Skill acquisition increases myelination and strengthens functional connectivity in the sensorimotor circuit of the adult rat

Abstract

The effects of skill acquisition on whole-brain structure and functional networks have been extensively investigated in humans but have yet to be explored in rodents. Forelimb reaching training in rodents results in well-established focal functional and structural reorganization within the motor cortex (M1) and cerebellum, indicating distributed alterations in both structure and function. However, it is unclear how local alterations in structure and function relate to distributed learning-related changes across motor networks. Here we trained adult rats in skilled reaching and used multimodal whole-brain in vivo MRI to assess both structural and functional plasticity over time.We detected increases in a myelin-related MRI metric in white matter, cortical areas, and to a lesser extent in the cerebellum, paralleled by strengthened functional connectivity between M1 and cerebellum, possibly reflecting a decrease in cerebellum inhibition over M1. Skill learning therefore leads to myelin increases in pathways that connect sensorimotor regions, and in functional connectivity increases between areas involved in motor learning, all of which correlate with performance. These findings closely mirror previous reports of network-level changes following motor learning in humans and underlines the correspondence between human and rodent brain circuits for motor learning, despite important differences in the anatomy of physiology of movement circuits between species.

Hebbian activity-dependent plasticity in white matter

“…Recent developments in MR physics are allowing researchers to measure quantitative MR parameters with higher reliability than ever before, thus providing additional tools to study the relatively subtle changes in myelination that can be experimentally induced in humans. In particular, quantitative markers based on magnetization transfer, such as the one used here, are especially sensitive to the myelin content of a voxel ( Mancini et al., 2020 ) and have been shown to be particularly sensitive to myelin changes in response to behavioral interventions ( Sampaio-Baptista et al., 2019 ). In summary, non-invasive quantitative markers are not only able to improve our understanding of white matter and myelin plasticity but may also afford the ability to translate key rodent findings to both healthy and clinical human cohorts ( Brodt et al., 2018 ).…”