Longitudinal stability of individual brain plasticity patterns in blindness.

The primary visual cortex (V1) in blindness is engaged in a wide spectrum of tasks and sensory modalities, including audition, touch, language, and memory. This widespread involvement raises questions regarding the constancy of its role and whether it might exhibit flexibility in its function over time, connecting to diverse network functions specific to task demands. This would suggest that reorganized V1 assumes a role like multiple-demand system regions. Alternatively, varying patterns of plasticity in blind V1 may be attributed to individual factors, with different blind individuals recruiting V1 preferentially for different functions. In support of this, we recently showed that V1 functional connectivity (FC) varies greatly across blind individuals. But do these represent stable individual patterns of plasticity, or are they driven more by instantaneous changes, like a multiple-demand system now inhabiting V1? Here, we tested whether individual FC patterns from the V1 of blind individuals are stable over time. We show that over two years, FC from the V1 is unique and highly stable in a small sample of repeatedly sampled congenitally blind individuals. Further, using multivoxel pattern analysis, we demonstrate that the unique reorganization patterns of these individuals allow decoding of participant identity. Together with recent evidence for substantial individual differences in V1 connectivity, this indicates that there may be a consistent role for V1 in blindness, which may differ for each individual. Further, it suggests that the variability in visual reorganization in blindness across individuals could be used to seek stable neuromarkers for sight rehabilitation and assistive approaches.

Longitudinal stability of individual brain plasticity patterns in blindness.

The primary visual cortex (V1) in individuals born blind is engaged in a wide spectrum of tasks and sensory modalities, including audition, touch, language, and memory. This widespread involvement raises questions regarding the constancy of its role and whether it might exhibit flexibility in its function over time, connecting to diverse network functions in response to task-specific demands. This would suggest that reorganized V1 takes on a role similar to cognitive multiple-demand system regions. Alternatively, it is possible that the varying patterns of plasticity observed in the blind V1 can be attributed to individual factors, whereby different blind individuals recruit V1 for different functions, highlighting the immense idiosyncrasy of plasticity. In support of this second account, we have recently shown that V1 functional connectivity varies greatly across blind individuals. But do these represent stable individual patterns of plasticity or merely instantaneous changes, for a multiple-demand system now inhabiting V1? Here we tested if individual connectivity patterns from the visual cortex of blind individuals are stable over time. We show that over two years, fMRI functional connectivity from the primary visual cortex is unique and highly stable in a small sample of repeatedly sampled congenitally blind individuals. Further, using multivoxel pattern analysis, we demonstrate that the unique reorganization patterns of these individuals allow decoding of participant identity. Together with recent evidence for substantial individual differences in visual cortex connectivity, this indicates there may be a consistent role for the visual cortex in blindness, which may differ for each individual. Further, it suggests that the variability in visual reorganization in blindness across individuals could be used to seek stable neuromarkers for sight rehabilitation and assistive approaches.

Evidence for an effector-independent action system from people born without hands.

Many parts of the visuomotor system guide daily hand actions, like reaching for and grasping objects. Do these regions depend exclusively on the hand as a specific body part whose movement they guide, or are they organized for the reaching task per se, for any body part used as an effector? To address this question, we conducted a neuroimaging study with people born without upper limbs-individuals with dysplasia-who use the feet to act, as they and typically developed controls performed reaching and grasping actions with their dominant effector. Individuals with dysplasia have no prior experience acting with hands, allowing us to control for hand motor imagery when acting with another effector (i.e., foot). Primary sensorimotor cortices showed selectivity for the hand in controls and foot in individuals with dysplasia. Importantly, we found a preference based on action type (reaching/grasping) regardless of the effector used in the association sensorimotor cortex, in the left intraparietal sulcus and dorsal premotor cortex, as well as in the basal ganglia and anterior cerebellum. These areas also showed differential response patterns between action types for both groups. Intermediate areas along a posterior-anterior gradient in the left dorsal premotor cortex gradually transitioned from selectivity based on the body part to selectivity based on the action type. These findings indicate that some visuomotor association areas are organized based on abstract action functions independent of specific sensorimotor parameters, paralleling sensory feature-independence in visual and auditory cortices in people born blind and deaf. Together, they suggest association cortices across action and perception may support specific computations, abstracted from low-level sensorimotor elements.

Plasticity based on compensatory effector use in the association but not primary sensorimotor cortex of people born without hands.

What forces direct brain organization and its plasticity? When brain regions are deprived of their input, which regions reorganize based on compensation for the disability and experience, and which regions show topographically constrained plasticity? People born without hands activate their primary sensorimotor hand region while moving body parts used to compensate for this disability (e.g., their feet). This was taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts, in primary sensorimotor cortex. We tested the selectivity for the compensatory body parts in the primary and association sensorimotor cortex of people born without hands (dysplasic individuals). Despite clear compensatory foot use, the primary sensorimotor hand area in the dysplasic subjects showed preference for adjacent body parts that are not compensatorily used as effectors. This suggests that function-based organization, proposed for congenital blindness and deafness, does not apply to the primary sensorimotor cortex deprivation in dysplasia. These findings stress the roles of neuroanatomical constraints like topographical proximity and connectivity in determining the functional development of primary cortex even in extreme, congenital deprivation. In contrast, increased and selective foot movement preference was found in dysplasics' association cortex in the inferior parietal lobule. This suggests that the typical motor selectivity of this region for manual actions may correspond to high-level action representations that are effector-invariant. These findings reveal limitations to compensatory plasticity and experience in modifying brain organization of early topographical cortex compared with association cortices driven by function-based organization.

Sensorimotor-independent development of hands and tools selectivity in the visual cortex.

The visual occipito-temporal cortex is composed of several distinct regions specialized in the identification of different object kinds such as tools and bodies. Its organization appears to reflect not only the visual characteristics of the inputs but also the behavior that can be achieved with them. For example, there are spatially overlapping responses for viewing hands and tools, which is likely due to their common role in object-directed actions. How dependent is occipito-temporal cortex organization on object manipulation and motor experience? To investigate this question, we studied five individuals born without hands (individuals with upper limb dysplasia), who use tools with their feet. Using fMRI, we found the typical selective hand-tool overlap (HTO) not only in typically developed control participants but also in four of the five dysplasics. Functional connectivity of the HTO in the dysplasics also showed a largely similar pattern as in the controls. The preservation of functional organization in the dysplasics suggests that occipito-temporal cortex specialization is driven largely by inherited connectivity constraints that do not require sensorimotor experience. These findings complement discoveries of intact functional organization of the occipito-temporal cortex in people born blind, supporting an organization largely independent of any one specific sensory or motor experience.