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Dual enhancement mechanisms for overnight motor memory consolidation

Abstract

Our brains are constantly processing past events1. These offline processes consolidate memories, leading in the case of motor skill memories to an enhancement in performance between training sessions. A similar magnitude of enhancement develops over a night of sleep following an implicit task, in which a sequence of movements is acquired unintentionally, or following an explicit task, in which the same sequence is acquired intentionally2. What remains poorly understood, however, is whether these similar offline improvements are supported by similar circuits, or through distinct circuits. We set out to distinguish between these possibilities by applying transcranial magnetic stimulation over the primary motor cortex (M1) or the inferior parietal lobule (IPL) immediately after learning in either the explicit or implicit task. These brain areas have both been implicated in encoding aspects of a motor sequence and subsequently supporting offline improvements over sleep35. Here we show that offline improvements following the explicit task are dependent on a circuit that includes M1 but not IPL. In contrast, offline improvements following the implicit task are dependent on a circuit that includes IPL but not M1. Our work establishes the critical contribution made by M1 and IPL circuits to offline memory processing, and reveals that distinct circuits support similar offline improvements.

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Figure 1: Experimental design.
Figure 2: A double dissociation between site of stimulation and subsequent offline improvements in different learning tasks.
Figure 3: Response time changes during learning in the different tasks.

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Acknowledgements

We thank the National Science Foundation (Division of Behavioral and Cognitive Sciences, BCS, 0921177; E.M.R.) and the National Institutes of Health (R01 NS051446-03S1; E.M.R.) who funded this work. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We also thank S. Tunovic for his assistance with many of the experiments, J. Saletin for helping with some aspects of the sleep analysis, and J. Mullington and M. Haack for helping with both the recording and scoring of participants’ sleep.

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J.B. performed the experiments and analysed the data. E.M.R designed the study, performed the experiments, analysed the data, interpreted the results and wrote the manuscript.

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Correspondence to Edwin M. Robertson.

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The authors declare no competing interests.

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Breton, J., Robertson, E. Dual enhancement mechanisms for overnight motor memory consolidation. Nat Hum Behav 1, 0111 (2017). https://doi.org/10.1038/s41562-017-0111

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