Integrating sensory and motor information through a complex network of electro-mechanoreceptors and neural connections, the vestibular system controls compensatory responses of the eye, head, and body elicited by external stimuli. Since gaze stabilizing responses depend, in large part, on input from the vestibular system, contributions of these quantifiable behaviors can be used as important barometers for the functional viability of the vestibular system after damage or injury. Aminoglycosidic insults to the vestibular receptors and primary afferents have been shown to elicit repair and regenerative responses in various submammalian classes. The exact mechanisms and return of function after these insults are not yet fully understood. Utilizing avians as the experimental model, this investigation examined anatomical changes in the vestibular labyrinth during regenerative recovery along with measuring the return of gaze stabilization over a long period of time. Specifically, contributions of eye and head movements in normal pigeons and quails were quantified utilizing scleral search coil techniques in response to a broadband battery of rotational stimuli. The two species differed in their compensatory strategies, with the pigeon relying primarily on head movement when the head was free to move, whereas the quail utilized both eyes and head near equally. Next, a group of pigeons was lesioned with translabyrinthine injections of streptomycin to kill hair cells and alter afferent connectivity. Gaze stabilization responses, which were then monitored longitudinally over six months or longer, showed recovery to near normal levels. Gaze responses to fast head movements recovered first, followed by low frequency responses. Conjointly, the afferent innervation pattern morphology was examined in the semicircular canal neuroepithelia. Neural reconstructions of calyx, dimorph, and bouton afferent-types were performed, and a unique 3-dimensional surface mapping of the organs was generated for both normal conditions and after long-term regenerative periods. Calyceal-bearing units occupied the central regions of the crista ampullaris, whereas bouton-bearing units were found along the periphery, and dimorph afferents were noted throughout the neuroepithelium. Regenerated afferents were more complex with larger innervation terminal fields as compared to normal afferents. These studies show that functional vestibular recovery during regeneration occurs over a period of time nearly corresponding with anatomic recovery.
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