Neural specialization for 'visual' concepts emerges in the absence of vision.

Vision provides a key source of information about many concepts, including 'living things' (e.g., tiger) and visual events (e.g., sparkle). According to a prominent theoretical framework, neural specialization for different conceptual categories is shaped by sensory features, e.g., living things are neurally dissociable from navigable places because living things concepts depend more on visual features. We tested this framework by comparing the neural basis of 'visual' concepts across sighted (n=22) and congenitally blind (n=21) adults. Participants judged the similarity of words varying in their reliance on vision while undergoing fMRI. We compared neural responses to living things nouns (birds, mammals) and place nouns (natural, manmade). In addition, we compared visual event verbs (e.g., 'sparkle') to non-visual events (sound emission, hand motion, mouth motion). People born blind exhibited distinctive univariate and multivariate responses to living things in a temporo-parietal semantic network activated by nouns, including the precuneus (PC). To our knowledge, this is the first demonstration that neural selectivity for living things does not require vision. We additionally observed preserved neural signatures of 'visual' light events in the left middle temporal gyrus (LMTG+). Across a wide range of semantic types, neural representations of sensory concepts develop independent of sensory experience.

Stimulus-evoked and resting-state alpha oscillations show a linked dependence on patterned visual experience for development.

Persistent visual impairments after congenital blindness due to dense bilateral cataracts have been attributed to altered visual cortex development within a sensitive period. Occipital alpha (8-14 Hz) oscillations were found to be reduced after congenital cataract reversal, while participants performed visual motion tasks. However, it has been unclear whether reduced alpha oscillations were task-specific, or linked to impaired visual behavior in cataract-reversed individuals. Here, we compared resting-state and stimulus-evoked alpha activity between individuals who had been treated for dense bilateral congenital cataracts (CC, n = 13, mean duration of blindness = 11.0 years) and age-matched, normally sighted individuals (SC, n = 13). We employed the visual impulse response function, adapted from VanRullen and MacDonald (2012), to test for the characteristic alpha response to visual white noise. Participants observed white noise stimuli changing in luminance with equal power at frequencies between 0 and 30 Hz. Compared to SC individuals, CC individuals demonstrated a reduced likelihood of exhibiting an evoked alpha response. Moreover, stimulus-evoked alpha power was reduced and correlated with a corresponding reduction of resting-state alpha power in the same CC individuals. Finally, CC individuals with an above-threshold evoked alpha peak had better visual acuity than CC individual without an evoked alpha peak. Since alpha oscillations have been linked to feedback communication, we suggest that the concurrent impairment in resting-state and stimulus-evoked alpha oscillations indicates an altered interaction of top-down and bottom-up processing in the visual hierarchy, which likely contributes to incomplete behavioral recovery in individuals who experienced transient congenital blindness.

The size-weight illusion is unimpaired in individuals with a history of congenital visual deprivation.

Visual deprivation in childhood can lead to lifelong impairments in multisensory processing. Here, the Size-Weight Illusion (SWI) was used to test whether visuo-haptic integration recovers after early visual deprivation. Normally sighted individuals perceive larger objects to be lighter than smaller objects of the same weight. In Experiment 1, individuals treated for dense bilateral congenital cataracts (who had no patterned visual experience at birth), individuals treated for developmental cataracts (who had patterned visual experience at birth, but were visually impaired), congenitally blind individuals and normally sighted individuals had to rate the weight of manually explored cubes that differed in size (Small, Medium, Large) across two possible weights (350 g, 700 g). In Experiment 2, individuals treated for dense bilateral congenital cataracts were compared to sighted individuals in a similar task using a string set-up, which removed haptic size cues. In both experiments, indistinguishable SWI effects were observed across all groups. These results provide evidence that early aberrant vision does not interfere with the development of the SWI, and suggest a recovery of the integration of size and weight cues provided by the visual and haptic modality.

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

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.

Sensitive Period for Cognitive Repurposing of Human Visual Cortex.

Studies of sensory loss are a model for understanding the functional flexibility of human cortex. In congenital blindness, subsets of visual cortex are recruited during higher-cognitive tasks, such as language and math tasks. Is such dramatic functional repurposing possible throughout the lifespan or restricted to sensitive periods in development? We compared visual cortex function in individuals who lost their vision as adults (after age 17) to congenitally blind and sighted blindfolded adults. Participants took part in resting-state and task-based fMRI scans during which they solved math equations of varying difficulty and judged the meanings of sentences. Blindness at any age caused "visual" cortices to synchronize with specific frontoparietal networks at rest. However, in task-based data, visual cortices showed regional specialization for math and language and load-dependent activity only in congenital blindness. Thus, despite the presence of long-range functional connectivity, cognitive repurposing of human cortex is limited by sensitive periods.