Sensory modality and spoken language shape reading network in blind readers of Braille.

The neural basis of reading is highly consistent across many languages and scripts. Are there alternative neural routes to reading? How does the sensory modality of symbols (tactile vs. visual) influence their neural representations? We examined these questions by comparing reading of visual print (sighted group, n = 19) and tactile Braille (congenitally blind group, n = 19). Blind and sighted readers were presented with written (words, consonant strings, non-letter shapes) and spoken stimuli (words, backward speech) that varied in word-likeness. Consistent with prior work, the ventral occipitotemporal cortex (vOTC) was active during Braille and visual reading. A posterior/anterior vOTC word-form gradient was observed only in sighted readers with more anterior regions preferring larger orthographic units (words). No such gradient was observed in blind readers. Consistent with connectivity predictions, in blind compared to sighted readers, posterior parietal cortices were recruited to a greater degree and contained word-preferring patches. Lateralization of Braille in blind readers was predicted by laterality of spoken language and reading hand. The effect of spoken language increased along a cortical hierarchy, whereas effect of reading hand waned. These results suggested that the neural basis of reading is influenced by symbol modality and spoken language and support connectivity-based views of cortical function.

Neural basis of approximate number in congenital blindness.

Although humans are unique among animals in their ability to manipulate symbolic numbers, we share with other species an approximate number sense that allows us to estimate and compare the number of objects or events in a set, such as the number of apples in a tree. Our ability to discriminate the numerosity of two sets decreases as the ratio between them becomes smaller (e.g., 8 vs 16 items is harder to discriminate than 8 vs 32 items). The intraparietal sulcus (IPS) plays a key role in this numerical approximation. Neuronal populations within the IPS code for numerosity, with stimuli of different numerosities eliciting discriminable spatial patterns of activity. The developmental origins of these IPS number representations are not known. Here, we tested the hypothesis that representations of number in the IPS require visual experience with object sets, by working with individuals blind from birth. While undergoing fMRI, congenitally blind (n = 17) and blindfolded sighted (n = 25) participants judged which of two sequences of beeps was more numerous. In both sighted and blind individuals, patterns of activity in the IPS discriminated among different numerosities (4, 8, 16 vs 32), with better discrimination in the IPS of the blind group. In both groups, decoding performance decreased as the ratio between numerosities decreased (e.g., 8 vs 16 was less discriminable than 8 vs 32). These findings suggest that number representations in the IPS either have innate precursors, or that auditory or tactile experience with sets is sufficient for typical development.

'Visual' cortices of congenitally blind adults are sensitive to response selection demands in a go/no-go task.

Studies of occipital cortex plasticity in blindness provide insight into how intrinsic constraints interact with experience to determine cortical specialization. We tested the cognitive nature and anatomical origins of occipital responses during non-verbal, non-spatial auditory tasks. In a go/no-go task, congenitally blind (N=23) and sighted (N=24) individuals heard rapidly occurring (<1/s) non-verbal sounds and made one of two button presses (frequent-go 50%, infrequent-go 25%) or withheld a response (no-go, 25%). Rapid and frequent button presses heighten response selection/inhibition demands on the no-go trials: In sighted and blind adults a right-lateralized prefrontal (PFC) network responded most to no-go trials, followed by infrequent-go and finally frequent-go trials. In the blind group only, a right-lateralized occipital network showed the same response profile and the laterality of occipital and PFC responses was correlated across blind individuals. A second experiment with spoken sentences and equations (N=16) found that no-go responses in occipital cortex are distinct from previously identified occipital responses to spoken language. Finally, in resting-state data (N=30 blind, N=31 blindfolded sighted), no-go responsive 'visual' cortex of blind relative to sighted participants was more synchronized with PFC and less synchronized with primary auditory and sensory-motor cortices. No-go responsive occipital cortex showed higher resting-state correlations with no-go responsive PFC than language responsive inferior frontal cortex. We conclude that in blindness, a right-lateralized occipital network responds to non-verbal executive processes, including response selection. These results suggest that connectivity with fronto-parietal executive networks is a key mechanism for plasticity in blindness.

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.

Cues to individuation facilitate 6-month-old infants' visual short-term memory.

Infants' ability to perform visual short-term memory (VSTM) tasks develops rapidly between 6 and 8 months. Here we tested the hypothesis that infants' VSTM performance is influenced by their ability to individuate simultaneously presented objects. We used a one-shot change detection task to ask whether 6-month-old infants (N = 47) would detect a change in the color of 1 item in a 2-item array when the stimulus context facilitated individuation of the items. In Experiment 1 the 2 items in the display differed in shape and color and in Experiment 2 the onset and offset times of the 2 items differed. In both experiments, 6-month-old infants detected a change, contrasting with previous results. Thus, young infants' encoding of information about individual items in multiple-item arrays is related to their ability to individuate those items. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

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.

Numerical cognition is resilient to dramatic changes in early sensory experience.

Humans and non-human animals can approximate large visual quantities without counting. The approximate number representations underlying this ability are noisy, with the amount of noise proportional to the quantity being represented. Numerate humans also have access to a separate system for representing exact quantities using number symbols and words; it is this second, exact system that supports most of formal mathematics. Although numerical approximation abilities and symbolic number abilities are distinct in representational format and in their phylogenetic and ontogenetic histories, they appear to be linked throughout development--individuals who can more precisely discriminate quantities without counting are better at math. The origins of this relationship are debated. On the one hand, symbolic number abilities may be directly linked to, perhaps even rooted in, numerical approximation abilities. On the other hand, the relationship between the two systems may simply reflect their independent relationships with visual abilities. To test this possibility, we asked whether approximate number and symbolic math abilities are linked in congenitally blind individuals who have never experienced visual sets or used visual strategies to learn math. Congenitally blind and blind-folded sighted participants completed an auditory numerical approximation task, as well as a symbolic arithmetic task and non-math control tasks. We found that the precision of approximate number representations was identical across congenitally blind and sighted groups, suggesting that the development of the Approximate Number System (ANS) does not depend on visual experience. Crucially, the relationship between numerical approximation and symbolic math abilities is preserved in congenitally blind individuals. These data support the idea that the Approximate Number System and symbolic number abilities are intrinsically linked, rather than indirectly linked through visual abilities.

An eye tracking investigation of color-location binding in infants' visual short-term memory.

Two experiments examined 8- and 10-month-old infants' (N = 71) binding of object identity (color) and location information in visual short-term memory (VSTM) using a one-shot change detection task. Building on previous work using the simultaneous streams change detection task, we confirmed that 8- and 10-month-old infants are sensitive to changes in binding between identity and location in VSTM. Further, we demonstrated that infants recognize specifically what changed in these events. Thus, infants' VSTM for binding is robust and can be observed in different procedures and with different stimuli.

Development of the Visual Word Form Area Requires Visual Experience: Evidence from Blind Braille Readers.

Learning to read causes the development of a letter- and word-selective region known as the visual word form area (VWFA) within the human ventral visual object stream. Why does a reading-selective region develop at this anatomical location? According to one hypothesis, the VWFA develops at the nexus of visual inputs from retinotopic cortices and linguistic input from the frontotemporal language network because reading involves extracting linguistic information from visual symbols. Surprisingly, the anatomical location of the VWFA is also active when blind individuals read Braille by touch, suggesting that vision is not required for the development of the VWFA. In this study, we tested the alternative prediction that VWFA development is in fact influenced by visual experience. We predicted that in the absence of vision, the "VWFA" is incorporated into the frontotemporal language network and participates in high-level language processing. Congenitally blind (n = 10, 9 female, 1 male) and sighted control (n = 15, 9 female, 6 male), male and female participants each took part in two functional magnetic resonance imaging experiments: (1) word reading (Braille for blind and print for sighted participants), and (2) listening to spoken sentences of different grammatical complexity (both groups). We find that in blind, but not sighted participants, the anatomical location of the VWFA responds both to written words and to the grammatical complexity of spoken sentences. This suggests that in blindness, this region takes on high-level linguistic functions, becoming less selective for reading. More generally, the current findings suggest that experience during development has a major effect on functional specialization in the human cortex.SIGNIFICANCE STATEMENT The visual word form area (VWFA) is a region in the human cortex that becomes specialized for the recognition of written letters and words. Why does this particular brain region become specialized for reading? We tested the hypothesis that the VWFA develops within the ventral visual stream because reading involves extracting linguistic information from visual symbols. Consistent with this hypothesis, we find that in congenitally blind Braille readers, but not sighted readers of print, the VWFA region is active during grammatical processing of spoken sentences. These results suggest that visual experience contributes to VWFA specialization, and that different neural implementations of reading are possible.

Reduced Left Lateralization of Language in Congenitally Blind Individuals.

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.

Absence of visual experience modifies the neural basis of numerical thinking.

In humans, the ability to reason about mathematical quantities depends on a frontoparietal network that includes the intraparietal sulcus (IPS). How do nature and nurture give rise to the neurobiology of numerical cognition? We asked how visual experience shapes the neural basis of numerical thinking by studying numerical cognition in congenitally blind individuals. Blind (n = 17) and blindfolded sighted (n = 19) participants solved math equations that varied in difficulty (e.g., 27 - 12 = x vs. 7 - 2 = x), and performed a control sentence comprehension task while undergoing fMRI. Whole-cortex analyses revealed that in both blind and sighted participants, the IPS and dorsolateral prefrontal cortices were more active during the math task than the language task, and activity in the IPS increased parametrically with equation difficulty. Thus, the classic frontoparietal number network is preserved in the total absence of visual experience. However, surprisingly, blind but not sighted individuals additionally recruited a subset of early visual areas during symbolic math calculation. The functional profile of these "visual" regions was identical to that of the IPS in blind but not sighted individuals. Furthermore, in blindness, number-responsive visual cortices exhibited increased functional connectivity with prefrontal and IPS regions that process numbers. We conclude that the frontoparietal number network develops independently of visual experience. In blindness, this number network colonizes parts of deafferented visual cortex. These results suggest that human cortex is highly functionally flexible early in life, and point to frontoparietal input as a mechanism of cross-modal plasticity in blindness.

How feedback improves children's numerical estimation.

Developmental change in children's number-line estimation has been thought to reveal a categorical logarithmic-to-linear shift in mental representations of number. Some have claimed that the broad and rapid change in estimation patterns that occurs with corrective feedback provides strong evidence for this shift. However, quantitative models of proportion judgment may provide a better account of children's estimation patterns while also predicting broad and rapid change following feedback. Here we test the hypothesis that local corrective feedback provides children with additional reference points, rather than catalyzing a shift to a different mental representation of number. We tested 117 children from several second-grade classrooms in a number-line feedback study. Data indicate that the proportion-judgment framework accounts for individual differences in estimation patterns, and that the effects of feedback are consistent with the unique quantitative predictions of the framework. They do not provide evidence supporting the representational shift hypothesis or, more broadly, for the proposal that cognitive change can occur rapidly at the level of entire mental representations.

"Visual" Cortex of Congenitally Blind Adults Responds to Syntactic Movement.

Human cortex is comprised of specialized networks that support functions, such as visual motion perception and language processing. How do genes and experience contribute to this specialization? Studies of plasticity offer unique insights into this question. In congenitally blind individuals, "visual" cortex responds to auditory and tactile stimuli. Remarkably, recent evidence suggests that occipital areas participate in language processing. We asked whether in blindness, occipital cortices: (1) develop domain-specific responses to language and (2) respond to a highly specialized aspect of language-syntactic movement. Nineteen congenitally blind and 18 sighted participants took part in two fMRI experiments. We report that in congenitally blind individuals, but not in sighted controls, "visual" cortex is more active during sentence comprehension than during a sequence memory task with nonwords, or a symbolic math task. This suggests that areas of occipital cortex become selective for language, relative to other similar higher-cognitive tasks. Crucially, we find that these occipital areas respond more to sentences with syntactic movement but do not respond to the difficulty of math equations. We conclude that regions within the visual cortex of blind adults are involved in syntactic processing. Our findings suggest that the cognitive function of human cortical areas is largely determined by input during development. SIGNIFICANCE STATEMENT: Human cortex is made up of specialized regions that perform different functions, such as visual motion perception and language processing. How do genes and experience contribute to this specialization? Studies of plasticity show that cortical areas can change function from one sensory modality to another. Here we demonstrate that input during development can alter cortical function even more dramatically. In blindness a subset of "visual" areas becomes specialized for language processing. Crucially, we find that the same "visual" areas respond to a highly specialized and uniquely human aspect of language-syntactic movement. These data suggest that human cortex has broad functional capacity during development, and input plays a major role in determining functional specialization.