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

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.