Shaping the structural dynamics of motor learning through cueing during sleep

Abstract

Enhancing the retention of recent memory traces through sleep reactivation is possible via Targeted Memory Reactivation (TMR), involving cueing learned material during post-training sleep. Evidence indicates detectable short-term microstructural changes in the brain within an hour after motor sequence learning, and post-training sleep is believed to contribute to the consolidation of these motor memories, potentially leading to enduring microstructural changes. In this study, we explored how TMR during post-training sleep affects performance gains and delayed microstructural remodeling, using both standard Diffusion Tensor Imaging (DTI) and advanced Neurite Orientation Dispersion & Density Imaging (NODDI). Sixty healthy young adults participated in a five-day protocol, undergoing five Diffusion-Weighted Imaging (DWI) sessions, pre- and post-two motor sequence training sessions, and after a post-training night of either regular sleep (RS) or TMR. Results demonstrated rapid skill acquisition on Day 1, followed by performance stabilization on Day 2, and improvement on Day 5, in both RS and TMR groups. (Re)training induced widespread microstructural changes in motor-related areas, initially involving the hippocampus, followed by a delayed engagement of the caudate nucleus. Mean Diffusivity (MD) changes were accompanied by increased Neurite Density Index (NDI) in the putamen, suggesting increased neurite density, while Free Water Fraction (FWF) reduction indicated glial reorganization. TMR-related structural differences emerged in the dorsolateral prefrontal cortex (DLPFC) on Day 2 and the right cuneus on Day 5, suggesting unique sleep TMR-related neural reorganization patterns. Persistence of practice-related structural changes, although moderated over time, suggest a lasting neural network reorganization, partially mediated by sleep TMR. Statement of SignificanceThis study demonstrates how motor practice triggers short-term and long-term microstructural reorganization in (sub)cortical grey matter, with a focus on how sleep Targeted Memory Reactivation (TMR) influences these changes, particularly in motor-related areas. Combining standard Diffusion Tensor Imaging (DTI) with advanced Neurite Orientation Dispersion & Density Imaging (NODDI) imaging techniques, we highlight distinct patterns of neural reorganization, suggesting glial and/or synaptic changes, in response to motor practice, possibly partially mediated by TMR. This research enhances our understanding of motor practice-related structural plasticity mechanisms and highlights the potential of targeted sleep interventions to modulate brain reorganization, suggesting new avenues for optimizing motor skill acquisition.