Footprints of inhibition in the response of cortical delay-tuned neurons of bats

Abstract

Responses of echo-delay-tuned neurons that encode target distance were investigated in the dorsal auditory cortex of anesthetized short-tailed fruit bats ( Carollia perspicillata). This species echolocates using short downward frequency-modulated (FM) biosonar signals. In response to FM sweeps of increasing level, 60 out of 131 studied neurons (47%) displayed a “paradoxical latency shift,” i.e., longer response latency to loud sounds and shorter latency to faint sounds. In addition, a disproportionately large number of neurons (80%) displayed nonmonotonic responses, i.e., weaker responses to loud sounds and stronger responses to faint sounds. We speculate that the observed paradoxical latency shift and nonmonotonic responses are extracellular footprints of inhibitory processes evoked by loud sounds and that they could represent a specialization for the processing of the emitted loud biosonar pulse. Supporting this idea is the fact that all studied neurons displayed strong response suppression when an artificial loud pulse and a faint echo were presented together at a nonoptimal delay. In 24 neurons, iontophoresis of bicuculline (an antagonist of A-type γ-aminobutyric acid receptors) did not remove inhibitory footprints but did increase the overall spike output, and in some cases it also modified the response bandwidth and shifted the neuron's “best delay.” We suggest that inhibition could play a dual role in shaping delay tuning in different auditory stations. Below the cortex it participates in delay-tuning implementation and leaves a footprint that is measurable in cortical responses, while in the cortex it provides a substrate for an in situ control of neuronal selectivity.