Recovery of gaze stability during vestibular regeneration

Many motion related behaviors, such as gaze stabilization, balance, orientation, and navigation largely depend on a properly functioning vestibular system. After vestibular insult, many of these responses are compromised but can return during the regeneration of vestibular receptors and afferents as is known to occur in birds, reptiles, and amphibians. Here we characterize gaze stability in pigeons to rotational motion during regeneration after complete bilateral vestibular loss via an ototoxic antibiotic. Immediate postlesion effects included severe head oscillations, postural ataxia, and total lack of gaze control. We found that these abnormal behaviors gradually subsided, and gaze stability slowly returned to normal function according to a temporal sequence that lasted several months. We also found that the dynamic recovery of gaze function during regeneration was not homogeneous for all types of motion. Instead high-frequency motion stability was first achieved, followed much later by slow movement stability. In addition, we found that initial gaze stability was established using almost exclusive head-response components with little eye-movement contribution. However, that trend reversed as recovery progressed so that when gaze stability was complete, the eye component had increased and the head response had decreased to levels significantly different from that observed in normal birds. This was true even though the head-fixed VOR response recovered normally. Recovery of gaze stability coincided well with the three stage temporal sequence of morphologic regeneration previously described by our laboratory.