Reduced Left Lateralization of Language in Congenitally Blind Individuals

Abstract

Abstract■ Language processing depends on a left-lateralized network of frontotemporal cortical regions. This network is remarkably consistent across individuals and cultures. However, there is also evidence that developmental factors, such as delayed exposure to language, can modify this network. Recently, it has been found that, in congenitally blind individuals, the typical frontotemporal language network expands to include parts of "visual" cortices. Here, we report that blindness is also associated with reduced left lateralization in frontotemporal language areas. We analyzed fMRI data from two samples of congenitally blind adults (n = 19 and n = 13) and one sample of congenitally blind children (n = 20). Laterality indices were computed for sentence comprehension relative to three different control conditions: solving math equations (Experiment 1), a memory task with nonwords (Experiment 2), and a "does this come next?" task with music (Experiment 3). Across experiments and participant samples, the frontotemporal language network was less left-lateralized in congenitally blind than in sighted individuals. Reduction in left lateralization was not related to Braille reading ability or amount of occipital plasticity. Notably, we observed a positive correlation between the lateralization of frontotemporal cortex and that of language-responsive occipital areas in blind individuals. Blind individuals with right-lateralized language responses in frontotemporal cortices also had right-lateralized occipital responses to language. Together, these results reveal a modified neurobiology of language in blindness. Our findings suggest that, despite its usual consistency across people, the neurobiology of language can be modified by nonlinguistic experiences. ■

Brain (re)organization following visual loss

“…Stevens and Weaver (2009) showed that early blind individuals exhibited reduced bold responses in their auditory cortex in response to tones, whereas, in contrast, Elbert et al (2002) showed that early blind individuals benefit from an expansion of the core tonotopic area of their auditory cortex. A pair of studies identified more subtle group laterality differences: Lane et al (2017) found stronger bilaterality for language processing in the congenitally blind, documenting a significantly reduced left-lateralized response for language stimuli, whereas Atilgan, Collignon, and Hasson (2017) found that cortical thickness measures in both auditory cortices were more strongly correlated with each other in the blind than in sighted individuals. The situation is quite similar in the somatosensory system, where only a handful of studies have documented changes within the primary sensory cortex of blind individuals (Pascual-Leone & Torres, 1993;Sterr et al, 1998aSterr et al, , 1998b.…”

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

“…Finally, language-responsive "visual" areas are co-lateralized with the fronto-temporal language network, and show higher functional correlations with classical "language" regions even in the absence of a task (i.e. at rest) (Kanjlia, Lane, Feigenson, & Bedny, 2016;Bedny, et al, 2011;Lane et al, 2017;Liu et al, 2007).…”

“…Consistent with this prior evidence for the malleability of the neural basis of language during development, evidence from studies of blindness suggests that the language network can be augmented with cortical real-estate that is typically occupied by visual perception. Individuals who are blind from birth recruit a network of "visual" areas during sentence processing, lexical retrieval, reading and word production tasks (Hamilton & Pascual-Leone, 1998;Kupers et al, 2007;Sadato et al, 1998;Bedny, Pascual-Leone, Dodell-Feder, Fedorenko, & Saxe, 2011;Lane, Kanjlia, Omaki, & Bedny, 2015;Lane et al, 2017;Röder, Stock, Bien, Neville, & Rösler, 2002;Watkins et al, 2012). This recruitment is part of a broader phenomenon, whereby in blindness, regions of the "visual" cortex are recruited for non-visual functions, including spatial localization and numerical cognition (for review, see Bedny, 2017;Collignon et al, 2011;Kanjlia, Lane, Feigenson, & Bedny, 2016;Kim, Kanjlia, Merabet, & Bedny, 2017;Röder, Rösler, & Neville, 2000).…”

“…One study of resting state connectivity found that individuals with retinitis pigmentosa, who did not become totally blind until adulthood, show elevated correlations between inferior frontal language areas and occipital cortices (Sabbah et al, 2016). 6 temporal language areas themselves (Lane et al, 2015;Lane et al, 2017;Röder et al, 2002). This phenomenon appears to be unrelated to the recruitment of visual cortex for language per se, since across blind individuals the amount of "visual" cortex recruitment for language is not predictive of the laterality of fronto-temporal language networks.…”

Functional outcomes following lesions in visual cortex: Implications for plasticity of high-level vision

“…However, functional neural reorganization such as crossmodal plasticity has often been reported after sensory deprivation: for example, in the blind, ‘visual cortex’ can be activated by tactile stimulation (Büchel, 1998; Sadato et al, 1996), or auditory stimulation (Gougoux et al, 2005; Striem-Amit et al, 2012) or can even be recruited during symbolic math calculation (Kanjlia et al, 2016) or syntactic functions (Lane et al, 2017). In particular, a functional dissociation between a ventral “What” stream for the processing of object shape and a dorsal “Where” stream for the processing of space exists in blind subjects in both the auditory and tactile domain (Amedi et al, 2007; Collignon et al, 2011).…”