Altered Contralateral Sensorimotor System Organization after Experimental Hemispherectomy: A Structural and Functional Connectivity Study

Abstract

Hemispherectomy is often followed by remarkable recovery of cognitive and motor functions. This reflects plastic capacities of the remaining hemisphere, involving large-scale structural and functional adaptations. Better understanding of these adaptations may (1) provide new insights in the neuronal configuration and rewiring that underlies sensorimotor outcome restoration, and (2) guide development of rehabilitation strategies to enhance recovery after hemispheric lesioning. We assessed brain structure and function in a hemispherectomy model. With MRI we mapped changes in white matter structural integrity and gray matter functional connectivity in eight hemispherectomized rats, compared with 12 controls. Behavioral testing involved sensorimotor performance scoring. Diffusion tensor imaging and resting-state functional magnetic resonance imaging were acquired 7 and 49 days post surgery. Hemispherectomy caused significant sensorimotor deficits that largely recovered within 2 weeks. During the recovery period, fractional anisotropy was maintained and white matter volume and axial diffusivity increased in the contralateral cerebral peduncle, suggestive of preserved or improved white matter integrity despite overall reduced white matter volume. This was accompanied by functional adaptations in the contralateral sensorimotor network. The observed white matter modifications and reorganization of functional network regions may provide handles for rehabilitation strategies improving functional recovery following large lesions.

A new model of experimental hemispherotomy in young adult Rattus norvegicus: a neural tract tracing and SPECT in vivo study

“…32 Thus, experimental studies are also performed to better understand the mechanisms of neuroplasticity involved in the functional recovery of these patients. 28,29,34,45,49 We observed that animals submitted to experimental hemispherotomy displayed a motor deficit 10 days after the surgical procedures. However, there was a significant improvement in motor coordination and balance displayed by these animals in the rotarod test 30 days after the hemispherotomy, suggesting brain neuroplasticity.…”

“…28,29,41 The functional recovery shown in the rats undergoing hemispherotomy in the present work is similar to that reported elsewhere. 19,34,53 In addition, the neurosurgical procedure preserved some critical connections subserving the motor function, such as the cortico-neostriatum-nigral pathways and the nigro-striatal projections.…”

“…According to the 2-way ANOVA, there was a significant effect of treatment (F [34,24] = 2, p < 0.0001), time (F[2,19] = 27, p < 0.007), and treatment versus time interaction (F [34,24] = 21.26, p < 0.0001) in the behavioral study. Although in the preoperative period (control, sham procedure, or experimental surgery groups) motor performance was significantly affected by brain injuries, there was an increase in the number of attempts to maintain balance on the moving cylinder in the rotarod test at 10 days (Bonferroni's post hoc test, p < 0.001) and 30 days (Bonferroni's post hoc test, p < 0.001) after the hemispherotomy compared with the control groups (Fig.…”

“…In addition, we should highlight the functional role played by neuronal activity in the basal nuclei, brainstem-descending reticular-spinal projections, and cerebellum in recovering animals; neuronal and myelin plasticity; 11 electrical stimulation; 27,54 and neurophysiological mechanisms 42 previously suggested by several researchers. 34,43,46,49 The current model of hemispherotomy also enables the development of new rehabilitation strategies in rodents undergoing experimental hemispherotomy for the improvement of postsurgical recovery after hemispheric injuries, and it allows us to describe the neurological bases of this surgical therapeutic intervention in children with pharmacologically refractory epilepsy.…”

Desenvolvimento de modelo experimental de hemisferotomia em ratos

“…Entretanto, por mais graves que sejam as consequências dessas lesões, podemos constatar que, frequentemente, ocorrem melhoras nos déficits funcionais. Essa recuperação pode ser observada em estudos experimentais realizados com modelos animais (Marino et al, 2001;Machado et al, 2003;Umeda e Funakoshi, 2014;Wanakhachornkrai et al, 2014;Otte et al, 2015).…”