Acute Partial Sleep Deprivation Negatively Affects Object Pattern Separation in Healthy Adults

Abstract

Introduction. Insufficient sleep is a growing problem in the modern 24/7 society, and thus uncovering its neurocognitive consequences is crucial. Partial sleep deprivation is known to cause rodents specific and significant impairments in pattern separation, a function of the dentate gyrus in the hippocampus. Humans are also known to experience hippocampal memory deficits after reductions of sleep quality or quantity. However, the role of the dentate gyrus in these memory impairments has not yet been explored in human subjects.

Method. The sample was randomly divided into sleep deprivation (n = 20) and control conditions (n = 19). A week after a short familiarization session, the participants underwent respectively either one night of extended wakefulness (slept between 3am-6:30am) or normal sleep (slept until 6:30am but chose their own bedtime). At 8am, both groups were cognitively tested with a battery assessing a range of memory processes including verbal, spatial, and working memory. Their pattern separation capacity was measured in two modalities; object and spatial, using previously validated tasks dependent on the dentate gyrus. Independent samples’ t-tests and ANOVAs were used to compare the groups on individual tasks. Additionally, the factor structure of the memory scores was explored using a principal component analysis.

Results. Comparisons between the scores of the two groups mostly yielded non-significant trends toward sleep deprivation impairing performance, and provided no evidence for dentate gyrus -specificity of the impairments. Spatial memory alone indicated clear proof of deficit, as both immediate and delayed recall of spatial locations was significantly weaker in the sleep deprived group. When exploring the factor structure of the scores in the test battery, the pattern separation tasks loaded on one, spatial processing of complex figures on another, and verbal learning on a third component.

Discussion. The preliminary data analysis of the current study found some supporting evidence for separate hippocampal processing pathways, but failed to replicate previous findings on the detrimental effects of sleep deprivation. However, it must be noted that this is a prelusive conclusion drawn on a smaller-than-desired sample size due to the impact of the current pandemic situation on the recruitment of research participants. As previous literature on sleep deprivation-induced memory deficits has mostly utilized longer sleep deprivation paradigms, there is much to be discovered about acute short sleep restriction. Moreover, translational findings about the dentate gyrus - specificity of these deficits in humans will require some further exploration. On the basis of this preliminary study, future research could benefit from exploring longitudinal within-subject designs, and adding neuroimaging techniques in order to measure compensatory processes such as additional neural activation. Afterall, acute partial sleep deprivation affects many of us, and it remains an important question whether one night of shorter sleep can significantly disrupt hippocampal memory and learning.