Motor Memory Consolidation in Sleep Shapes More Effective Neuronal Representations

Abstract

Learning a motor skill involves a latent process of consolidation that develops after training to enhance the skill in the absence of any practice and crucially depends on sleep. Here, we show that this latent consolidation during sleep changes the brain representation of the motor skill by reducing overall the neocortical contributions to the representation. Functional magnetic resonance brain imaging was performed during initial training and 48 h later, at retesting, on a sequential finger movement task with training followed by either a night of regular sleep or sleep deprivation. An additional night of sleep for all subjects served to rule out unspecific effects of sleep loss at retrieval testing. Posttraining sleep, but not sleep deprivation, led to improved motor skill performance at retrieval. This sleep-dependent improvement was linked to greatly reduced brain activation in prefrontal, premotor, and primary motor cortical areas, along with a stronger involvement of left parietal cortical regions. Our findings indicate that storing a motor skill during sleep reorganizes its brain representation toward enhanced efficacy.

Impaired Off-Line Consolidation of Motor Memories After Combined Blockade of Cholinergic Receptors During REM Sleep-Rich Sleep

“…Importantly, regulation of plasticity-related early genes depends strongly on the cholinergic receptor activation (von der Kammer et al, 1998(von der Kammer et al, , 2001Teber et al, 2004) and, here, blocking these receptors interfered likely with transcriptional changes required for long-term memory storage. This view is corroborated by recent evidence showing that cholinergic activation potentiates long-term potentiation maintenance in the medial prefrontal cortex (Lopes et al, 2008), a brain area that exhibited particularly strong sleep-dependent changes in activation during the same skill learning task as used here (Walker et al, 2005;Fischer et al, 2005). We suspect that the combined cholinergic receptor blockade during late, REM sleep-rich sleep interfered specifically with processes of synaptic consolidation required for sleep-dependent enhancements of skill performance (Dudai, 2004).…”

The episodic engram transformed: Time reduces retrieval-related brain activity but correlates it with memory accuracy

“…In balancing between usable information and its energetic cost (potentially tapped by the BOLD signal) (Bullmore and Sporns 2012), the system may have evolved to keep the critical ability to recognize correctly for longer times at a lesser expense. Supporting this view, previous results suggest that consolidation processes engaged during sleep change brain representation of an acquired motor skill by reducing cortical contributions, i.e., by decreasing BOLD signals measured during subsequent retrieval (Fischer et al 2005).…”

Plasticité fonctionnelle du cerveau et apprentissage moteur

“…Ce phénomène peut notamment être observé lorsque l'individu atteint un niveau de performance asymptotique durant la première session d'entraînement et démontre une amélioration spontanée des performances lors d'une seconde session de test après une période de temps écoulée sans entraînement additionnel. De nombreuses SYNTHÈSE REVUES études, celles de mon laboratoire incluses, ont récemment montré que ces gains (qui indiquent que le processus de consolidation a bel et bien eu lieu) sont dépendants du sommeil [19][20][21][22]. Ceci est particulièrement vrai lorsque la séquence est connue explicitement au moment de l'acquisition initiale [19,21], qu'elle est déterministe plutôt que probabiliste [23] [27], a élégamment démontré, chez de jeunes participants, que non seulement le striatum mais également l'hippocampe contribueraient au processus de consolidation d'un apprentissage implicite d'une séquence oculomotrice en conditionnant le processus de création de la trace mnésique motrice engendrée durant la période initiale de pratique ( Figure 5).…”