Inhibition sensitive to interaural time difference in the barn owl's inferior colliculus

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Abstract

In spontaneously active neurons in the external nucleus of the inferior colliculus of the barn owl, a stimulus-driven discharge was followed by a quiescent period lasting tens of milliseconds before the spontaneous activity resumed. The more favorable the interaural time difference, the longer the quiet period. The duration of the quiescent period also depended on stimulus frequency. Frequencies different from the neuron's best frequency induced shorter quiescent periods, although they could elicit similar rates of impulses. Also, the duration of the quiescent period was independent of interaural intensity difference. Thus, the quiet period is not due to an after-hyperpolarization but was an inhibitory effect that depended on the activity of other neurons. In some neurons, discharge continued after the stimulus without a quiescent period and gradually decayed over a period of 50–100 ms past the stimulus offset. The similarity between the quiescent period of the neurons mentioned above and the time course of the poststimulus discharge in these neurons suggests that these neurons serve as inhibitory interneurons.

Introduction

Inhibition plays an important role in the processing of auditory spatial information in the inferior colliculus. In bats, lateral inhibition sharpens neuronal selectivity for frequency (Yang et al., 1992), provides variable hyperpolarization that underlies selectivity to sound duration (Casseday et al., 1994) and long echo delays (Park and Pollak, 1993; Saitoh and Suga, 1995), and creates sensitivity to interaural intensity differences by combining contralateral excitation and ipsilateral inhibition (Park and Pollak, 1994). In the cat, the rabbit and the owl it was suggested that inhibition suppresses response to echoes and thus underlies the precedence effect (Carney and Yin, 1989; Yin, 1994; Fitzpatrick et al., 1995; Keller and Takahashi, 1996). In barn owls inhibition is thought to be involved in the computation of interaural time and intensity differences (Fujita and Konishi, 1991; Adolphs, 1993), and GABAergic neurons and terminals abound in the barn owl's inferior colliculus (Carr et al., 1989). Fujita and Konishi (1991)observed that application of the GABAA antagonist bicuculline resulted in an increase in the neuron's response to favorable interaural time differences (ITDs) and did not affect its response to unfavorable ones. This experiment suggested that inhibition is involved in the suppression of phase ambiguity. Inhibition is also implicated in the genesis of neurons sensitive to the direction of sound movement in the owl's external nucleus of the inferior colliculus (ICx) (Wagner and Takahashi, 1992). Despite all these findings, inhibitory neurons that respond to sound have not been documented. This report presents evidence for the existence of ITD-specific inhibition and a possible candidate for the neuron type that mediates it.

Section snippets

Animal preparations

Four adult barn owls were used. Prior to surgery and each physiological recording session, owls were anesthetized with ketamine-HCl (25 mg/kg/h) and diazepam (1 mg/kg/h). Initial surgical operations included a scalp incision, craniotomy and the attachment of a head-holding plate. The craniotomy in the exoccipital bone provided direct access through a sinus to the bony pocket encasing the optic lobe in which the inferior colliculus is found. A small hole in this bone allowed the passage of

The nature of the poststimulus quiescent period

Fourteen of 55 ICx neurons were spontaneously active. Most of the spontaneously active neurons (10 out of 14) ceased to fire completely for tens of milliseconds after the evoked response. This phenomenon is clearly observed on the background of a typical spontaneous firing rate of 10–40 spikes/s. Raster diagrams of neuronal activities show that the resumption of poststimulus discharge varies as a function of the stimulus ITD (Fig. 1A,C). The most favorable ITD, i.e., the one that evoked the

The evidence for ITD-dependent inhibition

The dependence of the poststimulus quiescence on ITD is a result of inhibition, and not a result of an after-hyperpolarization that occurs after every firing burst. This must be so because variations in the discharge rate created by stimulation with unfavorable frequencies or IIDs were not correlated with either the magnitude or duration of silence. This inhibition is, therefore, not general but specific to ITD and frequency. Inhibitory inputs that satisfy these conditions may come from the

Acknowledgements

I thank Jamie Mazer for making his software available to me. Susan Volman provided a very useful discussion, and a critical review of the manuscript. This study also benefited from the inspiration of Mark Konishi and the supportive atmosphere he created in his laboratory. This research was supported by the International Human Frontier Science Organization, the Sloan Foundation, and Research Grant No. SR01DC134-18 from the National Institute on Deafness and Other Communication Disorders,

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