Characterization of the Auditory Thalamic Nucleus of the Barn Owl

Citation

Proctor, Larry P. (1995) Characterization of the Auditory Thalamic Nucleus of the Barn Owl. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/ze17-3216. https://resolver.caltech.edu/CaltechETD:etd-10182007-094614

Abstract

The barn owl has the remarkable ability to accurately localize a target on the basis of auditory cues alone. The investigation of the central nervous system mechanisms underlying the sensory aspect of this behavior led to the discovery of neurons which have auditory receptive fields restricted to small regions of the acoustic environment. Neurons with these characteristics were found both in the forebrain and in the inferior colliculus. In the inferior colliculus, neurons which were near one another had receptive fields which were near one another in the sound field; there was a physiological map of auditory space. No such organization was observed in the forebrain. The auditory map of space in the inferior colliculus projects to the optic tectum where it is preserved and placed in register with a visual map of space. The auditory space map in the inferior colliculus and optic tectum have been functionally related to sound localization in a behavioral assay. Recent experiments have demonstrated that the thalamo-telencephalic auditory pathway is sufficient for localization of sound sources, despite the fact that a topographic map of auditory space has not been demonstrated in this neural pathway. The purpose of the work reported upon here was to examine the manner in which the auditory thalamus, nucleus ovoidalis (N.Ov), transforms the neural code which represents the auditory environment. Neurons in nucleus ovoidalis were characterized with respect to their responses to stimulation with sounds presented through earphones. This dichotic stimulation allowed for the independent control of the amplitude, frequency and temporal structure of the sounds delivered to the ear. The anatomy of the afferent and efferent pathways to the auditory thalamus were also investigated.

The activity of extracellularly isolated single-neurons was recorded in the nucleus ovoidalis of the anesthetized barn owl. This nucleus contains two subdivisions based on tonotopic organization. The central and medial portion of the nucleus is organized such that neurons responding well to high frequencies tend to be located dorsally while neurons which respond well to lower frequencies are located progressively more ventral. In the lateral portion of the nucleus, neurons in a dorsoventral electrode penetration have the same best frequency, between 4.5 and 5.0 kHz. Of 114 neurons whose best frequency tuning curves were characterized completely, 14 had two or three clearly distinguishable peaks. The response to sound localization cues at one of the frequency peaks was different from those at the other frequency peak(s). Of 207 neurons which were recorded within N.Ov, all responded to auditory stimulation with broad band noise and all were sensitive to at least one sound localization parameter. In contrast to previously studied auditory nuclei in the medulla and mesencephalon of the barn owl, there was no apparent systematic mapping of either sound localization cue in the dorsoventral, mediolateral or rostrocaudal axes.

Neurons within N.Ov had response tuning curves to interaural time difference (ITD), interaural intensity difference (IID) and frequency which were most similar to those found in the lateral shell and core subdivisions of the central nucleus of the inferior colliculus (ICc). However, neurons were found in ovoidalis which had combinations of response tuning curve types not previously observed in the auditory system of the barn owl. Thirteen neurons were classified as space-specific, although their response properties were not always similar to neurons in the space maps of ICx or optic tectum. Six neurons were found which had broad frequency tuning curves but which also had ambiguous ITD or IID tuning curves in response to white noise.

Injections of retrograde tracers into N.Ov resulted in stained cell bodies in ICc that were sparsely distributed across the three subdivisions of the nucleus. Labeled neurons were located in various positions along the dorsoventral axis of ICc, along which frequency is mapped. Retrogradely labeled somata were found bilaterally in ICc, though the number of labeled cells was higher in inferior colliculus ipsilateral to the injection site. The widely distributed pattern of retrograde staining in ICc was obtained irrespective of the location of the tracer injection within N.Ov. Anterograde tracers injected into the core/medial shell region of ICc resulted in a pattern of stained axonal terminals in the centromedial N.Ov that was relatively focal and which corresponded well with the tonotopic organization of this region of the nucleus. Injection of anterograde tracers into the lateral shell subdivision of ICc yielded labeled axon terminals in the lateral portion of N.Ov in caudal sections, while the heaviest staining was located along the dorsal aspect in the most rostral sections. Anterograde tracer studies revealed that N.Ov efferents originating from the medial portion of the nucleus have a restricted terminal field in the most medial region of the forebrain area Field L2a. The ventrolateral region of N.Ov, however, sends a wide projection pattern of efferent terminations across the mediolateral extent of caudal Field L2. Labeled axon terminals are quite dense in the lateral portion of Field L2 and rather diffuse in the medial aspect.

The unique combinations of physiological responses found in N.Ov as well as its patterns of afferent and efferent connectivity suggest that ovoidalis is reorganizing the neural information concerning acoustic stimuli. While tuning to sound localization cues is maintained, it is possible that such coding may be of secondary consideration in the thalamo-telencephalic pathway. The foundation for the neural representation of auditory recognition may well begin at the level of the auditory thalamus.

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