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.

Shared understanding of color among sighted and blind adults.

Empiricist philosophers such as Locke famously argued that people born blind might learn arbitrary color facts (e.g., marigolds are yellow) but would lack color understanding. Contrary to this intuition, we find that blind and sighted adults share causal understanding of color, despite not always agreeing about arbitrary color facts. Relative to sighted people, blind individuals are less likely to generate "yellow" for banana and "red" for stop sign but make similar generative inferences about real and novel objects' colors, and provide similar causal explanations. For example, people infer that two natural kinds (e.g., bananas) and two artifacts with functional colors (e.g., stop signs) are more likely to have the same color than two artifacts with nonfunctional colors (e.g., cars). People develop intuitive and inferentially rich "theories" of color regardless of visual experience. Linguistic communication is more effective at aligning intuitive theories than knowledge of arbitrary facts.

Reading Braille by Touch Recruits Posterior Parietal Cortex.

Blind readers use a tactile reading system consisting of raised dot arrays: braille/⠃⠗⠇. How do human brains implement reading by touch? The current study looked for signatures of reading-specific orthographic processes in braille, separate from low-level somatosensory responses and semantic processes. Of specific interest were responses in posterior parietal cortices (PPCs), because of their role in high-level tactile perception. Congenitally blind, proficient braille readers read real words and pseudowords by touch while undergoing fMRI. We leveraged the system of contractions in English braille, where one braille cell can represent multiple English print letters (e.g., "ing" ⠬, "one" ⠐⠕), making it possible to separate physical and orthographic word length. All words in the study consisted of four braille cells, but their corresponding Roman letter spellings varied from four to seven letters (e.g., "con-c-er-t" ⠒⠉⠻⠞. contracted: four cells; uncontracted: seven letters). We found that the bilateral supramarginal gyrus in the PPC increased its activity as the uncontracted word length increased. By contrast, in the hand region of primary somatosensory cortex (S1), activity increased as a function of a low-level somatosensory feature: dot-number per word. The PPC also showed greater response to pseudowords than real words and distinguished between real and pseudowords in multivariate-pattern analysis. Parieto-occipital, early visual and ventral occipito-temporal, as well as prefrontal cortices also showed sensitivity to the real-versus-pseudoword distinction. We conclude that PPC is involved in orthographic processing for braille, that is, braille character and word recognition, possibly because of braille's tactile modality.

Naturalistic Audio-Movies reveal common spatial organization across "visual" cortices of different blind individuals.

Occipital cortices of different sighted people contain analogous maps of visual information (e.g. foveal vs. peripheral). In congenital blindness, "visual" cortices respond to nonvisual stimuli. Do visual cortices of different blind people represent common informational maps? We leverage naturalistic stimuli and inter-subject pattern similarity analysis to address this question. Blindfolded sighted (n = 22) and congenitally blind (n = 22) participants listened to 6 sound clips (5-7 min each): 3 auditory excerpts from movies; a naturalistic spoken narrative; and matched degraded auditory stimuli (Backwards Speech, scrambled sentences), during functional magnetic resonance imaging scanning. We compared the spatial activity patterns evoked by each unique 10-s segment of the different auditory excerpts across blind and sighted people. Segments of meaningful naturalistic stimuli produced distinctive activity patterns in frontotemporal networks that were shared across blind and across sighted individuals. In the blind group only, segment-specific, cross-subject patterns emerged in visual cortex, but only for meaningful naturalistic stimuli and not Backwards Speech. Spatial patterns of activity within visual cortices are sensitive to time-varying information in meaningful naturalistic auditory stimuli in a broadly similar manner across blind individuals.

Superior verbal but not nonverbal memory in congenital blindness.

Previous studies suggest that people who are congenitally blind outperform sighted people on some memory tasks. Whether blindness-associated memory advantages are specific to verbal materials or are also observed with nonverbal sounds has not been determined. Congenitally blind individuals (n = 20) and age and education matched blindfolded sighted controls (n = 22) performed a series of auditory memory tasks. These included: verbal forward and backward letter spans, a complex letter span with intervening equations, as well as two matched recognition tasks: one with verbal stimuli (i.e., letters) and one with nonverbal complex meaningless sounds. Replicating previously observed findings, blind participants outperformed sighted people on forward and backward letter span tasks. Blind participants also recalled more letters on the complex letter span task despite the interference of intervening equations. Critically, the same blind participants showed larger advantages on the verbal as compared to the nonverbal recognition task. These results suggest that blindness selectively enhances memory for verbal material. Possible explanations for blindness-related verbal memory advantages include blindness-induced memory practice and 'visual' cortex recruitment for verbal processing.

Knowledge of animal appearance among sighted and blind adults.

How does first-person sensory experience contribute to knowledge? Contrary to the suppositions of early empiricist philosophers, people who are born blind know about phenomena that cannot be perceived directly, such as color and light. Exactly what is learned and how remains an open question. We compared knowledge of animal appearance across congenitally blind (n = 20) and sighted individuals (two groups, n = 20 and n = 35) using a battery of tasks, including ordering (size and height), sorting (shape, skin texture, and color), odd-one-out (shape), and feature choice (texture). On all tested dimensions apart from color, sighted and blind individuals showed substantial albeit imperfect agreement, suggesting that linguistic communication and visual perception convey partially redundant appearance information. To test the hypothesis that blind individuals learn about appearance primarily by remembering sighted people's descriptions of what they see (e.g., "elephants are gray"), we measured verbalizability of animal shape, texture, and color in the sighted. Contrary to the learn-from-description hypothesis, blind and sighted groups disagreed most about the appearance dimension that was easiest for sighted people to verbalize: color. Analysis of disagreement patterns across all tasks suggest that blind individuals infer physical features from non-appearance properties of animals such as folk taxonomy and habitat (e.g., bats are textured like mammals but shaped like birds). These findings suggest that in the absence of sensory access, structured appearance knowledge is acquired through inference from ontological kind.

'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.

Naturalistic Audio-Movies and Narrative Synchronize "Visual" Cortices across Congenitally Blind But Not Sighted Individuals.

How does developmental experience, as opposed to intrinsic physiology, shape cortical function? Naturalistic stimuli were used to elicit neural synchrony in individuals blind from birth (n = 18) and those who grew up with sight (n = 18). Blind and blindfolded sighted participants passively listened to three audio-movie clips, an auditory narrative, a sentence shuffled version of the narrative (maintaining language but lacking a plotline), and a version of the narrative backward (lacking both language and plot). For both groups, early auditory cortices were synchronized to a similar degree across stimulus types, whereas higher-cognitive temporoparietal and prefrontal areas were more synchronized by meaningful, temporally extended stimuli (i.e., audio movies and narrative). "Visual" cortices were more synchronized across blind than sighted individuals, but only for audio-movies and narrative. In the blind group, visual cortex synchrony was low for backward speech and intermediate for sentence shuffle. Meaningful auditory stimuli synchronize visual cortices of people born blind.SIGNIFICANCE STATEMENT Naturalistic stimuli engage cognitive processing at many levels. Here, we harnessed this richness to investigate the effect of experience on cortical function. We find that listening to naturalistic audio movies and narrative drives synchronized activity across "visual" cortices of blind, more so than sighted, individuals. Visual cortex synchronization varies with meaningfulness and cognitive complexity. Higher synchrony is observed for temporally extended meaningful stimuli (e.g., movies/narrative), intermediate for shuffled sentences, lowest for time varying complex noise. By contrast, auditory cortex was synchronized equally by meaningful and meaningless stimuli. In congenitally blind individuals most of visual cortex is engaged by meaningful naturalistic stimuli.

A Double Dissociation in Sensitivity to Verb and Noun Semantics Across Cortical Networks.

What is the neural organization of the mental lexicon? Previous research suggests that partially distinct cortical networks are active during verb and noun processing, but what information do these networks represent? We used multivoxel pattern analysis (MVPA) to investigate whether these networks are sensitive to lexicosemantic distinctions among verbs and among nouns and, if so, whether they are more sensitive to distinctions among words in their preferred grammatical class. Participants heard 4 types of verbs (light emission, sound emission, hand-related actions, mouth-related actions) and 4 types of nouns (birds, mammals, manmade places, natural places). As previously shown, the left posterior middle temporal gyrus (LMTG+), and inferior frontal gyrus (LIFG) responded more to verbs, whereas the inferior parietal lobule (LIP), precuneus (LPC), and inferior temporal (LIT) cortex responded more to nouns. MVPA revealed a double-dissociation in lexicosemantic sensitivity: classification was more accurate among verbs than nouns in the LMTG+, and among nouns than verbs in the LIP, LPC, and LIT. However, classification was similar for verbs and nouns in the LIFG, and above chance for the nonpreferred category in all regions. These results suggest that the lexicosemantic information about verbs and nouns is represented in partially nonoverlapping networks.

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.

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.

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.

"Visual" Cortex Responds to Spoken Language in Blind Children.

Plasticity in the visual cortex of blind individuals provides a rare window into the mechanisms of cortical specialization. In the absence of visual input, occipital ("visual") brain regions respond to sound and spoken language. Here, we examined the time course and developmental mechanism of this plasticity in blind children. Nineteen blind and 40 sighted children and adolescents (4-17 years old) listened to stories and two auditory control conditions (unfamiliar foreign speech, and music). We find that "visual" cortices of young blind (but not sighted) children respond to sound. Responses to nonlanguage sounds increased between the ages of 4 and 17. By contrast, occipital responses to spoken language were maximal by age 4 and were not related to Braille learning. These findings suggest that occipital plasticity for spoken language is independent of plasticity for Braille and for sound. We conclude that in the absence of visual input, spoken language colonizes the visual system during brain development. Our findings suggest that early in life, human cortex has a remarkably broad computational capacity. The same cortical tissue can take on visual perception and language functions. SIGNIFICANCE STATEMENT: Studies of plasticity provide key insights into how experience shapes the human brain. The "visual" cortex of adults who are blind from birth responds to touch, sound, and spoken language. To date, all existing studies have been conducted with adults, so little is known about the developmental trajectory of plasticity. We used fMRI to study the emergence of "visual" cortex responses to sound and spoken language in blind children and adolescents. We find that "visual" cortex responses to sound increase between 4 and 17 years of age. By contrast, responses to spoken language are present by 4 years of age and are not related to Braille-learning. These findings suggest that, early in development, human cortex can take on a strikingly wide range of functions.

"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.

Occipital cortex of blind individuals is functionally coupled with executive control areas of frontal cortex.

In congenital blindness, the occipital cortex responds to a range of nonvisual inputs, including tactile, auditory, and linguistic stimuli. Are these changes in functional responses to stimuli accompanied by altered interactions with nonvisual functional networks? To answer this question, we introduce a data-driven method that searches across cortex for functional connectivity differences across groups. Replicating prior work, we find increased fronto-occipital functional connectivity in congenitally blind relative to blindfolded sighted participants. We demonstrate that this heightened connectivity extends over most of occipital cortex but is specific to a subset of regions in the inferior, dorsal, and medial frontal lobe. To assess the functional profile of these frontal areas, we used an n-back working memory task and a sentence comprehension task. We find that, among prefrontal areas with overconnectivity to occipital cortex, one left inferior frontal region responds to language over music. By contrast, the majority of these regions responded to working memory load but not language. These results suggest that in blindness occipital cortex interacts more with working memory systems and raise new questions about the function and mechanism of occipital plasticity.

Shindigs, brunches, and rodeos: the neural basis of event words.

Events (e.g., "running" or "eating") constitute a basic type within human cognition and human language. We asked whether thinking about events, as compared to other conceptual categories, depends on partially independent neural circuits. Indirect evidence for this hypothesis comes from previous studies showing elevated posterior temporal responses to verbs, which typically label events. Neural responses to verbs could, however, be driven either by their grammatical or by their semantic properties. In the present experiment, we separated the effects of grammatical class (verb vs. noun) and semantic category (event vs. object) by measuring neural responses to event nouns (e.g., "the hurricane"). Participants rated the semantic relatedness of event nouns, as well as of two categories of object nouns-animals (e.g., "the alligator") and plants (e.g., "the acorn")-and three categories of verbs-manner of motion (e.g., "to roll"), emission (e.g., "to sparkle"), and perception (e.g., "to gaze"). As has previously been observed, we found larger responses to verbs than to object nouns in the left posterior middle (LMTG) and superior (LSTG) temporal gyri. Crucially, we also found that the LMTG responds more to event than to object nouns. These data suggest that part of the posterior lateral temporal response to verbs is driven by their semantic properties. By contrast, a more superior region, at the junction of the temporal and parietal cortices, responded more to verbs than to all nouns, irrespective of their semantic category. We concluded that the neural mechanisms engaged when thinking about event and object categories are partially dissociable.