Phase-specific reactivation modulates motor memory via hippocampal and striatal-mediated plasticity
Poster No:
2580
Submission Type:
Abstract Submission
Authors:
Judith NICOLAS1, Bradley King2, David Levesque3, Latifa Lazzouni4, David Wang5, Nir Grossman6, Stephan Swinnen7, Julien Doyon4, Julie Carrier8, Genevieve Albouy9
Institutions:
1Centre de Recherche en Neurosciences de Lyon, BRON, Not applicable, 2Department of Health and Kinesiology, College of Health, University of Utah, Salt Lake City, UT, 3Center for Advanced Research in Sleep Medicine, Centre Intégré Universitaire de Santé et de Servi, Montreal, Quebec, 4McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery, Montreal Neurological Inst, Montreal, Quebec, 5Elemind Technologies Inc Massachusetts Institute of Technology, Cambridge, MA, 6Faculty of Medicine, Department of Brain Sciences, Imperial College London, London, Not applicable, 7KU Leuven, Leuven, Vlaams Brabant, 8Department of Psychology, Université de Montréal, Montreal, Quebec, 9KU Leuven, Leuven, Belgium
First Author:
Co-Author(s):
Bradley King
Department of Health and Kinesiology, College of Health, University of Utah
Salt Lake City, UT
Department of Health and Kinesiology, College of Health, University of Utah
Salt Lake City, UT
David Levesque
Center for Advanced Research in Sleep Medicine, Centre Intégré Universitaire de Santé et de Servi
Montreal, Quebec
Center for Advanced Research in Sleep Medicine, Centre Intégré Universitaire de Santé et de Servi
Montreal, Quebec
Latifa Lazzouni
McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery, Montreal Neurological Inst
Montreal, Quebec
McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery, Montreal Neurological Inst
Montreal, Quebec
Nir Grossman
Faculty of Medicine, Department of Brain Sciences, Imperial College London
London, Not applicable
Faculty of Medicine, Department of Brain Sciences, Imperial College London
London, Not applicable
Julien Doyon
McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery, Montreal Neurological Inst
Montreal, Quebec
McConnell Brain Imaging Centre, Department of Neurology and Neurosurgery, Montreal Neurological Inst
Montreal, Quebec
Introduction:
Motor memory consolidation can be enhanced by targeted memory reactivation (TMR) during post-learning sleep (reviewed in Hu et al., 2020). Inspired by studies showing that auditory clicks delivered in a closed-loop (CL) fashion at the up state of the slow wave (SW) can optimize declarative memory consolidation, we tested whether applying TMR at specific phases of the SW (e.g., up vs. down stimulation) could influence motor memory consolidation. We used both EEG and fMRI to characterize the underlying neurophysiological processes. Inspired by studies showing that auditory clicks delivered in a closed-loop fashion at the up state of the SW can optimize declarative memory consolidation, we tested whether applying TMR at specific phases of the SW (e.g., up vs. down stimulation) could influence motor memory consolidation.
·Figure 1: Experimental protocol
Methods:
Twenty-eight young healthy adults (age range 18-30, 15 females) participated in this study. Each participant performed, in the fMRI scanner, a motor sequence learning (MSL) task including three different movement sequences before and after a night of sleep monitored with EEG (see details in Fig. 1). Sounds associated to the 3 different motor sequences were not replayed (control) or replayed either on the up or the down phase of the SW detected online during post-learning sleep. EEG data collected during reactivation were preprocessed using Fieldtrip with standard procedures (e.g., Nicolas et al., 2022). MRI data collected during task practice (TR = 2s, voxel size = 2.5x2.5x2.5mm; Philips Achieva 3T MR scanner) were preprocessed and analyzed using SPM12 with standard procedures (e.g., Dolfen et al., 2021). Based on previous evidence that the hippocampus and the striatum are critically involved in MSL (e.g., Albouy et al., 2015), task-related brain activity and connectivity were examined in these ROIs as well as motor areas.
Results:
Behavioral data analyses indicate that the offline overnight changes in performance speed were greater for the up- , as compared to the down-, reactivated sequences (up vs. down: t = 2.32, p = 0.014 (p-FDR = 0.035), Cohen's d = 0.44, Fig. 2a). Analyses of the sleep EEG data revealed a phase-specific modulation of sleep oscillations such that up-stimulated SW exhibited higher amplitude and greater sigma power nested in the SW peak than down-stimulated SW (p-value = 0.0040; Cohen's d = 0.67 and p = 0.0080; Cohen's d = 0.66 respectively, corrected with cluster-based permutations, Fig. 2b). Moreover, up-stimulation resulted in a greater overnight increase in task-related brain activity in striato-motor networks (up vs. down: x = 20, y = 18, z = 12, p-Small Volume Corrected (p-svc) = 0.009; up vs not: x = 18, y = 28, z =4, p-svc = 0.02; down vs not: x = 16, y = -2, z = 26, p-svc = 0.016) while it prevented hippocampal activity to decrease as compared to the not-reactivated condition (up vs. not: x = 36, y = -36, z = -4, p-svc = 0.028, Fig. 2c). Connectivity analyses showed that down stimulation resulted in an overnight increase in striatal connectivity (up vs not: x = -32, y = -20, z = 50, p-svc = 0.02, Fig 2d). Interestingly, this down-reactivated increase in striato-motor connectivity was associated to poorer overnight performance improvement (x = 26, y = -8, z = 44, p-svc = 0.025) whereas the increase in striato-hippocampal connectivity was associated to greater performance improvement (x = -16, y = -40, z = 6, p-svc = 0.014, Fig 2e).
·Figure 2: Phase-specific modulation of motor memory consolidation
Conclusions:
Altogether, these results suggest that slow-oscillation closed-loop TMR induced phase-specific modulations of (i) motor performance, (ii) activity and connectivity in task-relevant networks including the striatum, the hippocampus and the motor cortex and (iii) characteristics of sleep EEG features involved in plasticity processes. Interestingly, the different brain connectivity patterns observed at retest during practice of the down-reactivated sequence were effective or not to compensate for the deleterious effect of down stimulation on performance.
Brain Stimulation:
Non-Invasive Stimulation Methods Other
Learning and Memory:
Skill Learning 2
Modeling and Analysis Methods:
Connectivity (eg. functional, effective, structural)
EEG/MEG Modeling and Analysis
Perception, Attention and Motor Behavior:
Sleep and Wakefulness 1
Keywords:
FUNCTIONAL MRI
Learning
Memory
Motor
Plasticity
Sleep
Other - consolidation
1|2Indicates the priority used for review
Provide references using author date format
Dolfen, N., King, B. R., Schwabe, L., Gann, M. A., Veldman, M. P., von Leupoldt, A., Swinnen, S. P., & Albouy, G. (2021). Stress Modulates the Balance between Hippocampal and Motor Networks during Motor Memory Processing. Cerebral Cortex, 31(2), 1365‑1382. https://doi.org/10.1093/cercor/bhaa302
Hu, X., Cheng, L. Y., Chiu, M. H., & Paller, K. A. (2020). Promoting memory consolidation during sleep : A meta-analysis of targeted memory reactivation. Psychological Bulletin, 146(3), 218‑244. https://doi.org/10.1037/bul0000223
Nicolas, J., King, B. R., Levesque, D., Lazzouni, L., Coffey, E., Swinnen, S., Doyon, J., Carrier, J., & Albouy, G. (2022). Sigma oscillations protect or reinstate motor memory depending on their temporal coordination with slow waves. eLife, 11, e73930. https://doi.org/10.7554/eLife.73930