The Effect of Early Visual Deprivation on the Neural Bases of Auditory Processing

Abstract

Transient congenital visual deprivation affects visual and multisensory processing. In contrast, the extent to which it affects auditory processing has not been investigated systematically. Research in permanently blind individuals has revealed brain reorganization during auditory processing, involving both intramodal and crossmodal plasticity. The present study investigated the effect of transient congenital visual deprivation on the neural bases of auditory processing in humans. Cataract-reversal individuals and normally sighted controls performed a speech-in-noise task while undergoing functional magnetic resonance imaging. Although there were no behavioral group differences, groups differed in auditory cortical responses: in the normally sighted group, auditory cortex activation increased with increasing noise level, whereas in the cataract-reversal group, no activation difference was observed across noise levels. An auditory activation of visual cortex was not observed at the group level in cataract-reversal individuals. The present data suggest prevailing auditory processing advantages after transient congenital visual deprivation, even many years after sight restoration.

Significance statement: The present study demonstrates that people whose sight was restored after a transient period of congenital blindness show more efficient cortical processing of auditory stimuli (here speech), similarly to what has been observed in congenitally permanently blind individuals. These results underscore the importance of early sensory experience in permanently shaping brain function.

Keywords: auditory processing; fMRI; sight restoration; speech processing; visual deprivation.

Figure 1.

ROIs were located in the auditory cortex (top) and visual cortex (bottom). pSTG, Posterior superior temporal gyrus; CaS, calcarine sulcus; FuG, fusiform gyrus. These regions were selected on the basis of their involvement in speech processing in noise in the normally sighted population (i.e., pSTG; Wong et al., 2008), as well as on the basis of their involvement in speech processing in blind individuals (i.e., CaS and FuG; Hertrich et al., 2009; Dietrich et al., 2013).

Figure 2.

Behavioral performance. Left, Mean reaction time and SEs for normally sighted controls and cataract-reversal individuals. Right, Mean accuracy and SEs of the mean for normally sighted controls and cataract-reversal individuals. *p < 0.050.

Figure 3.

Mean β values and SEs in the ROIs for normally sighted controls and cataract-reversal individuals. Left, Posterior superior temporal gyrus; middle, calcarine sulcus; right, fusiform gyrus. *p < 0.050.

Figure 4.

Activations obtained when comparing brain responses to low SNR and brain responses to high SNR (low SNR > high SNR) in the group of normally sighted controls (A) and the group of cataract-reversal individuals (B), overlaid on the average cortex reconstruction of all participants.

Figure 5.

Activations obtained when comparing brain responses of normally sighted controls with brain responses of cataract-reversal individuals (sighted controls > cataract individuals) during low SNR auditory stimulation, overlaid on the average cortex reconstruction of all participants.

Figure 6.

Left, Correlation between β values in the calcarine sulcus (collapsed across hemisphere and SNR) and duration of visual recovery in cataract-reversal individuals. Middle, Correlation between β values in the calcarine sulcus (collapsed across hemisphere and SNR) and age in cataract-reversal individuals. Right, Correlation between β values in the calcarine sulcus (collapsed across hemisphere and SNR) and age in normally sighted individuals.