A sensitive period in the neural phenotype of language in blind individuals

Abstract

Congenital blindness modifies the neural basis of language: "visual" cortices respond to linguistic information, and fronto-temporal language networks are less left-lateralized. We tested the hypothesis that this plasticity follows a sensitive period by comparing the neural basis of sentence processing between adult-onset blind (AB, n = 16), congenitally blind (CB, n = 22) and blindfolded sighted adults (n = 18). In Experiment 1, participants made semantic judgments for spoken sentences and, in a control condition, solved math equations. In Experiment 2, participants answered "who did what to whom" yes/no questions for grammatically complex (with syntactic movement) and simpler sentences. In a control condition, participants performed a memory task with non-words. In both experiments, visual cortices of CB and AB but not sighted participants responded more to sentences than control conditions, but the effect was much larger in the CB group. Only the "visual" cortex of CB participants responded to grammatical complexity. Unlike the CB group, the AB group showed no reduction in left-lateralization of fronto-temporal language network, relative to the sighted. These results suggest that congenital blindness modifies the neural basis of language differently from adult-onset blindness, consistent with a developmental sensitive period hypothesis.

Keywords: Adult-onset blindness; Language development; Sensitive periods.

Fig. 1

Behavioral performance of Sighted (S), Adult-onset Blind (AB) and Congenitally Blind (CB) on Experiment 1 (Sentence (SENT) and Mathematical equations (MATH)) and Experiment 2 (MOVE (M), NONMOVE (NM) and NONWORD (NW)) conditions. Error bars represent standard error of mean (SEM).

Fig. 2

Whole brain analysis results of all subjects in the left and right hemispheres on the lateral, medial and ventral surface (cluster corrected, p < 0.05) for Experiment 1 (left) and Experiment 2 (right) in the Congenitally Blind (CB, n = 22), Adult Onset Blind (AB, n = 16 (Experiment 1), 15 (Experiment 2)) and Sighted (S, n = 18) groups.

Fig. 3

Percent Signal Change (PSC) in response to the Sentence and Equation conditions of Experiment 1 and the MOVE, NONMOVE and NONWORD conditions of Experiment 2 in the Sighted (S), Adult-Onset blind (AB) and Congenitally Blind (CB) groups in (a) occipital cortex and (b) frontal cortex ROIs. Error bars represent SEM.

Fig. 4

Effect of blindness duration (in Adult Onset Blind) and age (in Congenitally Blind) on visual cortex responses to language. PSC extracted from functionally defined individual LangV1 and CB LangOccip ROIs for the SENTENCE-NONWORD and MOVE-NONMOVE conditions in Experiment 2, and LangV1 and AB LangOccip ROIs for the SENTENCE-EQUATION conditions of Experiment 1.

Fig. 5

Mean laterality index for sighted (S), adult-onset blind (AB) and congenitally blind (CB) participants in response to the sentences > mathematics (Experiment 1) and sentences > nonwords (Experiment 2) condition in the whole brain excluding the occipital cortex. Error bars represent SEM.