Cross-Modal Plasticity in Higher-Order Auditory Cortex of Congenitally Deaf Cats Does Not Limit Auditory Responsiveness to Cochlear Implants

Abstract

Congenital sensory deprivation can lead to reorganization of the deprived cortical regions by another sensory system. Such cross-modal reorganization may either compete with or complement the "original" inputs to the deprived area after sensory restoration and can thus be either adverse or beneficial for sensory restoration. In congenital deafness, a previous inactivation study documented that supranormal visual behavior was mediated by higher-order auditory fields in congenitally deaf cats (CDCs). However, both the auditory responsiveness of "deaf" higherorder fields and interactions between the reorganized and the original sensory input remain unknown. Here, we studied a higher-order auditory field responsible for the supranormal visual function in CDCs, the auditory dorsal zone (DZ). Hearing cats and visual cortical areas served as a control. Using mapping with microelectrode arrays, we demonstrate spatially scattered visual (cross-modal) responsiveness in the DZ, but show that this did not interfere substantially with robust auditory responsiveness elicited through cochlear implants. Visually responsive and auditory-responsive neurons in the deaf auditory cortex formed two distinct populations that did not show bimodal interactions. Therefore, cross-modal plasticity in the deaf higher-order auditory cortex had limited effects on auditory inputs. The moderate number of scattered cross-modally responsive neurons could be the consequence of exuberant connections formed during development that were not pruned postnatally in deaf cats. Although juvenile brain circuits are modified extensively by experience, the main driving input to the cross-modally (visually) reorganized higher-order auditory cortex remained auditory in congenital deafness.

Adaptive benefit of cross-modal plasticity following cochlear implantation in deaf adults

“…However, the findings of this study do not support this hypothesis: longitudinal optical imaging of the human brain presented here reveals that increased cross-modal activation of auditory brain regions by lip-reading neither precludes an increase in cortical responsiveness to auditory speech, nor limits the recovery of speech understanding after implantation. Our findings in cochlear implanted adults parallel recent findings in an animal model showing that cross-modal plasticity within auditory brain regions does not preclude responsiveness to auditory stimulation with a CI and therefore should not be considered strictly maladaptive as traditionally thought (19). On the contrary, here we show that increased cross-modal activation after adult cochlear implantation is associated with increased auditory responsiveness and better speech understanding with a CI, indicating an adaptive benefit of crossmodal plasticity following implantation.…”

Congenital deafness affects deep layers in primary and secondary auditory cortex

“…Finally, in previous studies, field specificity in the capacity for cross‐modal takeover following congenital deafness has been documented: visual cross‐modal function was demonstrated in secondary fields DZ and PAF in CDCs (Lomber, Meredith, & Kral, ; Land et al, ), but not in primary fields A1 and anterior auditory field (AAF; Kral, Schroder, Klinke, & Engel, ; Lomber et al, ). AAF, however, showed somatosensory recruitment in cats deafened within the first month of life (Meredith & Lomber, ).…”

“…It remains unclear whether deficits as described in field A1 also involve higher‐order fields. While it has been shown that auditory responsiveness is preserved in field DZ of CDCs along with increased visual responsiveness (Land et al, ), the only previous direct comparison between two cortical hierarchical levels (primary vs. secondary) relates to connection patterns (Barone et al, ). Furthermore, cortical minicolumns, the smallest functional unit in the cerebral cortex (Mountcastle, ), have been investigated functionally and deficits in columnar activation patterns were described in field A1 of CDCs (Kral, Hartmann, Tillein, Heid, & Klinke, ; Kral, Tillein, Heid, Hartmann, & Klinke, ).…”

“…On the other hand, fields taken over by another function, in this case vision, should exhibit fewer dystrophic changes. Consequently, if cross‐modal reorganization was fully ‘protective’, there should be a dissociation of the effect of deafness between fields that were shown to cross‐modally reorganize, such as field DZ (Lomber et al, ; Barone et al, ; Land et al, ), and those where reorganization if this nature was investigated but not observed, such as field A1 (Kral et al, ; Lomber et al, ). If the same dystrophic changes were to be found similarly in fields with and without cross‐modal reorganization, this would indicate that cross‐modal takeover is (either in quality or quantity) not sufficient to counterbalance the absence of auditory input.…”

Multisensory Integration in Cochlear Implant Recipients

“…Together, these studies indicate both structural and functional reorganization in deaf cats, and auditory regions that are recruited for specific visual functions. The relationship between these reorganized auditory areas and later auditory habilitation via a cochlear implant was further investigated in translational work, which showed that auditory areas responsive to visual cues still retain their responsiveness to native auditory inputs although they appear to lack bimodal interactions (Land et al 2016). This, like other findings in humans, suggests that auditory processing can be successfully engaged while multisensory integrative abilities are altered or absent.…”