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Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity

Abstract

Sleep slow wave activity (SWA) is thought to reflect sleep need, increasing after wakefulness and decreasing after sleep. We showed recently that a learning task involving a circumscribed brain region produces a local increase in sleep SWA. We hypothesized that increases in cortical SWA reflect synaptic potentiation triggered by learning. To further investigate the link between synaptic plasticity and sleep, we asked whether a procedure leading to synaptic depression would cause instead a decrease in sleep SWA. We show here that if a subject's arm is immobilized during the day, motor performance deteriorates and both somatosensory and motor evoked potentials decrease over contralateral sensorimotor cortex, indicative of local synaptic depression. Notably, during subsequent sleep, SWA over the same cortical area is markedly reduced. Thus, cortical plasticity is linked to local sleep regulation without learning in the classical sense. Moreover, when synaptic strength is reduced, local sleep need is also reduced.

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Figure 1: Study design.
Figure 2: Performance decrement after immobilization.
Figure 3: Decreased MEP amplitude after immobilization.
Figure 4: Changes in SEPs in the presleep session after immobilization.
Figure 5: Changes in local SWA homeostasis during sleep after immobilization.
Figure 6: Characteristics of the local SWA change after immobilization.

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Acknowledgements

We thank M. Bove, C. Moisello, N. Garre, L. Rondi and F. Battaglia for help with the selection of the immobilization protocol; C. Cirelli for comments on the manuscript; S. Maata and F. Ferreri for help with the collection of MEPs; and R. Davidson and A. Alexander at the Keck Center for support with EEG and MRI facilities. This work was supported by grants from the Swiss Foundation for Fellowships in Biology and Medicine (R.H.), the National Parkinson Foundation (M.F.G.) and the US National Institutes of Health (1RO1 NS 055 185-01 to G.T.); and by a McDonnell Foundation grant (G.T. and M.F.G.).

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R.H. discussed the study design, tested subjects, analyzed electrophysiological data, performed statistics, prepared figures and drafted the manuscript. M.F.G. developed the behavioral protocol, discussed the study design, analyzed the behavioral data, performed statistics, prepared figures and contributed to the manuscript preparation. M.M., F.F., B.A.R. and M.J.P. helped with subject testing and data analysis. G.T. suggested the study design, supervised the experiments and worked on the manuscript.

Corresponding authors

Correspondence to M Felice Ghilardi or Giulio Tononi.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Local changes in EEG power in the spindle frequency range during sleep after immobilization. (PDF 949 kb)

Supplementary Methods (PDF 216 kb)

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Huber, R., Ghilardi, M., Massimini, M. et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci 9, 1169–1176 (2006). https://doi.org/10.1038/nn1758

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