Journal of Computational Neuroscience 13, 71–91, 2002 c  2002 Kluwer Academic Publishers. Manufactured in The Netherlands. A Unified Mechanism for Spontaneous-Rate and First-Spike Timing in the Auditory Nerve B. SURESH KRISHNA Center for Neural Science, New York University, New York, NY 10003, USA suresh@cns.nyu.edu Received September 27, 2001; Revised April 4, 2002; Accepted May 10, 2002 Action Editor: Shihab Shamma Abstract. Recent physiological experiments have provided detailed descriptions of the properties of first-spike latency and variability in auditory cortex and nerve in response to pure tones with different envelopes. The envelope- dependence of first-spike timing and precision in auditory cortical neurons appears to reflect properties established in the nerve. First-spike latency properties in individual auditory nerve fibers are strongly correlated with their spontaneous rate (SR). It is shown here that a minimal, plausible model of auditory transduction with two free parameters accurately reproduces the physiological data from the auditory nerve population. The model consists of a simple gain stage, a bandpass filter, a rectifying saturating non-linearity, and a lowpass filter in series. The output of the lowpass filter drives an inhomogeneous Poisson process. The shape of the non-linearity is determined by SR; in physiological terms, this shape depends upon the resting sensitivity of the synapse between the inner hair cell and the auditory nerve. An alternative model for SR generation, where SR is added to the stimulus-driven output of a fixed nonlinearity, fails to account for the data. The results provide a novel, comprehensive and physiologically-based explanation for the range of experimental results on the envelope-dependence of first-spike latency and precision, and its relationship with SR, in the auditory system. Keywords: spike timing, auditory nerve, spontaneous-rate, auditory cortex, latency Introduction First-spike latency (henceforth referred to simply as “latency”) has been explored as a neural code in many sensory systems (e.g. audition: Brugge et al., 1996; Eggermont, 1998a; Furukawa et al., 2000; vision: Gawne et al., 1996; Reich et al., 2001; olfaction: Hopfield, 1995; somatosensation: Panzeri et al., 2001). Bilateral latency differences are implicated in sound localization (Joris et al., 1998; Mason et al., 2001) and the Pulfrich effect (Anzai et al., 2001). Transient spike- timing assumes special importance in audition because ecological warning sounds are often brief; thus tran- sient, rapidly-transmitted, and precisely-timed spike responses may be essential for warning detection and localization. In general, latency decreases as stimulus intensity increases (e.g. audition: Heil and Irvine, 1997; Klug et al., 2000; vision: Maunsell et al., 1999; Warzecha and Egelhaaf, 2000; somatosensation: Mountcastle et al., 1957). In audition, the relationship between latency and sound pressure level (SPL) for pure tones has been stud- ied in detail in many brain regions (e.g. Heil and Irvine, 1996; Klug et al., 2000). Since latency decreases with intensity, intensity differences between the two ears also create latency differences between the two ears. This has led to the suggestion that binaural intensity dif- ferences can be detected by a comparator mechanism that detects timing differences between the two ears. In principle, this comparator could be similar or iden- tical to the interaural timing comparator that underlies azimuthal sound localization of low-frequency tones.