Hippocampal gamma‐slow oscillation coupling in macaques during sedation and sleep

Abstract

Behavioral and neurophysiological evidence suggests that the slow (≤1 Hz) oscillation (SO) during sleep plays a role in consolidating hippocampal (HIPP)‐dependent memories. The effects of the SO on HIPP activity have been studied in rodents and cats both during natural sleep and during anesthetic administration titrated to mimic sleep‐like slow rhythms. In this study, we sought to document these effects in primates. First, HIPP field potentials were recorded during ketamine‐dexmedetomidine sedation and during natural sleep in three rhesus macaques. Sedation produced regionally‐specific slow and gamma (∼40 Hz) oscillations with strong coupling between the SO phase and gamma amplitude. These same features were seen in slow‐wave sleep (SWS), but the coupling was weaker and the coupled gamma oscillation had a higher frequency (∼70 Hz) during SWS. Second, electrical stimuli were delivered to HIPP afferents in the parahippocampal gyrus (PHG) during sedation to assess the effects of sleep‐like SO on excitability. Gamma bursts after the peak of SO cycles corresponded to periods of increased gain of monosynaptic connections between the PHG and HIPP. However, the two PHG‐HIPP connectivity gains during sedation were both substantially lower than when the animal was awake. We conclude that the SO is correlated with rhythmic excitation and inhibition of the PHG‐HIPP network, modulating connectivity and gamma generators intrinsic to this network. Ketamine‐dexmedetomidine sedation produces a similar effect, but with a decreased contribution of the PHG to HIPP activity and gamma generation.

Document Details

Document Type
Pub Defense Publication
Publication Date
Jul 12, 2017
Source ID
10.1002/hipo.22757

Entities

People

  • Alexander Proekt
  • Andrew G Richardson
  • Eric D. Hudgins
  • Jan Van Der Spiegel
  • Joel M Stein
  • Max B Kelz
  • Milin Zhang
  • Pauline K. Weigand
  • Sandhitsu R. Das
  • Timothy H. Lucas
  • Xilin Liu

Organizations

  • Defense Advanced Research Projects Agency
  • Tsinghua University
  • University of Pennsylvania

Tags

Fields of Study

  • Biology

Readers

  • Circadian Sleep-Wake Regulation and Chronobiology
  • Neuroscience
  • Nuclear and Radiation Engineering.