Auditory cortical onset responses revisited. I. First-spike timing

Abstract

Sound onsets are salient and behaviorally relevant, and most auditory neurons discharge spikes locked to such transients. The acoustic parameters of sound onsets that shape such onset responses are unknown. In this paper is analyzed the timing of spikes of single neurons in the primary auditory cortex of barbiturate-anesthetized cats to the onsets of tone bursts. By parametric variation of sound pressure level, rise time, and rise function (linear or cosine-squared), the time courses of peak pressure, rate of change of peak pressure, and acceleration of peak pressure during the tones' onsets were systematically varied. For cosine-squared rise function tones of a given frequency and laterality, any neuron's mean first spike latency was an invariant and inverse function of the maximum acceleration of peak pressure occurring at tone onset. For linear rise function tones, latency was an invariant and inverse function of the rate of change of peak pressure. Thus latency is independent of rise time or sound pressure level per se. Latency- acceleration functions, obtained with cosine-squared rise function tones under different stimulus conditions (frequency, laterality) from any given neuron and across the neuronal pool, were of strikingly similar shape. The same was true for latency rate of change of peak pressure functions obtained with linear rise function tones. Latency-acceleration/rate of change of peak pressure functions could differ in their extent and in their position within the coordinate system. The positional differences reflect neuronal differences in minimum latency L(min) and in a sensitivity S to acceleration and rate of change of peak pressure (transient sensitivity), a hitherto unrecognized neuronal property that is distinctly different from firing threshold. Estimates of L(min) and S, which were derived by fitting a simple function to the neuronal latency-acceleration/rate of change of peak pressure functions, were independent of rise function. On average, L(min), decreased with increasing characteristic frequency (CF), but varied widely for neurons with the same CF. S varied with CF in a fashion similar to the cat's audiogram and, for a given neuron, varied with frequency. SD of first-spike latency was roughly proportional to the slope of the functions relating latency to acceleration/rate of change of peak pressure. Thus SD increased exponentially, rather than linearly, with mean latency, and did so at about twice the rate for linear than for cosine-squared rise function tones. The proportionality coefficients were quite similar across the neuronal pool and similar for both rise functions. Minimum SD increased nonlinearly with increasing L(min). These findings suggest a peripheral origin of S and a peripheral establishment of latency-acceleration/rate of change of peak pressure functions. Because of the striking similarity in the shapes of such functions across the neuronal pool, sound onsets will produce orderly and predictable spatiotemporal patterns of first-spike timing, which could be used to instantaneously track rapid transients and to represent transient features by partly scale-invariant temporal codes.