Neural Mechanisms of Behavior
Proceedings of the 2nd International Congress of Neuroethology
September 10-16, 1989 Berlin

Inhibitory Processes in the Formation of the Auditory Receptive Field

Ichiro Fujita and Masakazu Konishi
Frontier Research Program, RIKEN Institute of Physical and Chemical Research, Wako, Saitama 351-01, Japan;
Division of Biology 216-76, California Institute of Technology, Pasadena, California 91125, U. S. A.

The role of inhibition in the genesis of stimulus selectivity of brain sensory neurons has been the subject of several studies, yet none has addressed what role inhibitory processes play in successive stages of sensory processing. In the barn owl’s auditory system, neuronal selectivity for interaural time difference (ITD), the principal cue for the owl to locate the horizontal position of sound, can be traced from the first site of its emergence to the highest station where the neuronal map of auditory space is formed. This system, therefore, provides unique opportunities to study the roles of inhibition in generating a stimulus selectivity at successive stages of its synthesis.

Neuronal selectivity for ITD is generated in the nucleus laminaris (NL) and transmitted to a lemniscal nucleus (VLVa) and the “core” of the central nucleus of the inferior colliculus (ICc). ICc core projects ipsilaterally to the external nucleus of the inferior colliculus (ICx) and via the contralateral ICc “lateral shell” to the contralateral ICx. ITD selectivity is similar between NL and VLVa. It improves in ICc core and continues to improve among low-frequency ICx neurons. All neurons in NL, VLVa, ICc core and lateral shell respond maximally to one ITD and its phase equivalents, whether the stimulus is a tone or noise (“phase ambiguity”). ICx neurons also show this phenomenon to tone stimuli, but resolve it when stimulated with noise.

VLVa and all subdivisions of the inferior colliculus contain GABAergic cell bodies and terminals. Iontophoretic application of a selective GABAA antagonist, bicuculline methiodide (BMI), decreased ITD selectivity of ICc core neurons and some ICc lateral shell neurons and of ICx neurons with lower best frequency, but not of VLVa neurons. During BMI application, ICx neurons showed phase ambiguity to noise stimuli and no longer responded to a unique ITD. BMI administration increased the response magnitude and made the temporal discharge patterns more sustained in all nuclei tested.

Responses of VLVa and ICc neurons to unfavorable ITDs were below the monoaural response levels. Although BMI elevated both monoaural responses and binaural responses to unfavorable ITDs, the latter never exceeded the former. The results suggest that this suppression of firing is caused by a mechanism other than GABAA receptor-mediated inhibition in these nuclei or it occurs downstream in the pathway, i. E., in the NL.

The present results suggest that under physiological conditions GABAergic inhibition sharpens ITD selectivity in ICc core, ICc lateral shell and ICx, eliminates phase ambiguity in ICx by interactions across frequency channels, and controls response magnitude and temporal response patterns in VLVa, ICc core, ICc lateral shell and ICx. GABAergic inhibition thus plays major and specific roles in the processing of ITD in each nucleus of the pathway , and shapes the horizontal dimension of auditory receptive fields.

(Supported by NIH and Uehara Memorial Foundation)