Journal of Neuroscience, Vol 13, 2837-2852, Copyright © 1993 by Society for Neuroscience
Parallel pathways mediating both sound localization and gaze control in the forebrain and midbrain of the barn owl
EI Knudsen, PF Knudsen and T Masino
Department of Neurobiology, Stanford University School of Medicine, California 94305.
The hypothesis that sound localization and gaze control are mediated in
parallel in the midbrain and forebrain was tested in the barn owl. The
midbrain pathway for gaze control was interrupted by reversible
inactivation (muscimol injection) or lesion of the optic tectum. Auditory
input to the forebrain was disrupted by reversible inactivation or lesion
of the primary thalamic auditory nucleus, nucleus ovoidalis (homolog of the
medial geniculate nucleus). Barn owls were trained to orient their gaze
toward auditory or visual stimuli presented from random locations in a
darkened sound chamber. Auditory and visual test stimuli were brief so that
the stimulus was over before the orienting response was completed. The
accuracy and kinetics of the orienting responses were measured with a
search coil attached to the head. Unilateral inactivation of the optic
tectum had immediate and long-lasting effects on auditory orienting
behavior. The owls failed to respond on a high percentage of trials when
the auditory test stimulus was located on the side contralateral to the
inactivated tectum. When they did respond, the response was usually (but
not always) short of the target, and the latency of the response was
abnormally long. When the auditory stimulus was located on the side
ipsilateral to the inactivated tectum, responses were reliable and
accurate, and the latency of responses was shorter than normal. In a
tectally lesioned animal, response probability and latency to contralateral
sounds returned to normal within 2 weeks, but the increase in response
error (due to undershooting) persisted for at least 12 weeks. Despite
abnormalities in the response, all of the owls were capable of localizing
and orienting to contralateral auditory stimuli on some trials with the
optic tectum inactivated or lesioned. This was not true for contralateral
visual stimuli. Immediately following tectal inactivation, the owls
exhibited complete neglect for visual stimuli located more than 20 degrees
to the contralateral side (i.e., beyond the edge of the visual field of the
ipsilateral eye). In the tectally lesioned animal, this neglect diminished
with time. Unilateral inactivation of nucleus ovoidalis had different
effects in three owls. Response error to contralateral sound sources
increased for one owl and decreased for two; response error to ipsilateral
sources did not change significantly for any. The probability of response
to ipsilateral (but not contralateral) stimuli decreased for one owl. The
latency of response to ipsilateral (but not contralateral) stimuli
increased for one and decreased for another. All of the owls, however,
routinely localized and oriented toward ipsilateral and contralateral
auditory stimuli with nucleus ovoidalis inactivated.(ABSTRACT TRUNCATED AT
400 WORDS)
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