Impacts of Sleep Loss versus Waking Experience on Brain Plasticity: Parallel or Orthogonal?

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.

Keywords: consolidation; hippocampus; neocortex; sleep deprivation; synaptic and structural plasticity; synaptic homeostasis hypothesis.

Figure 1.. Different Methodologies for Induction of Sleep Deprivation Result in Divergent Effects on Synaptic Strength.

In the past few years, studies have reported that prolonged wake either increases net spine numbers and synaptic strength or (conversely) decreases synaptic strength. These discrepant observations could be explained by examining the methodology used in these studies to enforce wake. We propose a hypothetical scenario in which the magnitude of novel sensory stimuli (associated with both sleep deprivation methods) and prolonged wake itself have opposite effects on net synaptic strength. These effects (relative to sleep) are shown in the graph at the left. Provision of novel sensory stimuli alone (broken red line) leads to maximal increases in net synaptic strength in the neocortex and hippocampus. This increase is partially mitigated by the effects of wake itself (broken blue line) during novel-stimulus-induced sleep deprivation (unbroken red line). This is because prolonged wake alone (broken blue line) tends to reduce synaptic strength. Gentle handling (mild sensory stimulation) leads to a more moderate increase in net synaptic strength in the neocortex and hippocampus (broken violet line), which is similarly mitigated by the effects of wake itself (broken blue line) during gentle-handling sleep deprivation (unbroken violet line).