Functional Significance of Hair Cell Regeneration

Postmitotic hair cell regeneration in the inner ear of birds provides an opportunity to study the effect of renewed auditory input on auditory detection, discrimination, perception, and, in some species, vocal production and vocal learning. We used behavioral techniques to demonstrate that in budgerigars subjected to aminoglycoside ototoxicity, absolute thresholds recovered to within 20 dB of normal by 28 days when the papilla was completely repopulated. Frequency and intensity difference thresholds also were normal 4 weeks into recovery, but the discrimination among complex, species-species vocalizations still showed subtle effects. The ability to recognize familiar vocalizations was severely impaired, leading to the interpretation that with new hair cells previously familiar sounds were now unrecognizable. Nevertheless, new discriminations and classifications among species-species vocalizations could be easily learned. In these adult birds, the precision with which learned vocalizations were produced was only transiently affected during the first week of recovery when hearing loss and hair cell loss was at a maximum. Recovery of hearing following hair cell regeneration also occurs in the Belgian Waterslager canary, a bird with an inherited auditory deficit involving missing and damaged hair cells that is evident several weeks following hatching. These birds are constantly regenerating new hair cells throughout adulthood at a slow rate but never repair their auditory epithelium. Increasing the rate of proliferation by aminoglycoside treatment results in a recovery overshoot such that absolute thresholds improve slightly relative to pretreatment thresholds. These and other data suggest that the Belgian Waterslager canary may provide a unique model for investigating some genetic forms of early deafness.