Abstract
Hippocampal place cells assemblies are believed to support the cognitive map, and their reactivations during sleep are thought to be involved in spatial memory consolidation. By triggering intracranial rewarding stimulations by place cell spikes during sleep, we induced an explicit memory trace, leading to a goal-directed behavior toward the place field. This demonstrates that place cells' activity during sleep still conveys relevant spatial information and that this activity is functionally significant for navigation.
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Acknowledgements
We thank F.P. Battaglia, M.B. Zugaro, P. Faure, L. Roux, S. Bagur and S.I. Wiener for discussions, and A. Peyrache for discussion and critical readings of an earlier version of the manuscript. Some experiments were done with software developed by G. Cournelle and A. Baelde, engineering students from the ESPCI-ParisTech. This work was supported by the Fondation pour la Recherche Médicale DEQ20120323730, France, by the National Agency for Research ANR-REG-071220-01-01, France, by the CNRS: Programmes Interdisciplinaires de Recherche (Neuro-IC), ATIP-Avenir (2014) and by the city of Paris (Grant Emergence 2014). This work also received support under the program Investissements d'Avenir launched by the French Government and implemented by the ANR, with the references: ANR-10-LABX-54 MEMO LIFE and ANR-11-IDEX-0001-02 PSL* Research University. G.d.L. and M.M.L. were funded by the Ministère de l'Enseignement Supérieur et de la Recherche, France.
Author information
Author notes
- Gaetan de Lavilléon
- & Marie Masako Lacroix
These authors contributed equally to this work.
- Laure Rondi-Reig
- & Karim Benchenane
These authors jointly directed this work.
Affiliations
Team Memory, Oscillations and Brain States (MOBs), Brain Plasticity Unit, CNRS UMR 8249, Ecole Supérieure de Physique et de Chimie Industrielles de la Ville de Paris, Paris, France.
- Gaetan de Lavilléon
- , Marie Masako Lacroix
- & Karim Benchenane
Neuroscience Paris Seine, Cerebellum, Navigation and Memory Team, CNRS UMR 8246; INSERM, UMR-S 1130; Sorbonne Universités, University Pierre and Marie Curie, Paris, France.
- Gaetan de Lavilléon
- , Marie Masako Lacroix
- , Laure Rondi-Reig
- & Karim Benchenane
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Contributions
K.B. designed the experiment. G.d.L. and M.M.L. did the experiments. K.B., G.d.L. and M.M.L. analyzed the data. K.B., G.d.L., M.M.L. and L.R.-R. wrote the manuscript.
Competing interests
The authors declare no competing financial interests.
Corresponding author
Correspondence to Karim Benchenane.
Integrated supplementary information
Supplementary figures
- 1.
The place preference tasks.
- 2.
Characteristics of sleep pairing sessions with rewarding and non-rewarding MFB stimulations, showing similar properties and absence of sleep perturbation.
- 3.
Place cells activity and theta oscillations remain stable after MFB stimulations.
- 4.
MFB stimulation does not alter sleep sharp-wave ripples (SPW-Rs), nor associated neuronal activity.
- 5.
Offline spike sorting and online spike detection.
- 6.
Additional statistical quantification of the place preference induced by the sleep-pairing protocol.
- 7.
Partial correlations of occupancy and firing map before, during and after wake-pairing protocol.
- 8.
Comparison between place preference tasks in all configurations and effect of the circadian rhythm.
- 9.
Quantification of behavioral measures expressed in the sleep-pairing protocol (n = 5) and normalization methods.
- 10.
Fine characterization of mouse behavior during experiments
Supplementary information
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Supplementary Text and Figures
Supplementary Figures 1–10
- 2.
Supplementary Methods Checklist
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