Evolution of crossmodal reorganization of the voice area in cochlear-implanted deaf patients

Abstract

Psychophysical and neuroimaging studies in both animal and human subjects have clearly demonstrated that cortical plasticity following sensory deprivation leads to a brain functional reorganization that favors the spared modalities. In postlingually deaf patients, the use of a cochlear implant (CI) allows a recovery of the auditory function, which will probably counteract the cortical crossmodal reorganization induced by hearing loss. To study the dynamics of such reversed crossmodal plasticity, we designed a longitudinal neuroimaging study involving the follow-up of 10 postlingually deaf adult CI users engaged in a visual speechreading task. While speechreading activates Broca's area in normally hearing subjects (NHS), the activity level elicited in this region in CI patients is abnormally low and increases progressively with post-implantation time. Furthermore, speechreading in CI patients induces abnormal crossmodal activations in right anterior regions of the superior temporal cortex normally devoted to processing human voice stimuli (temporal voice-sensitive areas-TVA). These abnormal activity levels diminish with post-implantation time and tend towards the levels observed in NHS. First, our study revealed that the neuroplasticity after cochlear implantation involves not only auditory but also visual and audiovisual speech processing networks. Second, our results suggest that during deafness, the functional links between cortical regions specialized in face and voice processing are reallocated to support speech-related visual processing through cross-modal reorganization. Such reorganization allows a more efficient audiovisual integration of speech after cochlear implantation. These compensatory sensory strategies are later completed by the progressive restoration of the visuo-audio-motor speech processing loop, including Broca's area.

Copyright © 2011 Wiley Periodicals, Inc.

Figures

Figure 1

Brain activation patterns during speech‐reading. A: cochlear‐implant patients at T0 (n = 9). B: cochlear‐implant patients at T1 (n = 8). Speech‐reading elicits auditory activations in cochlear‐implant patients. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 2

Activity in the voice identity area during speech‐reading. A: activation patterns for each subject group and differential activation pattern between patients at T0 and NH controls. B: normalized regional cerebral blood flow (arbitrary units) in the right anterior superior temporal sulcus for each subject group. Activity level in the voice identity area decreases with the auditory experience, being high for inexperienced cochlear‐implant patients, and low for NH controls. Panel C shows the individual differences of activity between T0 and T1 (7 paired comparisons; the single outlier is a different patient than the one in Fig. 3C).

Figure 3

Activity in Broca's area during speech‐reading. A: activation patterns for each subject group and differential activation pattern between NH controls and patients at T0. B: normalized regional cerebral blood flow (arbitrary units) in the left posterior middle frontal gyrus for each subject group. Activity level in Broca's area increases with the auditory experience, being low for inexperienced cochlear‐implant patients and high for NH controls. Panel C shows the individual differences of activity between T0 and T1 (7 paired comparisons; the single outlier is a different patient than the one in Fig. 2C).

Figure 4

Functional/behavioral relationships observed in patients at T0. Inexperienced cochlear‐implant patients present a positive correlation (P = 0.0008) between the normalized regional cerebral blood flow (arbitrary units) in the voice identity area and their speech‐reading word/nonword recognition score (in % correct).

Figure 5

Relationship between activity levels in the voice identity area and Broca's area. At the population level there is a negative correlation (P = 0.0093) between normalized regional cerebral blood flows (arbitrary units) in the voice identity area and Broca's area. Inexperienced cochlear‐implant users display high activity in the voice identity area and low activity in Broca's area. While this is the reverse in NH controls, experienced CI users display intermediary activity levels in both areas.