Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum

Abstract

Multiple evidence in rodents shows that the strength of excitatory synapses in the cerebral cortex and hippocampus is greater after wake than after sleep. The widespread synaptic weakening afforded by sleep is believed to keep the cost of synaptic activity under control, promote memory consolidation, and prevent synaptic saturation, thus preserving the brain’s ability to learn day after day. The cerebellum is highly plastic and the Purkinje cells, the sole output neurons of the cerebellar cortex, are endowed with a staggering number of excitatory parallel fiber synapses. However, whether these synapses are affected by sleep and wake is unknown. Here, we used serial block face scanning electron microscopy to obtain the full 3D reconstruction of more than 7000 spines and their parallel fiber synapses in the mouse posterior vermis. This analysis was done in mice whose cortical and hippocampal synapses were previously measured, revealing that average synaptic size was lower after sleep compared to wake with no major changes in synapse number. Here, instead, we find that while the average size of parallel fiber synapses does not change, the number of branched synapses is reduced in half after sleep compared to after wake, corresponding to ~16% of all spines after wake and ~8% after sleep. Branched synapses are harbored by two or more spines sharing the same neck and, as also shown here, are almost always contacted by different parallel fibers. These findings suggest that during wake, coincidences of firing over parallel fibers may translate into the formation of synapses converging on the same branched spine, which may be especially effective in driving Purkinje cells to fire. By contrast, sleep may promote the off-line pruning of branched synapses that were formed due to spurious coincidences.

Document Details

Document Type
Pub Defense Publication
Publication Date
Dec 28, 2022
Source ID
10.7554/elife.84199

Entities

People

  • Andrea Schroeder
  • Chiara Cirelli
  • Giovanna Maria Spano
  • Giulio Tononi
  • Kelsey Marie Nemec
  • Luisa de Vivo
  • Michele Bellesi
  • Sebastian Weyn Banningh
  • Shannon Sandra Schiereck
  • Sophia S Loschky
  • William Marshall

Organizations

  • Brock University
  • National Institute of Mental Health
  • National Institute of Neurological Disorders and Stroke
  • Office of the Director
  • United States Department of Defense
  • University of Wisconsin–Madison

Tags

Fields of Study

  • Biology

Readers

  • Neuroscience

Technology Areas

  • Microelectronics