The cognitive cost of sleep lost

Abstract

A substantial body of literature supports the intuitive notion that a good night's sleep can facilitate human cognitive performance the next day. Deficits in attention, learning & memory, emotional reactivity, and higher-order cognitive processes, such as executive function and decision making, have all been documented following sleep disruption in humans. Thus, whilst numerous clinical and experimental studies link human sleep disturbance to cognitive deficits, attempts to develop valid and reliable rodent models of these phenomena are fewer, and relatively more recent. This review focuses primarily on the cognitive impairments produced by sleep disruption in rodent models of several human patterns of sleep loss/sleep disturbance. Though not an exclusive list, this review will focus on four specific types of sleep disturbance: total sleep deprivation, experimental sleep fragmentation, selective REM sleep deprivation, and chronic sleep restriction. The use of rodent models can provide greater opportunities to understand the neurobiological changes underlying sleep loss induced cognitive impairments. Thus, this review concludes with a description of recent neurobiological findings concerning the neuroplastic changes and putative brain mechanisms that may underlie the cognitive deficits produced by sleep disturbances.

Conflict of interest statement

Conflict of interest

There are no conflicts of interest to disclose for any of the authors related to this work.

Published by Elsevier Inc.

Figures

Fig. 1

Sleepiness is increased in rats following 24 h of total SD, as measured by sleep onset latencies (upper left panel) and electroencephalographic measures of sleep (remaining three panels). All measures shown were obtained during the same 3 h recovery period immediately following 24 h of total SD produced by the movement of the Lafayette activity wheel housing each individual rat (i.e., the total sleep time, NREM, REM sleep data shown were collected during the same 3 h period in which the rat sleep latency trials were conducted). Sleep onset latencies, considered a direct measure of sleepiness, were measured every 30 min during the 3 h recovery period; the electroencephalographic data was collapsed into 30 min bins showing that the percentage of time spent in total sleep time, NREM, and REM sleep all increased significantly during the first part of the 3 h recovery period relative to baseline (modified from Christie, McKenna, et al. (2008)).

Fig. 2

(A) Vigilance (i.e., sustained attention) performance is impaired by sleep disruption. (A) Studies in rats have used either the five choice serial reaction time test (5-CSRT; Cordova et al., 2006), or, more recently, the rat PVT to demonstrate sustained attention impairments produced by either 24 h of total sleep deprivation (SD), or by brain manipulations predicted to elevate sleepiness (e.g., the local perfusion of 300 μM adenosine (AD) in the basal forebrain (BF) region shown here). (B and C) Interindividual differences in the neurobehavioral response to sleep disruption are clearly seen in both rats (B) and humans (C). (B) The left panel shows the baseline (control) and sleep deprived performance differences in eight individual rats; some rats are relatively resilient to the impact of SD on attention performance (e.g., rats S4, S9, S2), whereas other rats are much more susceptible to SD-induced impairments (e.g., S5, S8, S7). The right panel in B shows that when the same group of rats was exposed to two independent trials of 10 h total SD, the number of errors of omission seen in the 5-CSRT was very similar for each individual rat on each of the two trials. Thus, rats that were resilient to the behavioral effects of sleep deprivation were resilient on both of these two 10 h SD treatments (S4, S9, S2), whereas those rats that were susceptible to SD (S5, S8, S7) showed similar impairments in performance during each of the two identical 10 h SD treatments. Panel C shows human findings that are strikingly similar to the rat data shown in the right dside of panel B. Human subjects exposed to two independent trials of 24 h of SD (data were collected during the last 24 h of 36 h total SD) showed interindividual differences in vigilance performance in the PVT (modified from Van Dongen et al. (2004); boxes and diamonds are data from the first and second SD exposures).

Fig. 3

Experimental sleep fragmentation in rats impairs higher-order cognitive function. The attentional set-shifting task is a compound discrimination task that assesses executive function, only performance on the extradimensional shift discrimination (the most difficult discrimination) was impaired following 24 h of SF. The term “executive function” encompasses several cognitive functions thought to be mediated by the frontal cortex (see text for details). Data are expressed as the mean (± SEM) trials to criterion (Y axis) which represents the number of trials required to meet the criterion of six consecutive correct responses on each of the discriminations labeled on the X axis. Rats were assigned to one of three conditions: cage control, movement control, and experimental sleep fragmentation. For details see the original paper from which this figure was modified (McCoy et al., 2007).

Fig. 4

Categorization of memory systems discussed in this review.

Fig. 5

Sleep disruption interferes with spatial memory consolidation. Exposure to experimental sleep fragmentation (SF) for 24 h before spatial learning acquisition trials does not alter spatial memory performance in the water maze (left panel), whereas 24 h of SF exposure after acquisition training robustly impairs memory of the platform location (right panel) in pigmented Fischer/Brown Norway rats. This suggests that, at least in these conditions, spatial memory consolidation is more easily impaired by sleep disruption than is spatial learning. The left panel shows that 24 h of SF before acquisition training had no effect on retention/memory, as measured by percent distance spent in the correct quadrant during a single probe trial run 24 h after the acquisition training. In the learning phase of this experiment, rats were given three blocks of acquisition trials (four trials/block) and there were no learning/acquisition differences in the distance swam to the hidden platform across the blocks of trials among the following groups of rats: Cage Controls; CC; movement controls; MC; 24 h of experimental SF placed either before, or after, the spatial learning acquisition trials (modified from Ward, McCoy, et al. (2009)).

Fig. 6

Impairment of hippocampal long-term potentiation (LTP) may mediate the spatial memory deficits produced by sleep disruption. The left panel shows the virtually complete blockade of hippocampal LTP (i.e., synaptic plasticity) in Sprague–Dawley rats following 24 h of experimental sleep fragmentation (SF; black circles; average responses across a 60 min period are shown for all three groups) compared to movement control (MC; gray circles) and cage control conditions (CC; open circles). The right panel shows examples of the field excitatory postsynaptic potential traces (fEPSP) from individual rats representing each treatment at time points T1 (black) and T2 (gray). Baseline traces (solid lines) were taken from an average of five traces at a midpoint of baseline recording. Post-tetanus traces (broken lines) were taken from an average of five traces 1/2 h after tetanic stimulation. The arrow represents the time point of tetanic stimulation (modified from Tartar et al. (2006)).