Impact of blindness onset on the functional organization and the connectivity of the occipital cortex

Collignon, Olivier; Dormal, Giulia; Albouy, Geneviève; Vandewalle, Gilles; Voss, Patrice; Phillips, Christophe; Leporé, Franco

doi:10.1093/brain/awt176

Cited by 203 publications

(205 citation statements)

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“…Interestingly, similar findings were previously reported in congenitally blind subjects [17,31]. Wiring of neural circuits during development depends on both molecular cues that guide connectivity and activity-dependent mechanisms that use patterned activation to adjust the strength and number of synaptic connections [32].…”

Section: Resultssupporting

confidence: 84%

“…These retinotopic regions [11] are notably involved in motion processing [11] and stereoscopic depth perception [12,13], two abilities that are highly dependent on early binocular visual experience [13,14] and impaired in this cohort of cataract-reversal patients [15,16]. These regions display crossmodal responses to auditory stimulation in adults with early-acquired blindness, but not in adults with late-acquired blindness, a pattern revealing a sensitive period for crossmodal plasticity [17], perhaps related to the rapid myelinization phase of these regions in early infancy [18]. Together, these findings suggest the existence of a regionspecific susceptibility to the effects of transient congenital visual deprivation on crossmodal reorganization.…”

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confidence: 99%

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Long-Lasting Crossmodal Cortical Reorganization Triggered by Brief Postnatal Visual Deprivation

et al. 2015

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Animal and human studies have demonstrated that transient visual deprivation early in life, even for a very short period, permanently alters the response properties of neurons in the visual cortex and leads to corresponding behavioral visual deficits. While it is acknowledged that early-onset and longstanding blindness leads the occipital cortex to respond to non-visual stimulation, it remains unknown whether a short and transient period of postnatal visual deprivation is sufficient to trigger crossmodal reorganization that persists after years of visual experience. In the present study, we characterized brain responses to auditory stimuli in 11 adults who had been deprived of all patterned vision at birth by congenital cataracts in both eyes until they were treated at 9 to 238 days of age. When compared to controls with typical visual experience, the cataract-reversal group showed enhanced auditory-driven activity in focal visual regions. A combination of dynamic causal modeling with Bayesian model selection indicated that this auditory-driven activity in the occipital cortex was better explained by direct cortico-cortical connections with the primary auditory cortex than by subcortical connections. Thus, a short and transient period of visual deprivation early in life leads to enduring large-scale crossmodal reorganization of the brain circuitry typically dedicated to vision.

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Section: Resultssupporting

confidence: 84%

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confidence: 99%

Long-Lasting Crossmodal Cortical Reorganization Triggered by Brief Postnatal Visual Deprivation

et al. 2015

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“…The finding that at least 150 ms of information accumulation is necessary for highlevel individuation of faces in the cortex (22) suggests that the faceselective response in the right dTFA occurs immediately after the initial perceptual encoding of face identity. Similar to our findings, auditory-driven activity in reorganized visual cortex in congenitally blind individuals was also better explained by direct connections with the primary auditory cortex (43) whereas it depended more on feedback inputs from high-level parietal regions in late-onset blindness (43). The crucial role of developmental periods of auditory deprivation in shaping the reorganization of long-range corticocortical connections remains, however, to be determined.…”

Section: Discussionsupporting

confidence: 85%

Functional selectivity for face processing in the temporal voice area of early deaf individuals

Benetti

Ackeren

Rabini

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Brain systems supporting face and voice processing both contribute to the extraction of important information for social interaction (e.g., person identity). How does the brain reorganize when one of these channels is absent? Here, we explore this question by combining behavioral and multimodal neuroimaging measures (magnetoencephalography and functional imaging) in a group of early deaf humans. We show enhanced selective neural response for faces and for individual face coding in a specific region of the auditory cortex that is typically specialized for voice perception in hearing individuals. In this region, selectivity to face signals emerges early in the visual processing hierarchy, shortly after typical face-selective responses in the ventral visual pathway. Functional and effective connectivity analyses suggest reorganization in long-range connections from early visual areas to the face-selective temporal area in individuals with early and profound deafness. Altogether, these observations demonstrate that regions that typically specialize for voice processing in the hearing brain preferentially reorganize for face processing in borndeaf people. Our results support the idea that cross-modal plasticity in the case of early sensory deprivation relates to the original functional specialization of the reorganized brain regions.cross-modal plasticity | deafness | modularity | ventral stream | identity processing T he human brain is endowed with the fundamental ability to adapt its neural circuits in response to experience. Sensory deprivation has long been championed as a model to test how experience interacts with intrinsic constraints to shape functional brain organization. In particular, decades of neuroscientific research have gathered compelling evidence that blindness and deafness are associated with cross-modal recruitment of the sensory-deprived cortices (1). For instance, in early deaf individuals, visual and tactile stimuli induce responses in regions of the cerebral cortex that are sensitive primarily to sounds in the typical hearing brain (2, 3).Animal models of congenital and early deafness suggest that specific visual functions are relocated to discrete regions of the reorganized cortex and that this functional preference in crossmodal recruitment supports superior visual performance. For instance, superior visual motion detection is selectively altered in deaf cats when a portion of the dorsal auditory cortex, specialized for auditory motion processing in the hearing cat, is transiently deactivated (4). These results suggest that cross-modal plasticity associated with early auditory deprivation follows organizational principles that maintain the functional specialization of the colonized brain regions. In humans, however, there is only limited evidence that specific nonauditory inputs are differentially localized to discrete portions of the auditory-deprived cortices. For example, Bola et al. have recently reported, in deaf individuals, cross-modal activations for visual rhythm discrimination in t...

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“…The study of neuroplastic reorganization in blind individuals offers a model through which neuroadaptive processes can be identified. For instance, cross-modal neuroplasticity is a mechanism by which blind individuals recruit visual-related cortices to process sensory information from other perceptual modalities (2)(3)(4)(5). In addition to occipital regions, parietal and frontal multimodal integration regions of blind adults are capable of functional connectivity reorganization (6).…”

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confidence: 99%

Brain circuit–gene expression relationships and neuroplasticity of multisensory cortices in blind children

Ortiz-Terán

Diez

Ortiz

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Sensory deprivation reorganizes neurocircuits in the human brain. The biological basis of such neuroplastic adaptations remains elusive. In this study, we applied two complementary graph theory-based functional connectivity analyses, one to evaluate whole-brain functional connectivity relationships and the second to specifically delineate distributed network connectivity profiles downstream of primary sensory cortices, to investigate neural reorganization in blind children compared with sighted controls. We also examined the relationship between connectivity changes and neuroplasticity-related gene expression profiles in the cerebral cortex. We observed that multisensory integration areas exhibited enhanced functional connectivity in blind children and that this reorganization was spatially associated with the transcription levels of specific members of the cAMP Response Element Binding protein gene family. Using systems-level analyses, this study advances our understanding of human neuroplasticity and its genetic underpinnings following sensory deprivation.blindness | children | neuroplasticity | functional connectivity | CREB family N europlasticity is an intrinsic ability of the brain to modify and rewire itself following experiences (1). The study of neuroplastic reorganization in blind individuals offers a model through which neuroadaptive processes can be identified. For instance, cross-modal neuroplasticity is a mechanism by which blind individuals recruit visual-related cortices to process sensory information from other perceptual modalities (2-5). In addition to occipital regions, parietal and frontal multimodal integration regions of blind adults are capable of functional connectivity reorganization (6). These brain areas are part of a multimodal integration network that acts as a bridge integrating multisensory functions across cortical regions (7). Our group has previously characterized the hierarchical structure and central position of the multimodal integration network in adult blind subjects (6). Although this finding advances our understanding of how information from primary unimodal cortices is adaptively integrated into higher-order associative areas, it remains unclear if neuroplastic changes within multimodal integration areas also occur in blind children. Furthermore, in addition to clarifying the sites of prominent neuroplastic changes, the biological mechanisms through which neuroplastic alterations occur have yet to be fully elucidated in blind individuals.Concurrent advances in cellular and molecular biology and neuroimaging provide a unique opportunity to explore the interlinked relationships between genes and neural circuits (8). A neuroimaging endophenotype is informative because it is more closely related to the genetic end product than clinical or behavioral phenotypes (9). Thus, examining properties of systemslevel brain organization and cortical gene expression has great potential to expand our understanding of neuroplastic mechanisms, particularly if specific gene expression patt...

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Impact of blindness onset on the functional organization and the connectivity of the occipital cortex

Cited by 203 publications

References 91 publications

Long-Lasting Crossmodal Cortical Reorganization Triggered by Brief Postnatal Visual Deprivation

Long-Lasting Crossmodal Cortical Reorganization Triggered by Brief Postnatal Visual Deprivation

Functional selectivity for face processing in the temporal voice area of early deaf individuals

Brain circuit–gene expression relationships and neuroplasticity of multisensory cortices in blind children

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