Directional Visual Motion Is Represented in the Auditory and Association Cortices of Early Deaf Individuals

Abstract

Individuals who are deaf since early life may show enhanced performance at some visual tasks, including discrimination of directional motion. The neural substrates of such behavioral enhancements remain difficult to identify in humans, although neural plasticity has been shown for early deaf people in the auditory and association cortices, including the primary auditory cortex (PAC) and STS region, respectively. Here, we investigated whether neural responses in auditory and association cortices of early deaf individuals are reorganized to be sensitive to directional visual motion. To capture direction-selective responses, we recorded fMRI responses frequency-tagged to the 0.1-Hz presentation of central directional (100% coherent random dot) motion persisting for 2 sec contrasted with nondirectional (0% coherent) motion for 8 sec. We found direction-selective responses in the STS region in both deaf and hearing participants, but the extent of activation in the right STS region was 5.5 times larger for deaf participants. Minimal but significant direction-selective responses were also found in the PAC of deaf participants, both at the group level and in five of six individuals. In response to stimuli presented separately in the right and left visual fields, the relative activation across the right and left hemispheres was similar in both the PAC and STS region of deaf participants. Notably, the enhanced right-hemisphere activation could support the right visual field advantage reported previously in behavioral studies. Taken together, these results show that the reorganized auditory cortices of early deaf individuals are sensitive to directional motion. Speculatively, these results suggest that auditory and association regions can be remapped to support enhanced visual performance.

Figure 1.

(A) Stimulation sequences consisted of 2 sec of directional (100% coherent dot) visual motion followed immediately by 8 sec of nondirectional (0% coherent dot) motion. The onset of directional motion thus occurred periodically every 10 sec, predicting a direction-selective response in the frequency domain at 0.1 Hz (i.e., 1/10 sec). The arrows drawn on the figure are purely for illustrating the direction of dot motion. (B) Top: An example of the BOLD response recorded by fMRI from a single voxel in visual area hMT+ from a hearing participant, averaged over four runs of visual motion presented in the CVF and DC corrected. Its location is illustrated on the sagittal slice of this participant’s anatomy in Talairach space. Bottom: A fast Fourier transform (FFT) is applied to each voxel to transform the data into the temporal frequency domain. This example voxel is sensitive to directional motion, as evidenced by the high-amplitude BOLD signal of the 0.1-Hz response peak.

Figure 2.

The size of STS region and hMT+ ROIs in deaf and hearing individuals. In the center, a sagittal slice (right hemisphere; Talairach x = 46) provides an example of the location of these regions defined in a single hearing participant; the STS region is drawn in green, being dorsal and slightly more anterior relative to hMT+, drawn in blue/purple. (A) The extent of activation in the STS region in deaf and hearing individuals (average [Avg.] across groups plotted on the far right, with error bars representing ± 1 SE), in each of the left and right hemisphere. (B) The extent of activation in hMT+, plotted as in A.

Figure 3.

The STS region ROIs in the anatomy of deaf and hearing individuals, in Talairach space. Data are thresholded with individually defined z score values (see the scale in the top right corner). These sagittal slices are centered around the functionally defined ROI for each hemisphere; in three cases where a functional ROI could not be defined in one hemisphere, the x coordinate mirrors that of the other hemisphere (and is written in italics).

Figure 4.

Amplitude values (baseline-subtracted) of the frequency domain analysis of periodic BOLD signal changes to directional motion at 0.1 Hz. Data are reported for deaf and hearing participants in response to visual stimuli presented in the LVF and RVF in the left (LH) and right (RH) hemispheres. Results are shown in the ROIs defined previously for the STS region (A) and hMT+ (B). Group data are plotted in bar graphs (error bars plotting ± 1 SE), and individual data are plotted as superimposed dots (deaf, filled-in; hearing, unfilled-in); each participant is plotted in a consistent color across plots.

Figure 5.

Responses to directional visual motion activated the PAC of deaf individuals. (A) At the group level, areas of activation in deaf participants’ temporal lobes encompassed the probabilistic area of the auditory cortex (shown in light blue on the standard Colin 27 brain; data at p < .001). Moreover, (B) significant responses to direction-selective motion at 0.1 Hz were found in the PAC (shaded in light blue) at the individual level, although the area of activation was small relative to the STS region: z Scores of three deaf individuals are shown here at the same thresholded level used to define their individual STS ROI (D2: z > 4.57; D3: z > 5.7; D4: z > 2.6). (C) The pattern of activation in the left and right PAC for deaf participants to visual motion in the LVF and RVF was similar to that of their STS region (compare with Figure 4A). Again, group data are plotted in bar graphs (error bars plotting ± 1 SE), and individual data are plotted as superimposed dots; colors are consistent across plots and labeling in B. L = left; R = right.