Neural Mechanisms of
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
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)