Desynchronization of slow oscillations in the basal ganglia during natural sleep

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

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

Abstract

Slow oscillations of neuronal activity alternating between firing and silence are a hallmark of slow-wave sleep (SWS). These oscillations reflect the default activity present in all mammalian species, and are ubiquitous to anesthesia, brain slice preparations, and neuronal cultures. In all these cases, neuronal firing is highly synchronous within local circuits, suggesting that oscillation–synchronization coupling may be a governing principle of sleep physiology regardless of anatomical connectivity. To investigate whether this principle applies to overall brain organization, we recorded the activity of individual neurons from basal ganglia (BG) structures and the thalamocortical (TC) network over 70 full nights of natural sleep in two vervet monkeys. During SWS, BG neurons manifested slow oscillations (∼0.5 Hz) in firing rate that were as prominent as in the TC network. However, in sharp contrast to any neural substrate explored thus far, the slow oscillations in all BG structures were completely desynchronized between individual neurons. Furthermore, whereas in the TC network single-cell spiking was locked to slow oscillations in the local field potential (LFP), the BG LFP exhibited only weak slow oscillatory activity and failed to entrain nearby cells. We thus show that synchrony is not inherent to slow oscillations, and propose that the BG desynchronization of slow oscillations could stem from its unique anatomy and functional connectivity. Finally, we posit that BG slow-oscillation desynchronization may further the reemergence of slow-oscillation traveling waves from multiple independent origins in the frontal cortex, thus significantly contributing to normal SWS.

Original languageAmerican English
Pages (from-to)E4274-E4283
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number18
DOIs
StatePublished - 1 May 2018

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. We thank Dr. Yaron Dagan and Dr. Tamar Ravins-Yaish for assistance with animal care, and Dr. Atira Bick and Dr. Adi Payis for assistance with MRI scanning. We thank Anatoly Shapochnikov, Dr. Hila Gabbay, Dr. Sharon Freeman, Dr. Uri Werner-Reiss, and Esther Singer for general assistance. We thank Dr. Marc Deffains for his assistance in neuronal recordings, and Dr. Yuval Nir for his assistance in planning the experiments and the analysis of the results. This work was supported by grants from the European Research Council, Israel Science Foundation, and Rosetrees Trust (to H.B.).

Funding Information:
We thank Dr. Yaron Dagan and Dr. Tamar Ravins-Yaish for assistance with animal care, and Dr. Atira Bick and Dr. Adi Payis for assistance with MRI scanning. We thank Anatoly Shapochnikov, Dr. Hila Gabbay, Dr. Sharon Freeman, Dr. Uri Werner-Reiss, and Esther Singer for general assistance. We thank Dr. Marc Deffains for his assistance in neuronal recordings, and Dr. Yuval Nir for his assistance in planning the experiments and the analysis of the results. This work was supported by grants from the European Research Council, Israel Science Foundation, and Rosetrees Trust (to H.B.).

Publisher Copyright:
© 2018 National Academy of Sciences. All rights reserved.

Keywords

  • Basal ganglia
  • Desynchronization
  • Nonhuman primate
  • Sleep
  • Slow oscillations

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