Frequency dependence of synchronization of cochlear nerve fibers in the alligator lizard: evidence for a cochlear origin of timing and non-timing neural pathways.

The dependence of synchronization of spike discharges on tone frequency was measured in cochlear nerve fibers of anesthetized alligator lizards at 21 degrees C. Synchronization measures were based on the fundamental component of a Fourier analysis of the instantaneous discharge rate in response to tone bursts. Measurements were obtained from fibers innervating hair cells in both the region of the cochlea that contains a tectorial membrane (tectorial fibers) and the region where hair-cell stereocilia are free-standing in scala media (free-standing fibers). Both rate and synchronization tuning-curves were measured automatically as a function of tone frequency. For tectorial fibers, the shapes of synchronization tuning-curves are roughly similar to the shapes of rate tuning-curves: the characteristic frequencies (CF's) of both curves are approximately equal. For free-standing fibers, the shape of synchronization tuning-curves differ markedly from those of rate tuning-curves. The CF's of synchronization and rate tuning-curves differ - the ranges are 0.2-0.6 kHz and 1-4 kHz, respectively - and the two CF's are uncorrelated. Synchronization filter-functions, which are contours of synchronization index at constant average discharge rate, were measured as a function of tone frequency for both tectorial and free-standing fibers. These synchronization filter-functions have the shapes of lowpass filters. For the populations of tectorial fibers and of free-standing fibers taken separately, these functions are independent of CF. The corner frequency of these functions is 0.50 +/- 0.038 kHz for tectorial fibers and 0.37 +/- 0.037 kHz for free-standing fibers. We conclude that these populations are characterized by different synchronization filters. For free-standing fibers, synchronization filter-functions measured at average driven discharge rates of about 20 and 40 spikes/s do not differ appreciably, and the high-frequency slope is -80 to -115 dB/decade. The results show that tectorial fibers encode timing information for low-level stimuli, whereas free-standing fibers do not. It is proposed that in the alligator lizard, neural pathways that encode timing information originate in the tectorial region and those that encode non-timing information originate in the free-standing region.