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Journal of Neuroscience, Vol 11, 722-739, Copyright © 1991 by Society for Neuroscience
The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system
I Fujita and M Konishi
Division of Biology, California Institute of Technology, Pasadena 91125.
The barn owl uses interaural time differences (ITDs) to localize the
azimuthal position of sound. ITDs are processed by an anatomically distinct
pathway in the brainstem. Neuronal selectivity for ITD is generated in the
nucleus laminaris (NL) and conveyed to both the anterior portion of the
ventral nucleus of the lateral lemniscus (VLVa) and the central (ICc) and
external (ICx) nuclei of the inferior colliculus. With tonal stimuli,
neurons in all regions are found to respond maximally not only to the real
ITD, but also to ITDs that differ by integer multiples of the tonal period.
This phenomenon, phase ambiguity, does not occur when ICx neurons are
stimulated with noise. The main aim of this study was to determine the role
of GABAergic inhibition in the processing of ITDs. Selectivity for ITD is
similar in the NL and VLVa and improves in the ICc and ICx. Iontophoresis
of bicuculline methiodide (BMI), a selective GABAA antagonist, decreased
the ITD selectivity of ICc and ICx neurons, but did not affect that of VLVa
neurons. Responses of VLVa and ICc neurons to unfavorable ITDs were below
the monaural response levels. BMI raised both binaural responses to
unfavorable ITDs and monaural responses, though the former remained smaller
than the latter. During BMI application, ICx neurons showed phase ambiguity
to noise stimuli and no longer responded to a unique ITD. BMI increased the
response magnitude and changed the temporal discharge patterns in the VLVa,
ICc, and ICx. Iontophoretically applied GABA exerted effects opposite to
those of BMI, and the effects could be antagonized with simultaneous
application of BMI. These results suggest that GABAergic inhibition (1)
sharpens ITD selectivity in the ICc and ICx, (2) contributes to the
elimination of phase ambiguity in the ICx, and (3) controls response
magnitude and temporal characteristics in the VLVa, ICc, and ICx. Through
these actions, GABAergic inhibition shapes the horizontal dimension of the
auditory receptive fields.
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