Interhemispheric competition during sleep

Nature. 2023 Apr;616(7956):312-318. doi: 10.1038/s41586-023-05827-w. Epub 2023 Mar 22.

Abstract

Our understanding of the functions and mechanisms of sleep remains incomplete, reflecting their increasingly evident complexity1-3. Likewise, studies of interhemispheric coordination during sleep4-6 are often hard to connect precisely to known sleep circuits and mechanisms. Here, by recording from the claustra of sleeping bearded dragons (Pogona vitticeps), we show that, although the onsets and offsets of Pogona rapid-eye-movement (REMP) and slow-wave sleep are coordinated bilaterally, these two sleep states differ markedly in their inter-claustral coordination. During slow-wave sleep, the claustra produce sharp-wave ripples independently of one another, showing no coordination. By contrast, during REMP sleep, the potentials produced by the two claustra are precisely coordinated in amplitude and time. These signals, however, are not synchronous: one side leads the other by about 20 ms, with the leading side switching typically once per REMP episode or in between successive episodes. The leading claustrum expresses the stronger activity, suggesting bilateral competition. This competition does not occur directly between the two claustra or telencephalic hemispheres. Rather, it occurs in the midbrain and depends on the integrity of a GABAergic (γ-aminobutyric-acid-producing) nucleus of the isthmic complex, which exists in all vertebrates and is known in birds to underlie bottom-up attention and gaze control. These results reveal that a winner-take-all-type competition exists between the two sides of the brain of Pogona, which originates in the midbrain and has precise consequences for claustrum activity and coordination during REMP sleep.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Attention
  • Birds / physiology
  • Brain* / anatomy & histology
  • Brain* / physiology
  • Fixation, Ocular
  • Functional Laterality* / physiology
  • Lizards* / anatomy & histology
  • Lizards* / physiology
  • Mesencephalon / physiology
  • Sleep* / physiology
  • Sleep, REM / physiology
  • Sleep, Slow-Wave / physiology
  • Time Factors
  • gamma-Aminobutyric Acid / metabolism

Substances

  • gamma-Aminobutyric Acid