bioRxiv Science⌕ Search

Biology subjects

Striem-Amit, E.

Publications and source records attributed to Striem-Amit, E..

9 recordsLinked to original sources

From Hands to Feet: Experience-Driven Plasticity in Secondary Somatosensory Cortex in People Born without Hands

In congenital handlessness, where individuals rely on their feet for compensatory manual functions, reorganization in the primary somatosensory cortex (SI) appears limited to local shifts by adjacent body parts. It remains unclear how congenital handlessness and lifelong compensatory foot use shape the sensorimotor system beyond SI, and whether compensatory abilities can drive broader functional reorganization. Here, we used task-based and resting-state functional magnetic resonance imaging (fMRI) to investigate how compensatory foot use changes body representations in the secondary somatosensory cortex (SII) in people born without hands (individuals with upper-limb dysplasia, IDs). We found that IDs showed foot selectivity in the left hand-selective SII, with stronger foot activity than typically-developed (TD) control participants during action execution. Notably, this reorganization in the left SII hand area cannot simply be explained by this areas intrinsic organization - the typical secondary preference of this area in the TDs when hand responses are excluded, as this area in TDs shows shoulder - but not foot - selectivity when the hand activity is excluded. This indicates a functional reorganization dependent on the IDs sensorimotor experience. Resting-state results further revealed altered functional connectivity between SII and primary sensorimotor regions in IDs. Our findings suggest that SII exhibits flexible, experience-dependent plasticity, revealing a hierarchical principle of cortical plasticity, whereby reorganization in the SI is constrained by somatotopic principles while SII reflects functionally or experience-dependent plasticity.

neuroscience↗

Unraveling the impact of congenital deafness on individual brain organization

Research on brain plasticity, particularly in the context of deafness, consistently emphasizes the reorganization of the auditory cortex. However, a critical question arises: to what extent do all individuals with deafness show the same level of reorganization? To address this question, we examined the individual differences in deafness functional connectivity (FC), specifically from the deprived auditory cortex. Our findings demonstrate a remarkable differentiation between individuals deriving from the absence of shared auditory experiences, resulting in heightened FC variability among deaf individuals, compared to more consistent FC in the hearing group. Notably, connectivity to language regions becomes more diverse across individuals in deafness. This does not stem from delayed language acquisition, as it is found in deaf native signers, who are exposed to rich natural language since birth. However, comparing FC diversity between deaf native signers and deaf delayed signers who were deprived of language in early development, we show that language experience also impacts individual differences, although to a more moderate extent. Overall, our research points out the intricate interplay between brain plasticity and individual differences, shedding light on the diverse ways reorganization manifests among individuals. It further joins findings in blindness, showing that individual differences are affected by sensory experience. Finally, these findings highlight the importance of considering individual differences in personalized rehabilitation for hearing loss.

neuroscience↗

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.

neuroscience↗

Are reaching and grasping effector-independent? Similarities and differences in reaching and grasping kinematics between the hand and foot

While reaching and grasping are highly prevalent manual actions, neuroimaging studies provide evidence that their neural representations may be shared between different body parts, i.e. effectors. If these actions are guided by effector-independent mechanisms, similar kinematics should be observed when the action is performed by the hand or by a cortically remote and less experienced effector, such as the foot. We tested this hypothesis with two characteristic components of action: the initial ballistic stage of reaching, and the preshaping of the digits during grasping based on object size. We examined if these kinematic features reflect effector-independent mechanisms by asking participants to reach toward and to grasp objects of different widths with their hand and foot. First, during both reaching and grasping, the velocity profile up to peak velocity matched between the hand and the foot, indicating a shared ballistic acceleration phase. Secondly, maximum grip aperture and time of maximum grip aperture of grasping increased with object size for both effectors, indicating encoding of object size during transport. Differences between the hand and foot were found in the deceleration phase and time of maximum grip aperture, likely due to biomechanical differences and the participants inexperience with foot actions. These findings provide evidence for effector-independent visuomotor mechanisms of reaching and grasping that generalize across body parts.

animal behavior and cognition↗

The role of visual experience in brain inter-individual variability

Visual cortex organization is highly consistent across individuals. But to what degree does this consistency depend on life experience, in particular sensory experience? In this study, we asked whether visual cortex reorganization in congenital blindness results in connectivity patterns that are particularly variable across individuals, focusing on resting-state functional connectivity (RSFC) patterns from primary visual cortex. We show that the absence of shared visual experience results in more-variable RSFC patterns across blind individuals than sighted controls. Increased variability is specifically found in areas that show a group difference between the blind and sighted in their RSFC. These findings reveal a relationship between brain plasticity and individual variability in which reorganization manifests variably across individuals. We further investigated the different patterns of reorganization in the blind, showing that the connectivity to frontal regions, proposed to have a role in reorganization of the visual cortex of the blind towards higher cognitive roles, is highly variable. In a supplementary analysis, we link some of the variability in visual-to-frontal connectivity to another environmental factor - duration of formal education. Together, these findings show a role of sensory and socioeconomic experience in imposing consistency on brain organization. By revealing the idiosyncratic nature of neural reorganization, these findings highlight the importance of considering individual differences in fitting sensory aids and restoration approaches for vision loss. Significance statementThe typical visual system is highly consistent across individuals. What are the origins of this consistency? Comparing the consistency of visual cortex connectivity between people born blind and sighted people, we showed that blindness results in higher variability, suggesting a key impact of individual experience on brain organization. Further, connectivity patterns that changed following blindness were particularly variable, resulting in diverse patterns of brain reorganization. Individual differences in reorganization were also directly affected by non-visual experiences in the blind (years of formal education). Together, these findings show a role of sensory and socioeconomic experiences in creating individual differences in brain organization and endorse the use of individual profiles for rehabilitation and restoration of vision loss.

neuroscience↗

Spoken language comprehension activates the primary visual cortex

Primary visual cortex (V1) is generally thought of as a low-level sensory area that primarily processes basic visual features. However, in congenitally blind individuals, V1 is involved in language processing, with no evidence of major changes in anatomical connectivity that could explain this seemingly drastic functional change. This is at odds with current accounts of neural plasticity, which emphasize the role of connectivity and conserved function in determining a neural tissues role even after atypical early experiences. To reconcile what appears to be unprecedented functional reorganization with known accounts of plasticity limitations, we tested whether V1 also responds to spoken language in sighted individuals. Using fMRI, we found that V1 in normally sighted individuals was indeed activated by comprehensible speech as compared to a reversed speech control condition, in a left-lateralized and focal manner. Activation in V1 for language was also significant and comparable for abstract and concrete words, suggesting it was not driven by visual imagery. Last, this activation did not stem from increased attention to the auditory onset of words, excluding general attention accounts. Together these findings suggest that V1 responds to verbal information even in sighted individuals, potentially to predict visual input. This capability might be the basis for the strong V1 language activation observed in people born blind, re-affirming the notion that plasticity is guided by pre-existing connectivity and abilities in the typically developed brain. Significance statementHow flexible is the human brain? Studies of congenitally blind individuals showed that language activates the primary visual cortex. This has been interpreted as evidence for unprecedented functional plasticity from a low-level visual to a language area. To reconcile these findings with known limitations of plasticity based on intrinsic physiology and connectivity, we tested if similar activation can be found in sighted participants. We show that left-lateralized primary visual cortex is activated by spoken language comprehension in sighted individuals, . This suggests that plasticity even in complete blindness from birth is not limitless and is guided by pre-existing connectivity and abilities in the typically-developed brain.

neuroscience↗

Large-scale organization of the hand action observation network in individuals born without hands

The human high-level visual cortex comprises regions specialized for the processing of distinct types of stimuli, such as objects, animals, and human actions. How does this specialization emerge? Here, we investigated the role of sensorimotor experience in shaping the organization of the action observation network as a window on this question. Observed body movements are frequently coupled with corresponding motor codes, e.g. during monitoring ones own movements and imitation, resulting in bidirectionally connected circuits between areas involved in body movements observation (e.g., of the hand) and the motor codes involved in their execution. If the organization of the action observation network is shaped by this sensorimotor coupling, then, it should not form for body movements that do not belong to individuals motor repertoire. To test this prediction, we used fMRI to investigate the spatial arrangement and functional properties of the hand and foot action observation circuits in individuals born without upper limbs. Multivoxel pattern decoding, pattern similarity, and univariate analyses revealed an intact hand action observation network in the individuals born without upper limbs. This suggests that the organization of the action observation network does not require effector-specific visuomotor coupling.

neuroscience↗

How do blind people represent rainbows? Disentangling components of conceptual representations.

How do we represent information that has no sensory features? How are abstract concepts like \"freedom\", devoid of external perceptible referents, represented in the brain? To address the role of sensory information in the neural representation of concepts, we investigated how people born blind process concepts whose referents are imperceptible to them because of their visual nature (e.g. \"rainbow\", or \"red\"). We find that the left dorsal anterior temporal lobe (ATL) shows preference both to typical abstract concepts (\"freedom\") and to concepts whose referents are not sensorially-available to the blind (\"rainbow\"), as compared to partially sensorially-perceptible referents (e.g. \"rain\"). Activation pattern similarity in dorsal ATL is related to the sensorial-accessibility ratings of the concepts in the blind. Parts of inferior-lateral aspects of ATL and the temporal pole responded preferentially to abstract concepts devoid of any external referents (\"freedom\") relative to imperceptible objects, in effect distinguishing between object and non-object concepts. The medial ATL showed a preference for concrete concepts (\"cup\"), along with a preference for partly perceptible items to the blind (\"rain\", as compared with \"rainbow\"), indicating this regions role in representing concepts with sensory referents beyond vision. The findings point to a new division of labor among medial, dorsal and lateral aspects of ATL in representing different properties of object and non-object concepts.

neuroscience↗

Limitations of compensatory plasticity: the organization of the primary sensorimotor cortex in foot-using bilateral upper limb dysplasics

What forces direct brain organization and its plasticity? When a brain region is deprived of its input would this region reorganize based on compensation for the disability and experience, or would strong limitations of brain structure limit its plasticity? People born without hands activate their sensorimotor hand region while moving body parts used to compensate for this ability (e.g. their feet). This has been taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts. Here we test the selectivity for functionally-compensatory body parts in the sensorimotor cortex of people born without hands. Despite clear compensatory foot use, the sensorimotor hand area in the dysplasic subjects showed preference for body parts whose cortical territory is close to the hand area, but which are not compensatorily used as effectors. This suggests that function-based organization, originally proposed for congenital blindness and deafness, does not apply to cases of the primary sensorimotor cortex deprivation in dysplasia. This is consistent with the idea that experience-independent functional specialization occurs at relatively high levels of representation. Indeed, increased and selective foot movement preference in the dysplasics was found in the association cortex, in the inferior parietal lobule. Furthermore, it stresses the roles of neuroanatomical constraints such as topographical proximity and connectivity in determining the functional development of brain regions. These findings reveal limitations to brain plasticity and to the role of experience in shaping the functional organization of the brain.\n\nSignificance StatementWhat determines the role of brain regions, and their plasticity when typical inputs or experience is not provided? To what extent can extreme compensatory use affect brain organization? We tested the functional reorganization of the primary sensorimotor cortex hand area in people born without hands, who use their feet for every-day tasks. We found that it is preferentially activated by close-by body-parts which cannot serve as effectors, and not by the feet. In contrast, foot-selective compensatory plasticity was found in the association cortex, in an area involved in tool use. This shows limitations of compensatory plasticity and experience in modifying brain organization of early topographical cortex, as compared to association cortices where function-based organization is the driving factor.\n\nClassificationBiological Sciences\\Neuroscience

neuroscience↗