Evidence that cochlear-implanted deaf patients are better multisensory integrators

Abstract

The cochlear implant (CI) is a neuroprosthesis that allows profoundly deaf patients to recover speech intelligibility. This recovery goes through long-term adaptative processes to build coherent percepts from the coarse information delivered by the implant. Here we analyzed the longitudinal postimplantation evolution of word recognition in a large sample of CI users in unisensory (visual or auditory) and bisensory (visuoauditory) conditions. We found that, despite considerable recovery of auditory performance during the first year postimplantation, CI patients maintain a much higher level of word recognition in speechreading conditions compared with normally hearing subjects, even several years after implantation. Consequently, we show that CI users present higher visuoauditory performance when compared with normally hearing subjects with similar auditory stimuli. This better performance is not only due to greater speechreading performance, but, most importantly, also due to a greater capacity to integrate visual input with the distorted speech signal. Our results suggest that these behavioral changes in CI users might be mediated by a reorganization of the cortical network involved in speech recognition that favors a more specific involvement of visual areas. Furthermore, they provide crucial indications to guide the rehabilitation of CI patients by using visually oriented therapeutic strategies.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Word-recognition scores for CI users in the three sensory modalities: auditory only (A only, green), visual only (V only, blue), and bisensory visuoauditory (VA, red). (A) Longitudinal performance (mean percentage correct ± SD) of the entire cohort of CI users (n = 97) at different times before (preoperatively) and after the cochlear implantation. In the left part of the graph, we have reported the speechreading performance (V only) of NH subjects (n = 42). (B) Individual performance levels for two CI users who have been regularly evaluated during a 3-year period after implantation. Both graphs show the significant recovery of auditory speech recognition during the first year compared with the weak performance before implantation and the stable high values of speechreading at all periods tested. In bisensory conditions, near-maximum scores are achieved.

Fig. 2.

Relationships between auditory and visuoauditory performance and bisensory gain. (A) For each group we have plotted the performance of individual subjects in auditory-only conditions with respect to the performance in visuoauditory conditions. Each point corresponds to a single subject tested in a single condition. This graph shows that the three experimental groups (CI users at T0, NH subjects with masking noise, and NH subjects with vocoder simulations) are clearly segregated in the correlation graph, indicating that the three populations present different gains after a bisensory presentation. (B) The visuoauditory gain (expressed as [(VA-A)/(100-A)]) is presented separately for three ranges of auditory performance (<30% correct, between 30% and 60% correct, and >60% correct) from each group. This subdivision shows that, in all cases, CI patients obtained a significantly higher visuoauditory gain than that observed in NH subjects tested with degraded auditory stimuli. The visuoauditory benefit for CI users is considerably greater than that computed from the NH subject vocoder group. The gains from these latter groups are directly comparable because of a similar processing of the auditory stimulus. Asterisks indicate statistically significant differences in visuoauditory benefits between CI users and both NH subject groups.

Fig. 3.

Fitting a model of multisensory integration to the data. Filled circles represent the data (green, auditory; blue, visual; red, bisensory), dotted lines represent the predicted bisensory performance in the absence of multisensory integration (“model 1” in Materials and Methods), and plain lines represent the prediction of an optimal multisensory integration model with a threshold T = 6 (“model 2” in Materials and Methods). (A and B) CI users performance at T0 (A) and 1 year after implantation (B). Each group represents the averaged performance of three CI users ranked by their auditory performance. Thus, group 1 represents the (true and predicted) performance of the three subjects with the worst auditory performance, and group 26 represent the performance of the three subjects with the best auditory performance. (C) NH subjects' word recognition scores as a function of the amplitude of auditory white noise. (D) Word recognition scores of NH subjects as a function of the number of auditory frequency channels (simulated implants). This analysis shows that visuoauditory performance of CI users is perfectly in agreement with the optimal multisensory model,whereas NH subjects listening to CI simulations obtain bisensory performance far below that predicted by the integrating model.