Dynamic interaction of spindles and gamma activity during cortical slow oscillations and its modulation by subcortical afferents

PLoS One. 2013 Jul 2;8(7):e67540. doi: 10.1371/journal.pone.0067540. Print 2013.

Abstract

Slow oscillations are a hallmark of slow wave sleep. They provide a temporal framework for a variety of phasic events to occur and interact during sleep, including the expression of high-frequency oscillations and the discharge of neurons across the entire brain. Evidence shows that the emergence of distinct high-frequency oscillations during slow oscillations facilitates the communication among brain regions whose activity was correlated during the preceding waking period. While the frequencies of oscillations involved in such interactions have been identified, their dynamics and the correlations between them require further investigation. Here we analyzed the structure and dynamics of these signals in anesthetized rats. We show that spindles and gamma oscillations coexist but have distinct temporal dynamics across the slow oscillation cycle. Furthermore, we observed that spindles and gamma are functionally coupled to the slow oscillations and between each other. Following the activation of ascending pathways from the brainstem by means of a carbachol injection in the pedunculopontine nucleus, we were able to modify the gain in the gamma oscillations that are independent of the spindles while the spindle amplitude was reduced. Furthermore, carbachol produced a decoupling of the gamma oscillations that are dependent on the spindles but with no effect on their amplitude. None of the changes in the high-frequency oscillations affected the onset or shape of the slow oscillations, suggesting that slow oscillations occur independently of the phasic events that coexist with them. Our results provide novel insights into the regulation, dynamics and homeostasis of cortical slow oscillations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Waves / drug effects
  • Brain Waves / physiology*
  • Carbachol / pharmacology
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / physiology*
  • Cholinergic Agonists / pharmacology
  • Electroencephalography
  • Injections, Intraventricular
  • Male
  • Neurons / drug effects
  • Neurons / physiology*
  • Pedunculopontine Tegmental Nucleus / drug effects
  • Pedunculopontine Tegmental Nucleus / physiology*
  • Rats
  • Rats, Sprague-Dawley
  • Sleep / drug effects
  • Sleep / physiology*
  • Wakefulness / drug effects
  • Wakefulness / physiology*

Substances

  • Cholinergic Agonists
  • Carbachol