Cortical plasticity for visuospatial processing and object recognition in deaf and hearing signers

Abstract

Experience-dependent plasticity in deaf participants has been shown in a variety of studies focused on either the dorsal or ventral aspects of the visual system, but both systems have never been investigated in concert. Using functional magnetic resonance imaging (fMRI), we investigated functional plasticity for spatial processing (a dorsal visual pathway function) and for object processing (a ventral visual pathway function) concurrently, in the context of differing sensory (auditory deprivation) and language (use of a signed language) experience. During scanning, deaf native users of American Sign Language (ASL), hearing native ASL users, and hearing participants without ASL experience attended to either the spatial arrangement of frames containing objects or the identity of the objects themselves. These two tasks revealed the expected dorsal/ventral dichotomy for spatial versus object processing in all groups. In addition, the object identity matching task contained both face and house stimuli, allowing us to examine category-selectivity in the ventral pathway in all three participant groups. When contrasting the groups we found that deaf signers differed from the two hearing groups in dorsal pathway parietal regions involved in spatial cognition, suggesting sensory experience-driven plasticity. Group differences in the object processing system indicated that responses in the face-selective right lateral fusiform gyrus and anterior superior temporal cortex were sensitive to a combination of altered sensory and language experience, whereas responses in the amygdala were more closely tied to sensory experience. By selectively engaging the dorsal and ventral visual pathways within participants in groups with different sensory and language experiences, we have demonstrated that these experiences affect the function of both of these systems, and that certain changes are more closely tied to sensory experience, while others are driven by the combination of sensory and language experience.

Figure 1

Examples of the simultaneous match-to-sample tasks. Blocks of Spatial or Object Matching depicted either Faces (A) or Houses (B) in the embedded squares. During Spatial Matching subjects decided which bottom square contained the photograph in same position relative to the thick line as in the top square. During Object Matching, subjects decided which of the two bottom squares depicted the same object as the sample in the top square, regardless of view.

Figure 2

Activation patterns in the dorsal visual pathway for hearing non-signers, deaf signers, and hearing signers. Coronal sections depicting clusters of activation from each group’s random effects analysis contrasting Spatial vs. Object matching, overlaid on a single subject’s structural image (Talairach and Tournoux coordinate y = −36). Regions in bilateral inferior parietal lobe (blue) were more active for Spatial than Object Matching (right IPL activity is not visible in this slice for hearing signers). Bilateral fusiform and parahippocampal regions (red) responded more during Object than Spatial matching.

Figure 3

Axial sections (z = −11) depicting regions that responded differentially to Faces and Houses during Object matching. Bilateral lateral fusiform gyri (red regions) were more active during Face than House matching in all groups, and bilateral parahippocampal gyri (blue regions) were more active during House than Face matching. All regions p < .05, corrected.

Figure 4

Group results in ROIs based on within-group analyses, showing sensory experience-related differences between deaf and hearing groups. Cell means for the deaf group (red bars) were higher than either hearing group (blue and yellow bars) during Spatial Matching in the left IPL (A) and lower than hearing groups in the right SPL (B). In the left IPL (A), pair-wise between-group ANOVAs demonstrated Task × Group interaction (deaf signers vs. hearing non-signers, p < .002; deaf signers vs. hearing signers, p < .005). The hearing groups (signing and non-signing) did not differ from each other in this region. In the right SPL region (B) pair-wise ANOVAs revealed a Task × Group interaction between the deaf group and the hearing non-signers (p < .001), and a main effect of Group when deaf and hearing signers where compared (p < .004). See Table 2 for local maxima for each group.

Figure 5

Group averaged hemodynamic responses in face-selective regions exhibiting group differences between deaf signers and hearing non-signers. The deaf group (red bars) showed a reduced response for faces in the right lateral fusiform gyrus (A) compared to hearing non-signers (blue bars) (p < .05), and an increased response in the right STG/STS region (B) (p < .05). However, comparison of these groups with hearing signers revealed no differences, suggesting that these effects are not specific to either sensory or signing experience alone. The right amygdala (C) was more active in deaf subjects than in hearing non-signers (p < .05) and hearing signers (p < .01), indicating an effect of deafness. Below each histogram are coronal slices depicting the conjunction of each groups’ clusters for the regions described above. Activity for each group, and their conjunctions, are color coded as follows: orange = all groups; purple = deaf signers and hearing non-signers; green = hearing groups; blue = hearing non-signers; yellow = hearing signers; red = deaf signers.