Recovery of hearing and vocal behavior after hair-cell regeneration

Abstract

Postmitotic hair-cell regeneration in the inner ear of birds provides an opportunity to study the effect of renewed auditory input on auditory perception, vocal production, and vocal learning in a vertebrate. We used behavioral conditioning to test both perception and vocal production in a small Australian parrot, the budgerigar. Results show that both auditory perception and vocal production are disrupted when hair cells are damaged or lost but that these behaviors return to near normal over time. Precision in vocal production completely recovers well before recovery of full auditory function. These results may have particular relevance for understanding the relation between hearing loss and human speech production especially where there is consideration of an auditory prosthetic device. The present results show, at least for a bird, that even limited recovery of auditory input soon after deafening can support full recovery of vocal precision.The avian inner ear provides a useful model for the study of hair-cell regeneration and recovery in the vertebrate ear, but the ultimate value of this regenerative capacity depends on whether it results in functional recovery of auditory and vocal behavior (1-3). In response to either acoustic trauma or insult from ototoxic drugs, both young and adult birds show a temporary period of hair-cell loss and regeneration, usually culminating in considerable anatomical, physiological, and behavioral recovery within several weeks (4-12). Behavioral recovery, as typically defined, refers only to a return of absolute auditory sensitivity to near pretrauma levels (13-16). Much less is known about the recovery of more complex auditory behavior, and nothing is known about the effect of hearing loss and recovery on the production or recognition of learned vocalizations. Though evolutionarily distant from humans, birds provide the only animal model for studying hearing restoration by renewed sensory-cell input and for examining the effect of such recovery on learned vocalizations. The question is whether a ''new'' auditory periphery results in sufficient functional recovery that a bird can again perceive, learn, and produce complex acoustic communication signals. The nature of this recovery bears on fundamental issues in auditory plasticity and sensorimotor interfaces. Moreover, the ability to track the time course of such recovery in a vertebrate auditory system may have particular significance for the effective use of auditory prosthetic devices, such as cochlear implants, for the severely hearing impaired (17).Budgerigars (domesticated parakeets), learn new vocalizations throughout life, especially in response to changes in their social milieu (18)(19)(20). Further, our work, as well as the work of others, has shown that these birds experience hair-cell loss and threshold shift after administration of the ototoxic drug kanamycin followed, within several days or weeks, by hair-cell regeneration and a gradual recovery to within 20 dB of normal auditory sensitivity (21,22). In th...

Manipulating cell cycle regulation in the mature cochlea

“…Thus, formation of new hair cells would reduce the number of supporting cells and compromise the ability to restore normal cochlear structure and function. In birds, where hair cell regeneration leads to functional recovery (Dooling et al, 1997;Marean et al, 1995;Niemiec et al, 1994;Saunders et al, 1992), non-sensory cells divide after a lesion to the epithelium (Hashino and Salvi, 1993;Raphael, 1992;Stone and Cotanche, 1994). To induce proliferation in the mature organ of Corti as part of the reparative process, it may be necessary to manipulate expression of genes that regulate cell cycle.…”

New studies on hair cell regeneration in birds

“…Contact calls from different birds are usually quite different and easy to discriminate, while discriminating synthetic contact calls modeled after natural ones provides a more difficult test. The relatively easy discrimination between contact calls from different birds was unaffected 4 weeks following kanamycin treatment, while the more difficult discrimination between a natural contact call and its synthetic analogue was significantly impaired for several months, improving to pre-injection performance levels only after 5-6 months [17]. These results are shown in Fig.…”

“…Figure 1 shows the effect of 8 days of kanamycin administration on the inner ear of budgerigars. After 6 days of kanamycin injections, virtually all of the hair cells are missing in the basal 40% of the papilla [17]. Hair cells begin to be replaced (regenerated) in the basal 40% during the next 6-7 days, while hair cell damage (swelling, stereocilia abnormalities) begins to be seen in the distal one-half of the papilla.…”

Hair cell regeneration: An exciting phenomenon . . . But will restoring hearing and balance be possible?

“…Dooling and his colleagues used budgerigars (Melopsittacus undulatus [Australian parrot]) to examine the return of complex auditory perception and vocal production after hair cell regeneration [106][107]. Budgerigars mimic sounds and readily learn new vocalizations throughout their lives, which has been likened to language acquisition in humans.…”