Impact of early deafness and early exposure to sign language on the cerebral organization for motion processing

Abstract

This functional magnetic resonance imaging study investigated the impact of early auditory deprivation and/or use of a visuospatial language [American sign language (ASL)] on the organization of neural systems important in visual motion processing by comparing hearing controls with deaf and hearing native signers. Participants monitored moving flowfields under different conditions of spatial and featural attention. Recruitment of the motion-selective area MT-MST in hearing controls was observed to be greater when attention was directed centrally and when the task was to detect motion features, confirming previous reports that the motion network is selectively modulated by different aspects of attention. More importantly, we observed marked differences in the recruitment of motion-related areas as a function of early experience. First, the lateralization of MT-MST was found to shift toward the left hemisphere in early signers, suggesting that early exposure to ASL leads to a greater reliance on the left MT-MST. Second, whereas the two hearing populations displayed more MT-MST activation under central than peripheral attention, the opposite pattern was observed in deaf signers, indicating enhanced recruitment of MT-MST during peripheral attention after early deafness. Third, deaf signers, but neither of the hearing populations, displayed increased activation of the posterior parietal cortex, supporting the view that parietal functions are modified after early auditory deprivation. Finally, only in deaf signers did attention to motion result in enhanced recruitment of the posterior superior temporal sulcus, establishing for the first time in humans that this polymodal area is modified after early sensory deprivation. Together these results highlight the functional and regional specificity of neuroplasticity in humans.

Fig. 1.

A, Schematic representation of the alternations of motion and static blocks for the luminance task and for the velocity task in the full-field condition. At the end of each run, subjects were asked to report the number of blocks that contained three or more changes. B, Stimuli in the central and peripheral field conditions covered the same spatial extent as in the full-field condition, but were organized in three separate rings. In the central condition, the changes in luminance or velocity were restricted to the central ring. In the peripheral field condition, the changes in luminance or velocity only occurred in the most peripheral ring.

Fig. 2.

Summary of the network of posterior regions recruited during motion processing in hearing controls; the frontal eye field (FEF) used to control for eye movement artifacts is also displayed.

Fig. 3.

Example of activations in motion-related areas for one deaf and one hearing participant.

Fig. 4.

A, Extent of the activation in MT–MST for hearing controls and deaf signers in the LH and RH. Deaf signers displayed a greater recruitment in the LH, whereas hearing controls showed a greater recruitment in the RH (population × hemisphere: p < 0.009);B, Extent of the activation in MT–MST for hearing controls and deaf signers when attention was directed toward the center and the periphery. Deaf signers showed an enhanced recruitment under the peripheral attention condition compared with hearing controls, whereas the opposite trend was observed under central attention (population × attention location: p < 0.019).

Fig. 5.

Percentage of signal change in the PPC for hearing controls, deaf signers, and hearing signers. The greater activation observed in deaf signers compared with hearing controls and hearing signers suggests a heightened recruitment of this area after early deafness (contrast analysis: p < 0.009; see Results, Impact of signing: the case of hearing signers, Posterior parietal cortex section for details).

Fig. 6.

A, Extent of activation in the post-STS for hearing controls, deaf signers, and hearing signers when subjects were required to monitor the display for luminance changes.B, Extent of activation in the post-STS for hearing controls, deaf signers, and hearing signers when subjects were required to monitor the display for velocity changes. Although a tendency for greater activation was observed in deaf signers in the luminance task (A), statistical analyses indicated that this tendency was not reliable. In contrast, a robust increase in activation can be seen in deaf signers during the velocity task (B, contrast analysis: p < 0.002).

Fig. 7.

A, Difference between the extent of activation in the LH and RH in MT–MST for each of the three populations. The hearing controls displayed a RH bias, but a LH bias was observed in both deaf and hearing signers, indicating that the acquisition of ASL was the major factor in the altered lateralization of the MT–MST complex (contrast analysis: p < 0.0052). B, Difference between the extent of activation in the central and the peripheral attention conditions in MT–MST for each of the three populations. Hearing controls and hearing signers showed the same bias for greater recruitment during central compared with peripheral attention, whereas the opposite trend is observed in deaf signers, suggesting that enhanced recruitment of MT–MST during peripheral attention is specifically attributable to auditory deprivation (contrast analysis: p < 0.034).