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A deficit in the ability to form new human memories without sleep

Nature Neuroscience volume 10, pages 385–392 (2007)Cite this article

Abstract

Evidence indicates that sleep after learning is critical for the subsequent consolidation of human memory. Whether sleep before learning is equally essential for the initial formation of new memories, however, remains an open question. We report that a single night of sleep deprivation produces a significant deficit in hippocampal activity during episodic memory encoding, resulting in worse subsequent retention. Furthermore, these hippocampal impairments instantiate a different pattern of functional connectivity in basic alertness networks of the brainstem and thalamus. We also find that unique prefrontal regions predict the success of encoding for sleep-deprived individuals relative to those who have slept normally. These results demonstrate that an absence of prior sleep substantially compromises the neural and behavioral capacity for committing new experiences to memory. It therefore appears that sleep before learning is critical in preparing the human brain for next-day memory formation—a worrying finding considering society's increasing erosion of sleep time.

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Figure 1: fMRI regions of significant activation during all encoding trials (relative to fixation baseline) in the sleep control and sleep deprivation groups separately (full coordinates given in Table 3).
Figure 2: fMRI group-level encoding differences.
Figure 3: Group-level differences in hippocampal functional connectivity.
Figure 4: fMRI group-level differences in Dm activation in the sleep deprivation (SD) relative to the sleep control (SC) group.
Figure 5: fMRI correlation analysis.

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Acknowledgements

We thank R. Buckner, M. Rugg, R. Stickgold and E. Robertson for their insightful and helpful comments regarding these findings, and H. O'Leary for technical magnetic resonance imaging assistance. This work was supported in part by grants from the US National Institutes of Health (MH69,935 (M.P.W.); NS48,242 (S.-S.Y); RR19,703 (F.A.J.)) and the American Academy of Sleep Medicine (M.P.W.).

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Authors and Affiliations

  1. Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, 02115, Massachusetts, USA

    Seung-Schik Yoo & Ferenc A Jolesz

  2. Department of Psychiatry, Sleep and Neuroimaging Laboratory, FD/Feldberg 862, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, 02115, Massachusetts, USA

    Peter T Hu, Ninad Gujar & Matthew P Walker

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Contributions

S.-S.Y.: designing experimental protocols, conducting the experiments, analyzing the data and writing the manuscripts. P.T.H.: conducting the experiments, analyzing the data and writing the manuscript. N.G.: conducting the experiments, analyzing the data and writing the manuscript. F.A.J.: designing experimental protocols and writing the manuscript. M.P.W.: designing experimental protocols, conducting the experiments, analyzing the data and writing the manuscript.

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Correspondence to Matthew P Walker.

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Supplementary information

Supplementary Fig. 1

fMRI group level encoding differences (depicted in the manuscript as Figures 2 and 4), displayed at the more liberal significance of P < 0.005; ≥ 5 contiguous voxels on glass brain MIP plots. (PDF 96 kb)

Supplementary Fig. 2

fMRI correlation analysis. (PDF 172 kb)

Supplementary Fig. 3

fMRI correlation analysis. (PDF 112 kb)

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Yoo, SS., Hu, P., Gujar, N. et al. A deficit in the ability to form new human memories without sleep. Nat Neurosci 10, 385–392 (2007). https://doi.org/10.1038/nn1851

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