Effect of skilled reaching training and enriched environment on generation of oligodendrocytes in the adult sensorimotor cortex and corpus callosum

Abstract

Background Increased motor activity or social interactions through enriched environment are strong stimulators of grey and white matter plasticity in the adult rodent brain. In the present study we evaluated whether specific reaching training of the dominant forelimb (RT) and stimulation of unspecific motor activity through enriched environment (EE) influence the generation of distinct oligodendrocyte subpopulations in the sensorimotor cortex and corpus callosum of the adult rat brain. Animals were placed in three different housing conditions: one group was transferred to an EE, a second group received daily RT, whereas a third group remained in the standard cage. Bromodeoxyuridine (BrdU) was applied at days 2–6 after start of experiments and animals were allowed to survive for 10 and 42 days.ResultsEnriched environment and daily reaching training of the dominant forelimb significantly increased the number of newly differentiated GSTπ+ oligodendrocytes at day 10 and newly differentiated CNPase+ oligodendrocytes in the sensorimotor cortex at day 42. The myelin level as measured by CNPase expression was increased in the frontal cortex at day 42. Distribution of newly differentiated NG2+ subpopulations changed between 10 and 42 days with an increase of GSTπ+ subtypes and a decrease of NG2+ cells in the sensorimotor cortex and corpus callosum. Analysis of neuronal marker doublecortin (DCX) showed that more than half of NG2+ cells express DCX in the cortex. The number of new DCX+NG2+ cells was reduced by EE at day 10.ConclusionsOur results indicate for the first time that specific and unspecific motor training conditions differentially alter the process of differentiation from oligodendrocyte subpopulations, in particular NG2+DCX+ cells, in the sensorimotor cortex and corpus callosum.Electronic supplementary materialThe online version of this article (doi:10.1186/s12868-017-0347-2) contains supplementary material, which is available to authorized users.

Remodeling of pre-existing myelinated axons and oligodendrocyte differentiation is stimulated by environmental enrichment in the young adult brain

“…4B, p=0.04) compared to SH controls. This finding is 270 concordant with previous observations of enhanced differentiation following activity-271 dependent stimulation (Cullen et al, 2019;Gibson et al, 2014;Hughes, Orthmann-Murphy, 272 Langseth, & Bergles, 2018;Keiner et al, 2017;Mitew et al, 2018;Xiao et al, 2016). 273…”

“…However, these artificial 28 methods to upregulate neuronal stimulation to promote myelin plasticity may be 29 problematic, as they may not actually reflect physiological levels of stimulation and have 30 recently been shown to promote the progression of tumor growth (Venkataramani et al, 31 2019;Venkatesh et al, 2019). Interestingly, young adult mice (Xiao et al, 2016) and rats 32 (Keiner et al, 2017) that were taught complex motor paradigms exhibited an increase in 33 new OL production, suggesting that OL adaptability extends to adulthood and is 34 physiologically relevant. While these findings are exciting, a complete understanding of the 35 precise changes in cellular dynamics induced by physiologically relevant stimulation and 36 how this ultimately influences myelin in the adult CNS remains unknown.…”

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

“…Taken together these results provide the first evidence that MTR is sensitive to longitudinal changes in myelin in white matter. While previous studies have focused on the motor cortex, where a higher number of recently differentiated oligodendrocytes are found after motor learning 42,43 , here, using a whole-brain approach, we detected MTR increases in S1 and S2, and a trend in cerebellum, suggesting increases in myelination in these areas as well.…”

Advances in noninvasive myelin imaging

“…Myelin plasticity could potentially be achieved by increased differentiation of OPCs, as well as changes in thickness, number and/or length of sheaths (Fields, 2015). Experiments have shown that experiences such as enriched environment and learning can induce such changes (Blumenfeld-Katzir et al, 2011;Sampaio-Baptista et al, 2013;Keiner et al, 2017) that can be indirectly detected with MRI in humans (Scholz et al, 2009;Sagi et al, 2012;Hofstetter et al, 2013).…”