Parallel pathways mediating both sound localization and gaze control in the forebrain and midbrain of the barn owl

Abstract

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° 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. In contrast, when the optic tectum and nucleus ovoidalis were both inactivated unilaterally, the owls no longer oriented toward contralateral auditory stimuli. However, the owls oriented their gaze forward in response to auditory "zeroing" stimuli even when the stimulus was located contralaterally, indicating that they could still hear sounds located contralaterally and could still make contraversive head turns. Thus, the most likely explanation is that they could no longer localize contralateral sound sources. Together, the results demonstrate that both sound localization and the control of gaze can be mediated by distinct parallel pathways in the midbrain and forebrain. copyright © 1993 society for neuroscience.