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

2019 ◽  
Author(s):  
Rashi Pant ◽  
Shipra Kanjlia ◽  
Marina Bedny

ABSTRACTIn congenital blindness, “visual” cortices respond to linguistic information, and fronto-temporal language networks are less left-lateralized. Does this plasticity follow a sensitive period? We tested this by comparing the neural basis of sentence processing in two experiments with adult-onset blind (AB, n=16), congenitally blind (CB, n=22) and blindfolded sighted controls (n=18). In Experiment 1, participants made semantic judgments for spoken sentences and solved math equations in a control condition. In Experiment 2, participants answered “who did what to whom” questions for grammatically complex (with syntactic movement) and grammatically simpler sentences. In a control condition, participants performed a memory task with lists of 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. Crucially, 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 blindness during development modifies the neural basis of language, and this effect follows a sensitive period.

2016 ◽  
Vol 113 (40) ◽  
pp. 11172-11177 ◽  
Author(s):  
Shipra Kanjlia ◽  
Connor Lane ◽  
Lisa Feigenson ◽  
Marina Bedny

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.


2017 ◽  
Vol 29 (1) ◽  
pp. 65-78 ◽  
Author(s):  
Connor Lane ◽  
Shipra Kanjlia ◽  
Hilary Richardson ◽  
Anne Fulton ◽  
Akira Omaki ◽  
...  

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.


2015 ◽  
Vol 27 (8) ◽  
pp. 1633-1647 ◽  
Author(s):  
Ben Deen ◽  
Rebecca Saxe ◽  
Marina Bedny

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.


2018 ◽  
Author(s):  
Shipra Kanjlia ◽  
Rashi Pant ◽  
Marina Bedny

AbstractStudies 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 fronto-parietal 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.


2021 ◽  
Author(s):  
Mengyu Tian ◽  
Elizabeth J. Saccone ◽  
Judy S. Kim ◽  
Shipra Kanjlia ◽  
Marina Bedny

The neural basis of reading is highly consistent across a variety of languages and visual scripts. An unanswered question is whether the sensory modality of symbols influences the neural basis of reading. According to the modality-invariant view, reading depends on the same neural mechanisms regardless of the sensory input modality. Consistent with this idea, previous studies find that the visual word form area (VWFA) within the ventral occipitotemporal cortex (vOTC) is active when blind individuals read Braille by touch. However, connectivity-based theories of brain function suggest that the neural entry point of written symbols (touch vs. vision) may influence the neural architecture of reading. We compared the neural basis of the visual print (sighted n=15) and tactile Braille (congenitally blind n=19) in proficient readers using analogous reading and listening tasks. Written stimuli varied in word-likeness from real words to consonant strings and non-letter shape strings. Auditory stimuli consisted of words and backward speech sounds. Consistent with prior work, vOTC was active during Braille and visual reading. However, in sighted readers, visual print elicited a posterior/anterior vOTC word-form gradient: anterior vOTC preferred larger orthographic units (words), middle vOTC preferring consonant strings, and posterior vOTC responded to shapes (i.e., lower-level physical features). No such gradient was observed in blind readers of Braille. Consistent with connectivity predictions, in blind Braille readers, posterior parietal cortices (PPC) and parieto-occipital areas were recruited to a greater degree and PPC contained word-preferring patches. Lateralization of Braille in blind readers was predicted by laterality of spoken language, as well as by reading hand. These results suggested that the neural basis of reading is influenced by symbol modality and support connectivity-based views of cortical function.


2021 ◽  
Author(s):  
Elizabeth Musz ◽  
Rita Loiotile ◽  
Janice Chen ◽  
Marina Bedny

AbstractOccipital cortices of different sighted people contain analogous maps of visual information (e.g., foveal vs. peripheral space). In congenital blindness, “visual” cortices enhance responses to nonvisual stimuli. Do deafferented visual cortices of different blind people represent common informational maps? We leverage a naturalistic stimulus paradigm and inter-subject pattern similarity analysis to address this question. Blindfolded sighted (S, n=22) and congenitally blind (CB, n=22) participants listened to three auditory excerpts from movies; a naturalistic spoken narrative; and matched degraded auditory stimuli (i.e., shuffled sentences and backwards speech) while undergoing fMRI scanning. In a parcel-based whole brain analysis, we measured the spatial activity patterns evoked by each unique, ten-second segment of each auditory clip. We then compared each subject’s spatial pattern to that of all other subjects in the same group (CB or S) within and across segments. In both blind and sighted groups, segments of meaningful auditory stimuli produced distinctive patterns of activity that were shared across individuals. Crucially, only in the CB group, this segment-specific, cross-subject pattern similarity effect emerged in visual cortex, but only for meaningful naturalistic stimuli and not backwards speech. These results suggest that spatial activity patterns within deafferented visual cortices encode meaningful, segment-level information contained in naturalistic auditory stimuli, and that these representations are spatially organized in a similar fashion across blind individuals.Significance StatementRecent neuroimaging studies show that the so-called “visual” cortices activate during non-visual tasks in people who are born blind. Do the visual cortices of people who are born blind develop similar representational maps? While congenitally blind individuals listened to naturalistic auditory stimuli (i.e., sound clips from movies), distinct timepoints within each stimulus elicited unique spatial activity patterns in visual cortex, and these patterns were shared across different people. These findings suggest that in blindness, the visual cortices encode meaningful information embedded in naturalistic auditory signals in a spatially distributed manner, and that a common representational map can emerge in visual cortex independent of visual experience.


2018 ◽  
Author(s):  
Rita E. Loiotile ◽  
Marina Bedny

AbstractHow functionally flexible is human cortex? In congenitally blind individuals, “visual” cortices are active during auditory and tactile tasks. The cognitive role of these responses and the underlying mechanisms remain uncertain. A dominant view is that, in blindness, “visual” cortices process information from low-level auditory and somatosensory systems. An alternative hypothesis is that higher-cognitive fronto-parietal systems take over “visual” cortices. We report that, in congenitally blind individuals, right-lateralized “visual” cortex responds to executiveload in a go/no-go task. These right-lateralized occipital cortices of blind, but not sighted, individuals mirrored the executive-function pattern observed in fronto-parietal systems. In blindness, the same “visual” cortex area, at rest, also increases its synchronization with prefrontal executive control regions and decreases its synchronization with auditory and sensorimotor cortices. These results support the hypothesis of top-down fronto-parietal takeover of “visual” cortices, and suggest that human cortex is highly flexible at birth.


2019 ◽  
Author(s):  
Shipra Kanjlia ◽  
Lisa Feigenson ◽  
Marina Bedny

AbstractThinking about numerical quantities is an integral part of daily human life that is supported by the intraparietal sulcus (IPS). The IPS is recruited during mathematical calculation and neuronal populations within the IPS code for the quantity of items in a set. Is the developmental basis of IPS number representations rooted in visual experience? We asked if the IPS possesses population codes for auditory quantities in sighted individuals and, critically, whether it does in the absence of any visual experience in congenitally blind individuals. We found that sequences of 4, 8, 16 and 32 tones each elicited unique patterns of fMRI activity in the IPS of both sighted and congenitally blind individuals, such that the quantity a participant heard on a given trial could be reliably predicted based on the pattern of observed IPS activity. This finding suggests that the IPS number system is resilient to dramatic changes in sensory experience.


2021 ◽  
Author(s):  
Elizabeth Musz ◽  
Rita Loiotile ◽  
Janice Chen ◽  
Rhodri Cusack ◽  
Marina Bedny

AbstractHow do life experiences impact cortical function? In people who are born blind, the “visual” cortices are recruited for nonvisual tasks such as Braille reading and sound localization (e.g., Collignon et al., 2011; Sadato et al., 1996). The mechanisms of this recruitment are not known. Do visual cortices have a latent capacity to respond to nonvisual information that is equal throughout the lifespan? Alternatively, is there a sensitive period of heightened plasticity that makes visual cortex repurposing possible during childhood? To gain insight into these questions, we leveraged naturalistic auditory stimuli to quantify and compare cross-modal responses congenitally blind (CB, n=22), adult-onset blind (vision loss >18 years-of-age, AB, n=14) and sighted (n=22) individuals. Participants listened to auditory excerpts from movies; a spoken narrative; and matched meaningless auditory stimuli (i.e., shuffled sentences, backwards speech) during fMRI scanning. These rich naturalistic stimuli made it possible to simultaneous engage a broad range of cognitive domains. We correlated the voxel-wise timecourses of different participants within each group. For all groups, all stimulus conditions induced synchrony in auditory cortex and for all groups only the narrative stimuli synchronized responses in higher-cognitive fronto-parietal and temporal regions. Inter-subject synchrony in visual cortices was high in the CB group for the movie and narrative stimuli but not for meaningless auditory controls. In contrast, visual cortex synchrony was equally low among AB and sighted blindfolded participants. Even many years of blindness in adulthood fail to enable responses to naturalistic auditory information in visual cortices of people who had sight as children. These findings suggest that cross-modal responses in visual cortex of people born blind reflect the plasticity of developing visual cortex during a sensitive period.


2017 ◽  
Vol 114 (23) ◽  
pp. 6139-6143 ◽  
Author(s):  
Tapan K. Gandhi ◽  
Amy Kalia Singh ◽  
Piyush Swami ◽  
Suma Ganesh ◽  
Pawan Sinha

It is unknown whether the ability to visually distinguish between faces and nonfaces is subject to a critical period during development. Would a congenitally blind child who gains sight several years after birth be able to acquire this skill? This question has remained unanswered because of the rarity of cases of late sight onset. We had the opportunity to work with five early-blind individuals who gained sight late in childhood after treatment for dense bilateral cataracts. We tested their ability to categorize patterns as faces, using natural images that spanned a spectrum of face semblance. The results show that newly sighted individuals are unable to distinguish between faces and nonfaces immediately after sight onset, but improve markedly in the following months. These results demonstrate preserved plasticity for acquiring face/nonface categorization ability even late in life, and set the stage for investigating the informational and neural basis of this skill acquisition.


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