Reactivation or transformation? Motor memory consolidation associated with cerebral activation time-locked to sleep spindles

Abstract

Motor memory consolidation is thought to depend on sleep-dependent reactivation of brain areas recruited during learning. However, up to this point, there has been no direct evidence to support this assertion in humans, and the physiological processes supporting such reactivation are unknown. Here, simultaneous electroencephalographic and functional magnetic resonance imaging (EEG-fMRI) recordings were conducted during post-learning sleep to directly investigate the spindle-related reactivation of a memory trace formed during motor sequence learning (MSL), and its relationship to overnight enhancement in performance (reflecting consolidation). We show that brain regions within the striato-cerebello-cortical network recruited during training on the MSL task, and in particular the striatum, were also activated during sleep, time-locked to spindles. Interestingly, the consolidated trace in the striatum was not simply strengthened, but was transformed/reorganized from rostrodorsal (associative) to caudoventral (sensorimotor) subregions. Moreover, the degree of the reactivation was correlated with overnight improvements in performance. Altogether, the present findings demonstrate that striatal reactivation linked to sleep spindles in the post-learning night, is related to motor memory consolidation.

Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI

“…Several studies have emphasized the role of sleep spindles ( Fogel and Smith, 2006 ; Ramanathan et al, 2015 ) and other features of NREM sleep such as slow wave activity ( Cousins et al, 2014 ; Gulati et al, 2014 ) in the consolidation of a procedural memory. Indeed, learning-dependent changes in sleep spindles take place following motor learning ( Fogel and Smith, 2006 ) and are shown to be related to the amount of off-line gains in performance ( Nishida and Walker, 2007 ), as well as enhanced activity in the putamen during NREM sleep ( Fogel et al, 2017 ) and at retest following sleep, but not wake ( Fogel et al, 2014 ). Altogether, this suggests that sleep spindle activity is a possible neurophysiological mechanism for driving the increased connectivity of the putamen within the consolidated pattern during NREM sleep.…”

Linking Network Activity to Synaptic Plasticity during Sleep: Hypotheses and Recent Data

“…Recent studies using repeated functional brain imaging during motor task acquisition demonstrated that a correlate of sleep-dependent performance enhancement is an increase in task-related brain activity in corticostriatal and cerebellar motor systems following a period of sleep (Debas et al, 2010 ; Fogel et al, 2017 ). This increase in task representation in the brain after a period of post-learning sleep is suggestive of synaptic strengthening, insofar as BOLD signal changes reflect changes in the extent of synaptic activity.…”

The hippocampus is necessary for the consolidation of a task that does not require the hippocampus for initial learning

“…Further indirect evidence that the hippocampus is important for sleep‐dependent MST consolidation comes from associations between MST improvement and sleep spindles. Sleep spindles and stage 2 sleep (a stage defined by spindle events) are associated with improvement on the MST (Albouy, Fogel, et al, ; Barakat et al, ; Barakat et al, ; Boutin et al, ; Fogel, Albouy, et al, ; Fogel, Vien, et al, ; Fogel et al, ; Laventure et al, ; Laventure et al, ; Manoach et al, ; Nishida & Walker, ; Walker, Brakefield, Morgan, Hobson, & Stickgold, ), and spindles are in turn often associated with hippocampal replay (Ji & Wilson, ; Peyrache et al, ; Siapas & Wilson, ; Sirota et al, ; Staresina et al, ). Consistent with the idea that spindles can provide an index of hippocampal involvement in consolidation, they have often been associated with improvement in tasks that are known to depend on the hippocampus (Saletin & Walker, ; though not all hippocampally dependent tasks show spindle correlations; Ackermann, Hartmann, Papassotiropoulos, de Quervain, & Rasch, ).…”