Entrainment to sleep spindles reflects dissociable patterns of connectivity between cortex and basal ganglia

Aviv D. Mizrahi-Kliger*, Alexander Kaplan, Zvi Israel, Hagai Bergman

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Sleep spindles are crucial for learning in the cortex and basal ganglia (BG) because they facilitate the reactivation of previously active neuronal ensembles. Studying field potentials (FPs) and spiking in the cortex and BG during sleep in non-human primates following pre-sleep learning, we show that FP sleep spindles are widespread in the BG and are similar to cortical spindles in morphology, spectral content, and response to the pre-sleep task. Further, BG spindles are concordant with electroencephalogram (EEG) spindles and associated with increased cortico-BG correlation. However, spindles across the BG differ markedly in their entrainment of local spiking. The spiking activity of striatal projection neurons exhibits consistent phase locking to striatal and EEG spindles, producing phase windows of peaked cross-region spindling. In contrast, firing in other BG nuclei is not entrained to either local or EEG sleep spindles. These results suggest corticostriatal synapses as the main hub for offline cortico-BG communication.

Original languageAmerican English
Article number111367
JournalCell Reports
Volume40
Issue number12
DOIs
StatePublished - 20 Sep 2022

Bibliographical note

Funding Information:
We thank Dr. Yaron Dagan and Dr. Tamar Ravins-Yaish for assistance with animal care. We thank Anatoly Shapochnikov, Dr. Hila Gabbay, Dr. Sharon Freeman, and Dr. Uri Werner-Reiss for general assistance. We thank Dr. Marc Deffains for his assistance in neuronal recordings. Finally, we would like to thank Prof. Yuval Nir and his team members for their extensive assistance in planning the experiments, analyzing the data, and finalizing the manuscript. This work was supported by grants from the Israel Science Foundation , Israel-China binational scientific foundation , and the ReTune Germany Collaborative center TRR295 (to H.B.).

Publisher Copyright:
© 2022 The Authors

Keywords

  • CP: Neuroscience
  • basal ganglia
  • corticostriatal network
  • learning and memory
  • sleep
  • sleep spindles

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