Significance Statement
Neuroplasticity refers to modifications in neural pathways and synapses that underlie changes in behavior, reactions, and cognition as a consequence of experience. These changes can be expressed as adaptations to new environments and the learning of new skills and ideas. In terms of auditory plasticity, one form is learning the melody of a song or recognizing the voice of a new friend when using the telephone. An example of pathologic plasticity is the emergence of tinnitus (“ringing in the ears”) following partial hearing loss. Tinnitus is a complex pathology that extends across a wide network of auditory and non-auditory circuits. Hearing loss initiates abnormalities in excitatory synapses and a recession of inhibitory circuits, both changes that could cause phantom sound and interfere with the functional benefits of assisted hearing devices such as the cochlear implant.
After documenting structural alterations in the auditory brain of congenitally deaf animal models, we sought to explore whether the prompt attention to hearing loss would mitigate one onset of secondary brain pathologies. We administered cochlear implants to juvenile cats with congenital deafness. The cochlear implant bypasses the nonfunctioning sensory receptors and stimulates the auditory nerve fibers directly. The reactive pathophysiology in the auditory brain system created by hearing loss was returned to near normal in the juvenile by cochlear implants—synapses returned to their normal form, the elaborate branchings of auditory nerve endings were restored, and inhibitory circuits resumed their normal position. Ultimately, we show that restoration of auditory nerve activity via electrical stimulation through cochlear implants serves to correct key features of brain pathology caused by hearing loss. These corrective brain changes are inferred to enable the benefits enjoyed by cochlear implant users. The data reinforce the maxim of “use it or lose it.” That is, uncorrected hearing loss triggers pathologic change that impairs rehabilitation, whereas the prompt recovery of auditory activity restores the system back towards normal. Moreover, we predict that rigorous training with cochlear implants and/or hearing aids offer promise of heretofore unattained benefits.
Figure Legend
Summary diagram illustrating endbulb of Held plasticity under conditions of normal hearing, congenital deafness, and congenital deafness with cochlear implantation. The endbulb (black) embraces the postsynaptic neuron (blue). Deafness results in a reduction of terminal arborization and complexity. Endbulb synapses of deaf animals hypertrophy and lose their characteristic dome shape. Synaptic vesicle density also increases. Electrical stimulation through a cochlear implant in young but not older cats restores synaptic morphology. Synapses regain their dome shape and punctate distribution, and synaptic vesicle density around the release site returns to normal. The endbulb itself partially regains its highly branched arborization, but swellings do not return to the small size typical of those in hearing cats.
Journal Reference
Cell and Tissue Research, July 2015, Volume 361, Issue 1, pp 251-269
Ryugo D
Hearing Research, Garvan Institute, Darlinghurst, NSW, Australia, [email protected].
Abstract
Data from our laboratory show that the auditory brain is highly malleable by experience. We establish a base of knowledge that describes the normal structure and workings at the initial stages of the central auditory system. This research is expanded to include the associated pathology in the auditory brain stem created by hearing loss. Utilizing the congenitally deaf white cat, we demonstrate the way that cells, synapses, and circuits are pathologically affected by sound deprivation. We further show that the restoration of auditory nerve activity via electrical stimulation through cochlear implants serves to correct key features of brain pathology caused by hearing loss. The data suggest that rigorous training with cochlear implants and/or hearing aids offers the promise of heretofore unattained benefits.
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