Extent of Bilateral Neuronal Network Reorganization and Functional Recovery in Relation to Stroke Severity

Abstract

Remodeling of neuronal structures and networks is believed to significantly contribute to (partial) restoration of functions after stroke. However, it has been unclear to what extent the brain reorganizes and how this correlates with functional recovery in relation to stroke severity. We applied serial resting-state functional MRI and diffusion tensor imaging together with behavioral testing to relate longitudinal modifications in functional and structural connectivity of the sensorimotor neuronal network to changes in sensorimotor function after unilateral stroke in rats. We found that gradual improvement of functions is associated with wide-ranging changes in functional and structural connectivity within bilateral neuronal networks, particularly after large stroke. Both after medium and large stroke, brain reorganization eventually leads to (partial) normalization of neuronal signal synchronization within the affected sensorimotor cortical network (intraregional signal coherence), as well as between the affected and unaffected sensorimotor cortices (interhemispheric functional connectivity). Furthermore, the bilateral network configuration shifts from subacutely increased "small-worldness," possibly reflective of initial excessive neuronal clustering and wiring, toward a baseline small-world topology, optimal for global information transfer and local processing, at chronic stages. Cortical network remodeling was accompanied by recovery of initially disrupted structural integrity in corticospinal tract regions, which correlated positively with retrieval of sensorimotor functions. Our study demonstrates that the degree of functional recovery after stroke is associated with the extent of preservation or restoration of ipsilesional corticospinal tracts in combination with reinstatement of interhemispheric neuronal signal synchronization and normalization of smallworld cortical network organization.

Aberrant White Matter Networks Mediate Cognitive Impairment in Patients with Silent Lacunar Infarcts in Basal Ganglia Territory

“…Previous studies have demonstrated that cortical brain infarcts can lead to cortical WM network remodeling. 31 However, it is unclear whether disruption of cortical WM networks occurred in patients with subcortical silent brain infarcts. In this report, specific attention was directed toward the disruption of cortical WM networks in patients with brain infarcts located in the basal ganglia.…”

Optogenetic Approaches to Target Specific Neural Circuits in Post-stroke Recovery

“…Imaging techniques, such as intrinsic optical imaging, VSD imaging, and 2-photo calcium imaging, have been used in conjunction with forelimb stimulations to study post-stroke activation patterns and functional remapping. Remapping occurs after stroke most prominently in peri-infarct zones, but is also observed in connected regions such as the unaffected hemisphere (e.g., contralesional cortex) [13,82,139,143,144]. Remodeling in peri-infarct zones and in the unaffected hemisphere, such as loss and recovery of dendritic spines and axonal sprouting, has been reported [12,145,146].…”

“…In addition, by combining fMRI in the same rats they reported a transhemispheric fiber connection through the corpus callosum that was lost in the rats without recovery of BOLD signals at 5 weeks after stroke. Van Meer et al [143] applied serial diffusion tensor imaging and resting-state fMRI, in which no stimulus was applied but the spontaneous BOLD fluctuations were analyzed, in order to correlate white matter integrity and functional connectivity to stroke recovery. Similar to a scenario described in patients, improvement of sensorimotor function is correlated with restoration of interhemispheric functional connectivity and normalization of network configuration of the bilateral sensorimotor cortex.…”

Study of Ability of Plastic Motor of Cerebral Cortex in Patients after Stroke (Literature Review)

“…В последствии было подтверждено, что снижение межполушарных взаимосвязей между ипсилатеральными и контралатеральными регио-нами первичной сенсомоторной коры, связано с уменьшением транскаллозальной передачи мар-ганца в этих областях [36]. Используя опытную модель инсульта, было показано, что степень функционального восстановления после ишемии связана со степенью сохранения или поражения кортикоспинальных трактов на стороне поврежде-ния в сочетании с восстановлением нейрональных сигналов, межполушарной синхронизации и норма-лизации функции коры [37]. Аналогично экспери-ментальной модели, подобные изменения функ-циональных взаимосвязей в состоянии покоя были выявлены и у больных непосредственно после перенесенного инсульта, что выражалось в значи-тельном сокращении количества функциональных взаимосвязей, особенно межполушарных, из об-ласти сенсомоторной коры на стороне поврежде-ния [38].…”

“…Авторы показали, что в нейронной сети мозга, в процессе восстанов-ления возникают изменения топологии с неопти-мальной конфигурацией сети. Однако в экспери-ментальной модели инсульта, наблюдается неод-нозначная картина изменения характеристик ней-ронной сети [37]. Установлено, что длина кратчайшего пути и расширение сети мотонейронов после инсульта у крыс, были значительно увеличенными в первые дни, затем они снижались до нормальных показа-телей.…”