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

2017 ◽  
Author(s):  
Ella Striem-Amit ◽  
Gilles Vannuscorps ◽  
Alfonso Caramazza

SummaryWhat 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.Significance 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.ClassificationBiological Sciences\Neuroscience

2018 ◽  
Vol 115 (30) ◽  
pp. 7801-7806 ◽  
Author(s):  
Ella Striem-Amit ◽  
Gilles Vannuscorps ◽  
Alfonso Caramazza

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.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Mingqi Zhao ◽  
Marco Marino ◽  
Jessica Samogin ◽  
Stephan P. Swinnen ◽  
Dante Mantini

AbstractThe primary sensorimotor cortex plays a major role in the execution of movements of the contralateral side of the body. The topographic representation of different body parts within this brain region is commonly investigated through functional magnetic resonance imaging (fMRI). However, fMRI does not provide direct information about neuronal activity. In this study, we used high-density electroencephalography (hdEEG) to map the representations of hand, foot, and lip movements in the primary sensorimotor cortex, and to study their neural signatures. Specifically, we assessed the event-related desynchronization (ERD) in the cortical space. We found that the performance of hand, foot, and lip movements elicited an ERD in beta and gamma frequency bands. The primary regions showing significant beta- and gamma-band ERD for hand and foot movements, respectively, were consistent with previously reported using fMRI. We observed relatively weaker ERD for lip movements, which may be explained by the fact that less fine movement control was required. Overall, our study demonstrated that ERD based on hdEEG data can support the study of motor-related neural processes, with relatively high spatial resolution. An interesting avenue may be the use of hdEEG for deeper investigations into the pathophysiology of neuromotor disorders.


2019 ◽  
Author(s):  
František Váša ◽  
Rafael Romero-Garcia ◽  
Manfred G. Kitzbichler ◽  
Jakob Seidlitz ◽  
Kirstie J. Whitaker ◽  
...  

AbstractAdolescent changes in human brain function are not entirely understood. Here we used multi-echo functional magnetic resonance imaging (fMRI) to measure developmental change in functional connectivity (FC) of resting-state oscillations between pairs of 330 cortical regions and 16 subcortical regions in N=298 healthy adolescents. Participants were aged 14-26 years and were scanned on two or more occasions at least 6 months apart. We found two distinct modes of age-related change in FC: “conservative” and “disruptive”. Conservative development was characteristic of primary cortex, which was strongly connected at 14 years and became even more connected in the period 14-26 years. Disruptive development was characteristic of association cortex, hippocampus and amygdala, which were not strongly connected at 14 years but became more strongly connected during adolescence. We defined the maturational index (MI) as the signed coefficient of the linear relationship between baseline FC (at 14 years,FC14) and adolescent change in FC (∆FC14−26). Disruptive systems (with negative MI) were functionally specialised for social cognition and autobiographical memory and were significantly co-located with prior maps of aerobic glycolysis (AG), AG-related gene expression, post-natal expansion of cortical surface area, and adolescent shrinkage of cortical depth. We conclude that human brain organization is disrupted during adolescence by the emergence of strong functional connectivity of subcortical nuclei and association cortical areas, representing metabolically expensive re-modelling of synaptic connectivity between brain regions that were not strongly connected in childhood. We suggest that this re-modelling process may support emergence of social skills and self-awareness during healthy human adolescence.


2020 ◽  
Author(s):  
Julien Vezoli ◽  
Martin Vinck ◽  
Conrado A. Bosman ◽  
Andre M. Bastos ◽  
Christopher M Lewis ◽  
...  

What is the relationship between anatomical connection strength and rhythmic synchronization? Simultaneous recordings of 15 cortical areas in two macaque monkeys show that interareal networks are functionally organized in spatially distinct modules with specific synchronization frequencies, i.e. frequency-specific functional connectomes. We relate the functional interactions between 91 area pairs to their anatomical connection strength defined in a separate cohort of twenty six subjects. This reveals that anatomical connection strength predicts rhythmic synchronization and vice-versa, in a manner that is specific for frequency bands and for the feedforward versus feedback direction, even if interareal distances are taken into account. These results further our understanding of structure-function relationships in large-scale networks covering different modality-specific brain regions and provide strong constraints on mechanistic models of brain function. Because this approach can be adapted to non-invasive techniques, it promises to open new perspectives on the functional organization of the human brain.


Author(s):  
Nick Ward

After stroke, there is little restitution of neural tissue, but reorganization of surviving neural networks appears to be important for recovery of function. Non-invasive techniques such as functional magnetic resonance imaging and magnetoencephalography allow some aspects of this brain reorganization to be studied. For example, early after stroke there appears to be an upregulation in task-related activity, which diminishes with time and recovery. Those with the most complete recovery tend to have the most ‘normal’ activation pattern, and those with less complete recovery tend to rely on additional brain regions. This reorganization is functionally relevant. Advances in functional neuroimaging allow the study of alterations in connections between brain regions. Understanding how brain organization is related to anatomical damage, as well as impairment and recovery that can take place over weeks and months following stroke opens the way for functional brain imaging to become a clinically useful tool in rehabilitation.


2021 ◽  
Author(s):  
Jason He ◽  
Mark Mikkelsen ◽  
David Huddleston ◽  
Deana Crocetti ◽  
Kim Cecil ◽  
...  

Background. Individuals with Tourette syndrome (TS) often report that they express tics as a means of alleviating the experience of unpleasant sensations. These sensations are perceived as an urge to act and are referred to as premonitory urges. Premonitory urges have been the focus of recent efforts to develop interventions to reduce tic expression in those with TS. Increasing evidence points to the role of both structural and functional alterations of prefrontal and limbic brain regions regarding the experience of premonitory urges to tic in TS. This study examined the contribution of brain GABA and glutamate levels of the right primary sensorimotor cortex (SM1), supplementary motor area (SMA), and insular cortex (insula) to tic and urge severity in children with TS.Methods. Edited magnetic resonance spectroscopy was used to assess GABA+ (GABA + macromolecules) and Glx (glutamate + glutamine) of the right SM1, SMA and insula in 68 children with TS (MAge = 10.59, SDAge = 1.33) and 41 typically developing controls (MAge = 10.26, SDAge = 2.21). We first compared GABA+ and Glx levels of these brain regions between groups. We then explored the association between regional GABA+ and Glx levels with urge and tic severity. Results. GABA+ and Glx of the right SM1, SMA and insula were comparable between the children with TS and typically developing controls. In children with TS, lower levels of SMA GABA+ was associated with more severe and more frequent premonitory urges. Neither GABA+ nor Glx levels were associated with tic severity. Conclusions. These results broadly support the role of GABAergic neurotransmission within the SMA in the experience of premonitory urges in children with TS.


2013 ◽  
Vol 109 (5) ◽  
pp. 1444-1456 ◽  
Author(s):  
B. J. Shannon ◽  
R. A. Dosenbach ◽  
Y. Su ◽  
A. G. Vlassenko ◽  
L. J. Larson-Prior ◽  
...  

It has been posited that a critical function of sleep is synaptic renormalization following a net increase in synaptic strength during wake. We hypothesized that wake would alter the resting-state functional organization of the brain and increase its metabolic cost. To test these hypotheses, two experiments were performed. In one, we obtained morning and evening resting-state functional MRI scans to assess changes in functional brain organization. In the second experiment, we obtained quantitative positron emission tomography measures of glucose and oxygen consumption to assess the cost of wake. We found selective changes in brain organization. Most prominently, bilateral medial temporal regions were locally connected in the morning but in the evening exhibited strong correlations with frontal and parietal brain regions involved in memory retrieval. We speculate that these changes may reflect aspects of memory consolidation recurring on a daily basis. Surprisingly, these changes in brain organization occurred without increases in brain metabolism.


2017 ◽  
Vol 2017 ◽  
pp. 1-8 ◽  
Author(s):  
Xiang Xiao ◽  
Qiang Lin ◽  
Wai-Leung Lo ◽  
Yu-Rong Mao ◽  
Xin-chong Shi ◽  
...  

Background. Functional magnetic resonance imaging (fMRI) is a promising method for quantifying brain recovery and investigating the intervention-induced changes in corticomotor excitability after stroke. This study aimed to evaluate cortical reorganization subsequent to virtual reality-enhanced treadmill (VRET) training in subacute stroke survivors.Methods. Eight participants with ischemic stroke underwent VRET for 5 sections per week and for 3 weeks. fMRI was conducted to quantify the activity of selected brain regions when the subject performed ankle dorsiflexion. Gait speed and clinical scales were also measured before and after intervention.Results. Increased activation in the primary sensorimotor cortex of the lesioned hemisphere and supplementary motor areas of both sides for the paretic foot (p<0.01) was observed postintervention. Statistically significant improvements were observed in gait velocity (p<0.05). The change in voxel counts in the primary sensorimotor cortex of the lesioned hemisphere is significantly correlated with improvement of 10 m walk time after VRET (r=−0.719).Conclusions. We observed improved walking and increased activation in cortical regions of stroke survivors after VRET training. Moreover, the cortical recruitment was associated with better walking function. Our study suggests that cortical networks could be a site of plasticity, and their recruitment may be one mechanism of training-induced recovery of gait function in stroke. This trial is registered with ChiCTR-IOC-15006064.


2008 ◽  
Vol 108 (3) ◽  
pp. 491-500 ◽  
Author(s):  
Warren Boling ◽  
Michael Parsons ◽  
Michal Kraszpulski ◽  
Carrie Cantrell ◽  
Aina Puce

Object The pli de passage moyen (PPM) is an omega-shaped cortical landmark bulging into the central sulcus. There has been considerable interest in the PPM given that hand motor and sensory tasks have been found on functional magnetic resonance (fMR) imaging to activate the structure. Note, however, that the cortical function subserved by the PPM is not completely understood. Finger and thumb function are somatotopically organized over the central area and encompass a larger cortical surface than the anatomical PPM. Therefore, a sensory or motor hand area within the PPM would be redundant with the somatotopically organized digit function in the primary sensorimotor cortex. In this study the authors aimed to clarify the function subserved by the PPM and further evaluate hand area function in the primary sensorimotor cortex. Methods To further elucidate the function subserved by the PPM, patients underwent cortical stimulation in the region of the PPM as well as fMR imaging–demonstrated activation of the hand area. Two separate analytical methods were used to correlate hand area functional imaging with whole-hand sensory and motor responses induced by cortical stimulation. Results A relationship of the anatomical PPM with cortical stimulation responses as well as hand fMR imaging activation was observed. Conclusions A strong relationship was identified between the PPM, whole-hand sensory and motor stimulation responses, and fMR imaging hand activation. Whole-hand motor and whole-hand sensory cortical regions were identified in the primary sensorimotor cortex. It was localized to the PPM and exists in addition to the somatotopically organized finger and thumb sensory and motor areas.


Author(s):  
Tamar Makin ◽  
London Plasticity Lab

Phantom sensations are experienced by almost every person who has lost their hand in adulthood. This mysterious phenomenon spans the full range of bodily sensations, including the sense of touch, temperature, movement, and even the sense of wetness. For a majority of upper-limb amputees, these sensations will also be at times unpleasant, painful, and for some even excruciating to the point of debilitating, causing a serious clinical problem, termed phantom limb pain (PLP). Considering the sensory organs (the receptors in the skin, muscle or tendon) are physically missing, in order to understand the origins of phantom sensations and pain the potential causes must be studied at the level of the nervous system, and the brain in particular. This raises the question of what happens to a fully developed part of the brain that becomes functionally redundant (e.g. the sensorimotor hand area after arm amputation). Relatedly, what happens to the brain representation of a body part that becomes overused (e.g. the intact hand, on which most amputees heavily rely for completing daily tasks)? Classical studies in animals show that the brain territory in primary somatosensory cortex (S1) that was “freed up” due to input loss (hereafter deprivation) becomes activated by other body part representations, those neighboring the deprived cortex. If neural resources in the deprived hand area get redistributed to facilitate the representation of other body parts following amputation, how does this process relate to persistent phantom sensation arising from the amputated hand? Subsequent work in humans, mostly with noninvasive neuroimaging and brain stimulation techniques, have expanded on the initial observations of cortical remapping in two important ways. First, research with humans allows us to study the perceptual consequence of remapping, particularly with regards to phantom sensations and pain. Second, by considering the various compensatory strategies amputees adopt in order to account for their disability, including overuse of their intact hand and learning to use an artificial limb, use-dependent plasticity can also be studied in amputees, as well as its relationship to deprivation-triggered plasticity. Both of these topics are of great clinical value, as these could inform clinicians how to treat PLP, and how to facilitate rehabilitation and prosthesis usage in particular. Moreover, research in humans provides new insight into the role of remapping and persistent representation in facilitating (or hindering) the realization of emerging technologies for artificial limb devices, with special emphasis on the role of embodiment. Together, this research affords a more comprehensive outlook at the functional consequences of cortical remapping in amputees’ primary sensorimotor cortex.


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