Unusual discharge patterns of single fibers in the pigeon's auditory nerve.

Abstract

Extracellular recording from single auditory nerve fibers in the pigeon, Columba livia, revealed some unusual discharge patterns of spontaneous and evoked activity. Time interval histograms (TIHs) of spontaneous activity showed a random interval distribution in 73% of the auditory fibers (Fig. 1a). The remaining 27% revealed periodicity in the TIHs (Fig. 1b-e), determined by the characteristic frequency (CF) of a given fiber. Normally, those fibers had a CF less than 2.2 kHz. In both cases spontaneous activity was irregular. The time pattern of quasiperiodic spontaneous firing in different auditory fibers is described by three main types of autocorrelation histograms (ACHs; decaying, nondecaying, and modulated), reflecting the spontaneous oscillations of the hair cell membrane potential (Fig. 1b-d). Single-tone suppression in auditory fibers with quasi-periodic spontaneous activity was found (Figs. 2, 10) and it could be observed if the eighth nerve was cut. There was no suppressive effect in fibres with random spontaneous firing. The frequency selectivity properties of auditory fibers were studied by means of an automatic method. Both 'simple' (Fig. 4) and 'complex' (Figs. 7, 8) response maps were found. Apart from the usual excitatory area, complex response maps were characterized by suppressive areas lying either above (Fig. 7), below (Fig. 8e), or on both sides of the CF (Fig. 8a-c). Generally, complex response maps were observed for fibers showing quasiperiodic spontaneous activity (Figs. 7, 8). Input-output functions at frequencies evoking single-tone suppression were nonmonotonic, while they were always monotonic at frequencies near the CF (Fig. 12). No difference in sharpness was observed between normal frequency threshold curves (FTCs) and excitatory areas of 'complex' response maps (Fig. 9). 'On-off' responses evoked by suppressive stimuli were found (Figs. 2, 3). They had a periodic pattern determined by the CF and did not depend on the stimulus frequency (Fig. 3). Low-CF fibers were observed which changed their time discharge structure to tone levels about 45 dB lower than their thresholds at the CF (Fig. 6). The observed features of the discharge patterns of the pigeon's auditory fibers reflect the distinctive nature of the fundamental mechanisms of auditory analysis in birds that are connected with electrical tuning of the hair cells and probably with the micromechanics of the bird's cochlea.