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

Abstract

It has been suggested that visual language is maladaptive for hearing restoration with a cochlear implant (CI) due to cross-modal recruitment of auditory brain regions. Rehabilitative guidelines therefore discourage the use of visual language. However, neuroscientific understanding of cross-modal plasticity following cochlear implantation has been restricted due to incompatibility between established neuroimaging techniques and the surgically implanted electronic and magnetic components of the CI. As a solution to this problem, here we used functional near-infrared spectroscopy (fNIRS), a noninvasive optical neuroimaging method that is fully compatible with a CI and safe for repeated testing. The aim of this study was to examine cross-modal activation of auditory brain regions by visual speech from before to after implantation and its relation to CI success. Using fNIRS, we examined activation of superior temporal cortex to visual speech in the same profoundly deaf adults both before and 6 mo after implantation. Patients' ability to understand auditory speech with their CI was also measured following 6 mo of CI use. Contrary to existing theory, the results demonstrate that increased cross-modal activation of auditory brain regions by visual speech from before to after implantation is associated with better speech understanding with a CI. Furthermore, activation of auditory cortex by visual and auditory speech developed in synchrony after implantation. Together these findings suggest that cross-modal plasticity by visual speech does not exert previously assumed maladaptive effects on CI success, but instead provides adaptive benefits to the restoration of hearing after implantation through an audiovisual mechanism.

Keywords: cochlear implantation; cross-modal plasticity; functional near-infrared spectroscopy; superior temporal cortex; visual speech.

Fig. 1.

Sensitivity profiles for cortical regions of interest. Left hemisphere measurement channels (9, 10, and 12) and right hemisphere measurement channels (20, 21, and 23) are highlighted. Color scale depicts relative sensitivity to hypothetical cortical activation logarithmically from 0.001 to 1. Reprinted with permission from ref. .

Fig. 2.

Group-averaged amplitude of cross-modal activation before and after implantation. Group-averaged amplitude of cross-modal activation of STC by visual speech (in beta weight) of (A) bilateral STC, (B) left STC, and (C) right STC. Inset cortical images illustrate the sensitivity profile for the cortical regions of interest. *P < 0.05 main effect of time when assessed across both groups combined, based on the estimated marginal means from the linear mixed model analysis. n.s., nonsignificant. Error bars represent ±1 SE. CI, cochlear implant users; NH, normal-hearing controls; T0, preimplantation; T1, postimplantation.

Fig. S1.

Relationship between change in cross-modal bilateral STC activation and duration of deafness. Change in cross-modal activation of bilateral STC by visual speech (∆ beta weight; arbitrary units) from T0 to T1 is plotted against the duration of bilateral hearing loss before implantation (years), with regression line shown.

Fig. 3.

Relationship between change in cross-modal STC activation and speech understanding. Change in cross-modal activation of bilateral STC by visual speech (Δ beta weight; arbitrary units) from T0 to T1 is plotted against speech understanding at T1 (RAU), with the regression line shown.

Fig. S2.

Change in cross-modal activation of left and right STC and speech understanding. Change in cross-modal activation of STC by visual speech (Δ beta weight; arbitrary units) from T0 to T1 is plotted against speech understanding (RAU) at T1, with the regression line shown for (A) the left hemisphere and (B) the right hemisphere.

Fig. 4.

Change in cross-modal STC activation and auditory responsiveness. Change in cross-modal activation of bilateral STC by visual speech from T0 to T1 (Δ beta weight; arbitrary units) is plotted against change in bilateral auditory responsiveness from T0 to T1 with the regression line shown.

Fig. S3.

Change in cross-modal STC activation and auditory responsiveness in control subjects. Change in cross-modal activation of bilateral STC by visual speech from T0 to T1 (Δ beta weight; arbitrary units) is plotted against change in bilateral auditory responsiveness from T0 to T1 with the regression line shown.

Fig. S4.

Mean position of fNIRS optodes and measurement channels. Measurement channels are labeled numerically, source optodes are indicated in red, and detector optodes are indicated in blue.