the missing fundamental by cats. , 1976, The Journal of the Acoustical Society of America.

[27]  E. de Boer,et al.  On the “Residue” and Auditory Pitch Perception , 1976 .

[28]  Terrance Raymond Bourk,et al.  Electrical responses of neural units in the anteroventral cochlear nucleus of the cat , 1976 .

[29]  E. Owens,et al.  An Introduction to the Psychology of Hearing , 1997 .

[30]  B. Moore.  An Introduction to the Psychology of Hearing , 1977 .

[31]  J R Pierce,et al.  Uncertainty concerning the direct use of time information in hearing: place clues in white-spectra stimuli. , 1977, The Journal of the Acoustical Society of America.

[32]  J. L. Goldstein,et al.  Evidence for a general template in central optimal processing for pitch of complex tones. , 1978, The Journal of the Acoustical Society of America.

[33]  E. Evans.  Place and time coding of frequency in the peripheral auditory system: some physiological pros and cons. , 1978, Audiology : official organ of the International Society of Audiology.

[34]  W. Yost.  Strength of the pitches associated with ripple noise. , 1978, The Journal of the Acoustical Society of America.

[35]  R. Patterson,et al.  Amplitude-modulated noise: the detection of modulation versus the detection of modulation rate. , 1978, The Journal of the Acoustical Society of America.

[36]  Ernst Terhardt,et al.  Calculating virtual pitch , 1979, Hearing Research.

[37]  M. Sachs,et al.  Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers. , 1979, The Journal of the Acoustical Society of America.

[38]  W. Yost,et al.  Models of the pitch and pitch strength of ripple noise , 1979 .

[39]  Gerhard Stoll,et al.  Scaling of pitch strength , 1979, Hearing Research.

[40]  D K Eddington,et al.  Fundamental considerations in designing auditory implants. , 1979, Acta oto-laryngologica.

[41]  E. Javel.  Coding of AM tones in the chinchilla auditory nerve: implications for the pitch of complex tones. , 1980, The Journal of the Acoustical Society of America.

[42]  Jerzy E. Rose,et al.  Neural Correlates of Some Psychoacoustic Experiences , 1980 .

[43]  B. Delgutte.  Representation of speech-like sounds in the discharge patterns of auditory-nerve fibers. , 1979, The Journal of the Acoustical Society of America.

[44]  Pitch of amplitude-modulated low-pass noise and predictions by temporal and spectral theories. , 1980, The Journal of the Acoustical Society of America.

[45]  C. Daniel Geisler,et al.  Auditory-nerve fiber responses to frequency-modulated tones , 1981, Hearing Research.

[46]  E. M. Burns,et al.  Played-again SAM: Further observations on the pitch of amplitude-modulated noise , 1981 .

[47]  E. Terhardt,et al.  Pitch of complex signals according to virtual‐pitch theory: Tests, examples, and predictions , 1982 .

[48]  M. Liberman.  The cochlear frequency map for the cat: labeling auditory-nerve fibers of known characteristic frequency. , 1982, The Journal of the Acoustical Society of America.

[49]  E. Terhardt,et al.  Algorithm for extraction of pitch and pitch salience from complex tonal signals , 1982 .

[50]  L. F. Willems,et al.  Measurement of pitch in speech: an implementation of Goldstein's theory of pitch perception. , 1982, The Journal of the Acoustical Society of America.

[51]  M. B. Sachs,et al.  Representation of whispered vowels in discharge patterns of auditory-nerve fibers , 1982, Hearing Research.

[52]  Lawrence L. Feth,et al.  Pitch of Sinusoids and Complex Tones Above 10 kHz , 1983 .

[53]  J. L. Goldstein,et al.  A central spectrum model: a synthesis of auditory-nerve timing and place cues in monaural communication of frequency spectrum. , 1983, The Journal of the Acoustical Society of America.

[54]  William A. Yost,et al.  Psychophysics and neurophysiology of repetition noise processing in a vertebrate auditory system , 1983, Hearing Research.

[55]  B. Delgutte,et al.  Speech coding in the auditory nerve: I. Vowel-like sounds. , 1984, The Journal of the Acoustical Society of America.

[56]  Murray B. Sachs,et al.  Representation of voice pitch in discharge patterns of auditory-nerve fibers , 1984, Hearing Research.

[57]  A. de Cheveigne.  A pitch perception model , 1986, ICASSP '86. IEEE International Conference on Acoustics, Speech, and Signal Processing.

[58]  Steven Greenberg,et al.  Possible Role of Low and Medium Spontaneous Rate Cochlear Nerve Fibers in the Encoding of Waveform Periodicity , 1986 .

[59]  J. W. Horst,et al.  Coding of spectral fine structure in the auditory nerve. I. Fourier analysis of period and interspike interval histograms. , 1986, The Journal of the Acoustical Society of America.

[60]  E. Evans.  Cochlear Nerve Fibre Temporal Discharge Patterns, Cochlear Frequency Selectivity and the Dominant Region for Pitch , 1986 .

[61]  C. D. Geisler,et al.  Responses of auditory-nerve fibers to multiple-tone complexes. , 1987, The Journal of the Acoustical Society of America.

[62]  D. Schwarz,et al.  Perception of the missing fundamental in nonhuman primates. , 1988, The Journal of the Acoustical Society of America.

[63]  J. H. ten Kate,et al.  Synchrony-dependent autocorrelation in eighth-nerve-fiber response to rippled noise. , 1988, The Journal of the Acoustical Society of America.

[64]  J Lazzaro,et al.  Silicon modeling of pitch perception. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[65]  J. Smurzyński,et al.  Pitch identification and discrimination for complex tones with many harmonics , 1990 .

[66]  D. O. Kim,et al.  Responses of DCN-PVCN neurons and auditory nerve fibers in unanesthetized decerebrate cats to AM and pure tones: Analysis with autocorrelation/power-spectrum , 1990, Hearing Research.

[67]  Pitch perception in silicon , 1990, Nature.

[68]  Hugo Fastl,et al.  Psychoacoustics: Facts and Models , 1990 .

[69]  D. D. Greenwood.  A cochlear frequency-position function for several species--29 years later. , 1990, The Journal of the Acoustical Society of America.

[70]  R. Meddis,et al.  Virtual pitch and phase sensitivity of a computer model of the auditory periphery. II: Phase sensitivity , 1991 .

[71]  A S Feng,et al.  Coding of temporal parameters of complex sounds by frog auditory nerve fibers. , 1991, Journal of neurophysiology.

[72]  Ray Meddis,et al.  Virtual pitch and phase sensitivity of a computer model of the auditory periphery , 1991 .

[73]  A. R. Palmer,et al.  Segregation of the Responses to Paired Vowels in the Auditory Nerve of the Guinea-Pig Using Autocorrelation , 1992 .

[74]  Coding of Fundamental Frequency in Auditory Nerve Fibers: Effects of Signal Level and Phase Spectrum. , 1992 .

[75]  Peter Cariani,et al.  Coding of the Pitch of Harmonic and Inharmonic Complex Tones in the Interspike Intervals of Auditory-Nerve Fibers. , 1992 .

[76]  Dik J. Hermes,et al.  Pitch analysis , 1993 .

[77]  Richard F. Lyon,et al.  On the importance of time—a temporal representation of sound , 1993 .

[78]  Peter Cariani,et al.  Transient changes in neural discharge patterns may enhance the separation of concurrent vowels with different fundamental frequencies , 1994 .

[79]  Remo Guidieri.  Res , 1995, RES: Anthropology and Aesthetics.

[80]  R. Patterson,et al.  Time-domain modeling of peripheral auditory processing: a modular architecture and a software platform. , 1995, The Journal of the Acoustical Society of America.

[81]  S Grossberg,et al.  A spectral network model of pitch perception. , 1995, The Journal of the Acoustical Society of America.

[82]  Ternary Structures.  ON REPRESENTATION OF , 1995 .

[83]  W A Yost,et al.  A time domain description for the pitch strength of iterated rippled noise. , 1996, The Journal of the Acoustical Society of America.

[84]  Shihab Shamma,et al.  Auditory Representations of Timbre and Pitch , 1996 .