RESUMO
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.
Assuntos
Adaptação Fisiológica , Consolidação da Memória , Desempenho Psicomotor , Sono , Humanos , Feminino , Masculino , Consolidação da Memória/fisiologia , Sono/fisiologia , Adaptação Fisiológica/fisiologia , Adulto Jovem , Adulto , Desempenho Psicomotor/fisiologia , Destreza Motora/fisiologia , Aprendizagem/fisiologia , AdolescenteRESUMO
Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with practice (micro-offline gains, MOGs). This phenomenon is reminiscent of memory replay observed in the hippocampus during spatial learning in rodents. Whether the hippocampus is also involved in the production of MOGs remains currently unknown. Using a multimodal approach in humans, here we show that activity in the hippocampus and the precuneus increases during the quiet rest periods and predicts the level of MOGs before asymptotic performance is achieved. These functional changes were followed by rapid alterations in brain microstructure in the order of minutes, suggesting that the same network that reactivates during the quiet periods of training undergoes structural plasticity. Our work points to the involvement of the hippocampal system in the reactivation of procedural memories.
Assuntos
Hipocampo/fisiologia , Aprendizagem/fisiologia , Destreza Motora/fisiologia , Adolescente , Adulto , Feminino , Humanos , Imageamento por Ressonância Magnética , Masculino , Memória , Adulto JovemRESUMO
Anterograde interference refers to the negative impact of prior learning on the propensity for future learning. There is currently no consensus on whether this phenomenon is transient or long lasting, with studies pointing to an effect in the time scale of hours to days. These inconsistencies might be caused by the method employed to quantify performance, which often confounds changes in learning rate and retention. Here, we aimed to unveil the time course of anterograde interference by tracking its impact on visuomotor adaptation at different intervals throughout a 24-h period. Our empirical and model-based approaches allowed us to measure the capacity for new learning separately from the influence of a previous memory. In agreement with previous reports, we found that prior learning persistently impaired the initial level of performance upon revisiting the task. However, despite this strong initial bias, learning capacity was impaired only when conflicting information was learned up to 1 h apart, recovering thereafter with passage of time. These findings suggest that when adapting to conflicting perturbations, impairments in performance are driven by two distinct mechanisms: a long-lasting bias that acts as a prior and hinders initial performance and a short-lasting anterograde interference that originates from a reduction in error sensitivity.
Assuntos
Aprendizagem/fisiologia , Desempenho Psicomotor/fisiologia , Adulto , Feminino , Humanos , Masculino , Fatores de Tempo , Adulto JovemRESUMO
BACKGROUND: Fractional anisotropy (FA) and mean diffusivity (MD) are frequently used to evaluate longitudinal changes in white matter (WM) microstructure. Recently, there has been a growing interest in identifying experience-dependent plasticity in gray matter using MD. Improving registration has thus become a major goal to enhance the detection of subtle longitudinal changes in cortical microstructure. PURPOSE: To optimize normalization of diffusion tensor images (DTI) to improve registration in gray matter and reduce variability associated with multisession registrations. STUDY TYPE: Prospective longitudinal study. SUBJECTS: Twenty-one healthy subjects (18-31 years old) underwent nine MRI scanning sessions each. FIELD STRENGTH/SEQUENCE: 3.0T, diffusion-weighted multiband-accelerated sequence, MP2RAGE sequence. ASSESSMENT: Diffusion-weighted images were registered to standard space using different pipelines that varied in the features used for normalization, namely, the nonlinear registration algorithm (FSL vs. ANTs), the registration target (FA-based vs. T1 -based templates), and the use of intermediate individual (FA-based or T1 -based) targets. We compared the across-session test-retest reproducibility error of these normalization approaches for FA and MD in white and gray matter. STATISTICAL TESTS: Reproducibility errors were compared using a repeated-measures analysis of variance with pipeline as the within-subject factor. RESULTS: The registration of FA data to the FMRIB58 FA atlas using ANTs yielded lower reproducibility errors in white matter (P < 0.0001) with respect to FSL. Moreover, using the MNI152 T1 template as the target of registration resulted in lower reproducibility errors for MD (P < 0.0001), whereas the FMRIB58 FA template performed better for FA (P < 0.0001). Finally, the use of an intermediate individual template improved reproducibility when registration of the FA images to the MNI152 T1 was carried out within modality (FA-FA) (P < 0.05), but not via a T1 -based individual template. DATA CONCLUSION: A normalization approach using ANTs to register FA images to the MNI152 T1 template via an individual FA template minimized test-retest reproducibility errors both for gray and white matter. LEVEL OF EVIDENCE: 1 TECHNICAL EFFICACY STAGE: 1 J. Magn. Reson. Imaging 2020;52:766-775.