Unilateral hearing during development: hemispheric specificity in plastic reorganizations

Abstract

The present study investigates the hemispheric contributions of neuronal reorganization following early single-sided hearing (unilateral deafness). The experiments were performed on ten cats from our colony of deaf white cats. Two were identified in early hearing screening as unilaterally congenitally deaf. The remaining eight were bilaterally congenitally deaf, unilaterally implanted at different ages with a cochlear implant. Implanted animals were chronically stimulated using a single-channel portable signal processor for two to five months. Microelectrode recordings were performed at the primary auditory cortex under stimulation at the hearing and deaf ear with bilateral cochlear implants. Local field potentials (LFPs) were compared at the cortex ipsilateral and contralateral to the hearing ear. The focus of the study was on the morphology and the onset latency of the LFPs. With respect to morphology of LFPs, pronounced hemisphere-specific effects were observed. Morphology of amplitude-normalized LFPs for stimulation of the deaf and the hearing ear was similar for responses recorded at the same hemisphere. However, when comparisons were performed between the hemispheres, the morphology was more dissimilar even though the same ear was stimulated. This demonstrates hemispheric specificity of some cortical adaptations irrespective of the ear stimulated. The results suggest a specific adaptation process at the hemisphere ipsilateral to the hearing ear, involving specific (down-regulated inhibitory) mechanisms not found in the contralateral hemisphere. Finally, onset latencies revealed that the sensitive period for the cortex ipsilateral to the hearing ear is shorter than that for the contralateral cortex. Unilateral hearing experience leads to a functionally-asymmetric brain with different neuronal reorganizations and different sensitive periods involved.

Rapid bilateral improvement in auditory cortex activity in postlingually deafened adults following cochlear implantation

“…For instance, our finding of a correlation between the duration of deafness and the N1 latency indicates that longer duration of deafness limits cortical adaptation to the implant signal, at least in the ipsilateral hemisphere to the CI. This supports previous observations of hemispheric specificity of some cortical adaptations (Kral et al, 2013), and is consistent with the finding that longer duration of deafness leads to reduced cortical activation (Green et al, 2005) and poorer auditory discrimination ability with a CI (Sandmann et al, 2010). The limitation in cortical adaptation may be related to physiological deficiencies (Nadol, 1997;Nadol and Wen-Zhuang, 1992;Nadol et al, 1989) and central reorganization during the period of auditory deprivation, in particular a decline in sound memory and a take-over of the auditory cortex by the remaining sensory modalities (Lazard et al, 2013(Lazard et al, , 2012Sandmann et al, 2012).…”

“…Specifically, sequentially implanted CI children develop abnormally high lateralization of auditory cortex response contralateral to the stimulated ear when the implantation of the second ear is delayed more than 1.5 years (Gordon et al, 2013). Together with the results from animal studies, these findings point to specific sensitive developmental periods at the ipsilateral and the contralateral hemisphere (Kral et al, 2002(Kral et al, , 2013. Thus, profound deafness beyond these sensitive periods has severe consequences for the development of ipsilateral and contralateral activation after cochlear implantation (Kral and Sharma, 2012).…”

Strengthening of Hearing Ear Representation Reduces Binaural Sensitivity in Early Single-Sided Deafness

“…Differences in developmental time courses of inhibitory and excitatory synapses in the hearing brain [Gao et al, 1999[Gao et al, , 2000 facilitate distinct reorganisations taking place in these two hemispheres in sequential implantations. Consequently, the mechanisms of the reorganisation and the final functional state following early singlesided deafness differ in the two hemispheres -the reorganisations show a strong hemispheric specificity [Kral et al, 2013a]. Such a re-sculptured, asymmetric brain is specialised for the unilateral hearing condition, which may be detrimental for the later use of the initially deaf ear.…”

“…The earlier the asymmetry sets in, the larger the effects [Kral et al, 2013a, b]. Interestingly, additionally to a sensitive period for plasticity in the cortex contralateral to the trained ear [for a review, see Kral and Sharma, 2012], the ipsilateral cortex showed even a shorter sensitive period and, within it, more extensive reorganisations [Kral et al, 2013a].…”

Functional Neuroimaging Studies in Asymmetric Hearing Loss

“…Kral et al [2013] studied white cats suffering from AHL implanted at an early and late age, and compared the subsequent plasticity following chronic CI stimula- 51 tion with local field potentials. The plasticity mechanism was similar at all ages, only the extent of the effect faded with increasing age, with faster progression at the ipsilateral hemisphere.…”