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Sleep Consolidation Potentiates Sensorimotor Adaptation

  1. Valeria Della-Maggiore1,3,4
  1. 1Universidad de Buenos Aires-CONICET. Instituto de Fisiología y Biofísica Bernardo Houssay (IFIBIO Houssay), Facultad de Medicina, Departamento de Ciencias Fisiológicas, Ciudad de Buenos Aires C1121ABG, Argentina
  2. 2Departamento de Medicina Interna, Servicio de Medicina Pulmonar y Sueño, Hospital Universitario Austral, Pilar, Buenos Aires B1629AHJ, Argentina
  3. 3Department of Neurology and Neurosurgery, McGill University Montreal, Quebec H3A2B4, Canada
  4. 4Escuela de Ciencia y Tecnología (ECyT), Universidad Nacional de San Martin, San Martin, Buenos Aires, CP 1650, Argentina
  1. Author contributions: A.S., G.L., G.G., A.D., P.C., L.R., and V.D.-M. designed research; A.S., G.L., and P.C. performed research; A.S. and G.L. analyzed data; A.S., G.L., G.G., A.D., L.R., D.P.-C., and V.D.-M. contributed unpublished reagents/analytic tools; A.S. and V.D.-M. wrote the paper.

Abstract

Contrary to its well-established role in declarative learning, the impact of sleep on motor memory consolidation remains a subject of debate. Current literature suggests that while motor skill learning benefits from sleep, consolidation of sensorimotor adaptation (SMA) depends solely on the passage of time. This has led to the proposal that SMA may be an exception to other types of memories. Here, we addressed this ongoing controversy in humans through three comprehensive experiments using the visuomotor adaptation paradigm (N = 290, 150 females). In Experiment 1, we investigated the impact of sleep on memory retention when the temporal gap between training and sleep was not controlled. In line with the previous literature, we found that memory consolidates with the passage of time. In Experiment 2, we used an anterograde interference protocol to determine the time window during which SMA memory is most fragile and, thus, potentially most sensitive to sleep intervention. Our results show that memory is most vulnerable during the initial hour post-training. Building on this insight, in Experiment 3, we investigated the impact of sleep when it coincided with the critical first hour of memory consolidation. This manipulation unveiled a benefit of sleep (30% memory enhancement) alongside an increase in spindle density and spindle–SO coupling during NREM sleep, two well-established neural markers of sleep consolidation. Our findings reconcile seemingly conflicting perspectives on the active role of sleep in motor learning and point to common mechanisms at the basis of memory formation.

  • Received February 16, 2024.
  • Revision received May 23, 2024.
  • Accepted June 12, 2024.

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