GABA shapes a topographic organization of response latency in the mustache bat's inferior colliculus

Abstract

Many neurons in the auditory forebrain of the mustache bat act as coincidence detectors for signals separated in time by up to 20 msec. Differences in path lengths cannot adequately explain how the nervous system delays one signal relative to the other to such a large degree. Several researchers have proposed that an inhibitory mechanism might account for long delays, but it has not been known where these delays are created. Previous studies, using a variety of mammals, have reported that the inferior colliculus contains some cells with much longer latencies than those of cells in lower auditory centers, suggesting that the inferior colliculus might be the site where long delays are generated. We characterized the latencies of cells in the 60 kHz contour of the mustache bat inferior colliculus and examined how GABAergic inhibition affected the latencies of those cells. Evaluations of the influence of GABA were made by documenting changes in response latency that occurred when GABAergic inputs were reversibly blocked by iontophoretic application of the GABAA antagonist bicuculline. Prior to bicuculline application, latencies varied over a wide range among the population of cells and we observed a pattern of latency changes with dorsoventral location. The pattern was that the population of neurons in the dorsal regions of the inferior colliculus had a wide range of latencies while the population in more ventral regions had progressively narrower latency ranges. Thus, while some cells at each depth had comparably short latencies, the average latency of the population at a given depth was long in the dorsal inferior colliculus and became progressively shorter ventrally. The same characteristic distribution of latencies and pattern of latency changes with depth were observed for cells that had different aural preferences, different rate-intensity functions, and different discharge patterns, suggesting that latency is an important organizational feature of the inferior colliculus. Bicuculline substantially shortened latency in about half of the cells studied, and it dramatically altered the pattern of latency changes with depth. These results suggest that GABA normally lengthens response latencies and creates a dorsoventral grading of delays in the inferior colliculus. This wide range of latencies could provide the large latency differences necessary for the coincidence detectors in the medial geniculate body tuned to signals separated by up to 20 msec.