Impacts of Sleep Loss versus Waking Experience on Brain Plasticity: Parallel or Orthogonal?. Issue 6 (June 2020)

• Record Type: Journal Article
• Authors: Havekes, Robbert; Aton, Sara J.
• Is Part Of: Trends in neurosciences. Volume 43:Issue 6(2020)
• Page Start: 385
• Page End: 393
• Publication Date: 2020-06
• Subjects: sleep deprivation -- synaptic and structural plasticity -- hippocampus -- neocortex -- synaptic homeostasis hypothesis -- consolidation; Neurology -- Periodicals; Neurophysiology -- Periodicals; Neurobiology -- Periodicals; 612.8
• DOI: 10.1016/j.tins.2020.03.010
• Languages: English
• ISSNs: 0166-2236

Abstract

Abstract : Recent studies on the effects of sleep deprivation on synaptic plasticity have yielded discrepant results. Sleep deprivation studies using novelty exposure as a means to keep animals awake suggests that sleep (compared with wake) leads to widespread reductions in net synaptic strength. By contrast, sleep deprivation studies using approaches avoiding novelty-induced arousal (i.e., gentle handling) suggest that sleep can promote synaptic growth and strengthening. How can these discrepant findings be reconciled? Here, we discuss how varying methodologies for the experimental disruption of sleep (with differential introduction of novel experiences) could fundamentally alter the experimental outcome with regard to synaptic plasticity. Thus, data from experiments aimed at assessing the relative impact of sleep versus wake on the brain may instead reflect the quality of the waking experience itself. The highlighted work suggests that brain plasticity resulting from novel experiences versus wake per se has unique and distinct features. Highlights: Sleep deprivation has been reported to either strengthen or weaken neocortical and hippocampal synapses, with results varying between studies using distinct methods used to keep animals awake. Novelty exposure as a method to promote wake in experimental animals can lead to a net increase in synaptic strength in regions including the hippocampus, M1, and S1. These effects of environmental novelty can be difficult to disentangled from effects of prolonged wake per se . Sleep deprivation using the gentle handling method is aimed at avoiding novelty-induced synaptic plasticity. Gentle-handling sleep deprivation (in contrast to novelty-induced sleep deprivation) can cause a net decrease in synaptic strength in both the hippocampus and the neocortex. Fluctuations in gonadal hormones during the estrus cycle (and biological differences between males and females) can cause large-scale changes in neocortical and hippocampal spine density and synaptic efficacy. These changes can mask the effects of learning or sleep–wake cycles on synapses. Circadian rhythms may modulate synaptic structure and function independent of sleep and wake. Thus, in studies comparing timepoints across the 24-h light–dark cycle, it is nearly impossible to dissociate the impact of circadian time from other factors such as sleep and wake on synaptic plasticity.