Sleep after spatial learning promotes covert reorganization of brain activity

doi:10.1073/pnas.0510198103

Sleep after spatial learning promotes covert reorganization of brain activity

*Cyclotron Research Center, University of Liège, Bâtiment B30, 4000 Liège, Belgium; and
^‡Department of Neurology, Centre Hospitalier Universitaire, University of Liège, 4000 Liège, Belgium

Edited by Marcus E. Raichle, Washington University School of Medicine, St. Louis, MO, and approved March 17, 2006 (received for review November 24, 2005)

Abstract

Sleep promotes the integration of recently acquired spatial memories into cerebral networks for the long term. In this study, we examined how sleep deprivation hinders this consolidation process. Using functional MRI, we mapped regional cerebral activity during place-finding navigation in a virtual town, immediately after learning and 3 days later, in subjects either allowed regular sleep (RS) or totally sleep-deprived (TSD) on the first posttraining night. At immediate and delayed retrieval, place-finding navigation elicited increased brain activity in an extended hippocampo-neocortical network in both RS and TSD subjects. Behavioral performance was equivalent between groups. However, striatal navigation-related activity increased more at delayed retrieval in RS than in TSD subjects. Furthermore, correlations between striatal response and behavioral performance, as well as functional connectivity between the striatum and the hippocampus, were modulated by posttraining sleep. These data suggest that brain activity is restructured during sleep in such a way that navigation in the virtual environment, initially related to a hippocampus-dependent spatial strategy, becomes progressively contingent in part on a response-based strategy mediated by the striatum. Both neural strategies eventually relate to equivalent performance levels, indicating that covert reorganization of brain patterns underlying navigation after sleep is not necessarily accompanied by overt changes in behavior.

Footnotes

^§To whom correspondence should be addressed. E-mail: philippe.peigneux{at}ulg.ac.be
↵ ^†Present address: Functional Neuroimaging Unit, University of Montreal, 4565, Queen Mary, Montreal, QC, Canada H3W 1W5.
Author contributions: P.O., P.M., and P.P. designed research; P.O. and P.P. performed research; E.B., C.D., and A.L. contributed new reagents/analytic tools; P.O. and P.P. analyzed data; and P.O., G.R., P.M., and P.P. wrote the paper.
Conflict of interest statement: No conflicts declared.
Data deposition: The neuroimaging data reported in this paper have been deposited with the fMRI Data Center, www.fmridc.org (accession no. 2-2006-121CE).
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations:

fMRI,

functional MRI;

RS,

regular sleep;

SWS,

slow-wave sleep;

TSD,

totally sleep-deprived.