Does Congenital Deafness Affect the Structural and Functional Architecture of Primary Visual Cortex?

Abstract

Deafness results in greater reliance on the remaining senses. It is unknown whether the cortical architecture of the intact senses is optimized to compensate for lost input. Here we performed widefield population receptive field (pRF) mapping of primary visual cortex (V1) with functional magnetic resonance imaging (fMRI) in hearing and congenitally deaf participants, all of whom had learnt sign language after the age of 10 years. We found larger pRFs encoding the peripheral visual field of deaf compared to hearing participants. This was likely driven by larger facilitatory center zones of the pRF profile concentrated in the near and far periphery in the deaf group. pRF density was comparable between groups, indicating pRFs overlapped more in the deaf group. This could suggest that a coarse coding strategy underlies enhanced peripheral visual skills in deaf people. Cortical thickness was also decreased in V1 in the deaf group. These findings suggest deafness causes structural and functional plasticity at the earliest stages of visual cortex.

Keywords: Deafness; functional magnetic resonance imaging (fMRI); peripheral visual field (PVF); primary visual cortex (V1).

Fig. (1)

Mapping stimulus and retinotopic maps. (a) In the scanner participants viewed rotating wedge and expanding ring stimuli containing a high contrast flickering checkerboard pattern whilst maintaining fixation on a small blue dot in the center of the screen. (b-e) Maps of population receptive field (pRF) parameters for a deaf (b, c) and a hearing (d, e) participant. Data are projected on an inflated model of the right cortical hemisphere. Polar angle (b, d), eccentricity (c ,e) are shown in deaf and hearing participants respectively. The region of interest in primary visual cortex included in the analysis is outlined in each map. All maps are thresholded at R²=0.1, corresponding to the model fit required for the inclusion of the data point for analysis.

Fig. (2)

Full width at half maximum (FWHM) sizes of the pRF averaged across participants’ hemispheres in each group and plotted against eccentricity in primary visual cortex. Data were fitted with a cumulative Gaussian curve. Independent samples t-tests were used to assess whether there were differences between groups at each eccentricity bin. Significantly different bins (p<0.05) are denoted with an asterisk. Red: Deaf participants, Black: Control group. Error bars denote +/- standard error of the mean.

Fig. (3)

Average pRF profile illustrating differences between the deaf (red) and hearing (black) groups in steps of 4° eccentricity.

Fig. (4)

pRF center sizes averaged across participants’ hemispheres in each group and plotted against eccentricity in primary visual cortex. Data have been fitted with a cumulative Gaussian curve. Independent samples t-tests were used to assess whether there were differences between groups for each eccentricity bin. Significantly different bins (p<0.05) are denoted with an asterisk. Red: Deaf participants, Black: Control group. Error bars denote +/- standard error of the mean.

Fig. (5)

No outlier removal procedures have been applied to the data so all participants are included in this graph. PRF center sizes averaged across participants in each group, plotted against eccentricity in V1. Red: Deaf participants, Black: Control group. Error bars denote +/- standard error of the mean. This demonstrates that the pattern of results is qualitatively the same prior to the stringent data exclusion procedures which were applied, suggesting these did not have a distorting effect on results.

Fig. (6)

For 3 participants from the deaf and hearing groups we plotted the Difference-of-Gaussian model predictions and bold time series data at vertices in primary visual cortex. These time series were selected on the basis that they were at the 80^th percentile of all the model fits, when these were ordered from the poorest to the best fit. The model predictions are plotted in blue and the observed bold response at that vertex is plotted in grey. Blank periods in which a blank grey screen was presented rather than a mapping stimulus are highlighted in red.

Fig. (7)

FWHM for V1 were estimated using Difference-of-Gaussians and standard 2D Gaussian population receptive field models. Red dashed line: Deaf participants DoG, Black dashed line: Control group DoG. Red solid line: Deaf participants standard pRF, Black solid line: Control group standard pRF. Error bars denote +/- standard error of the mean. This demonstrates that irrespective of the model used to estimate the FWHM, the pattern of results is qualitatively the same, whereby deaf FWHMs are greater than those of the hearing group, and this difference is most notable in the near – far periphery.

Fig. (8)

Visual positional discrimination thresholds in the central (1.5°), middle (10°) and peripheral visual field (20°) averaged across participants in each group. Red: Deaf participants, Black: Control group. Error bars denote +/- standard error of the mean. Analysis is based on 13 deaf participants and 15 hearing participants.