24 hours of sleep deprivation in the rat increases sleepiness and decreases vigilance: introduction of the rat-psychomotor vigilance task

Abstract

A novel animal-analog of the human psychomotor vigilance task (PVT) was validated by subjecting rats to 24 h of sleep deprivation (SD) and examining the effect on performance in the rat-PVT (rPVT), and a rat multiple sleep latency test (rMSLT). During a three-phase (separate cohorts) crossover design, vigilance performance in the rPVT was compared with 24 h SD-induced changes in sleepiness assessed by polysomnographic evaluation and the rMSLT. Twenty-four hours of SD was produced by brief rotation of activity wheels at regular intervals in which the animals resided throughout the experiment. In the rPVT experiment, exercise controls (EC) experienced the same overall amount of locomotor activity as during SD, but allowed long periods of undisturbed sleep. After 24 h SD response latencies slowed, and lapses increased significantly during rPVT performance when compared with baseline and EC conditions. During the first 3 h of the recovery period following 24 h SD, polysomnographic measures indicated sleepiness. Latency to fall asleep after 24 h SD was assessed six times during the first 3 h after SD. Rats fell asleep significantly faster immediately after SD, than after non-SD baseline sessions. In conclusion, 24 h of SD in rats increased sleepiness, as indicated by polysomnography and the rMSLT, and impaired vigilance as measured by the rPVT. The rPVT closely resembles the human PVT test widely used in human sleep research and will assist investigation of the neurobiologic mechanisms that produce vigilance impairments after sleep disruption.

Figure 1. Vigilance performance in the rPVT is impaired by 24 h of sleep deprivation (SD)

Panel A. Response latencies are significantly slowed after 24 h of total sleep deprivation (SD), when compared to either baseline (no wheel movement), or 24 h of exercise control (EC), ** = p<0.005. Panel B. The mean number of lapses, including omissions, increased significantly after 24-h SD, when compared to either 24-h EC or 24-h undisturbed baseline. * = p<0.05. Panel C. The number of premature errors (responses during the inter-trial interval) does not change as a function of experimental condition. Panel D. The number of rewarded nose-pokes is somewhat lower after 24 h SD, but this effect was not significant (p=0.08). The data plotted are means ±SEM.

Figure 2. EEG measures indicated sleepiness during undisturbed recovery (Post-SD, 11AM-2PM) following sleep deprivation (SD, 11AM-11AM))

NREM sleep episode duration (Panel A), and normalized NREM delta values (Panel B) were elevated in the recovery period. A significant decrease in the number of awakenings per hour was noted (Panel C). Panels D, E, and F demonstrate significant increases of the hourly amounts of NREM, REM, and total sleep time, expressed as percentages of total time per hour. Baseline data are represented by closed triangles, and post-SD values by crosses. The data plotted are means ±SEM. Each animal was used as its own control. Asterisks indicate significant pairwise post-hoc comparisons between baseline and post-SD values, Bonferroni corrected.

Figure 3. The rMSLT (Post-SD, 11AM-2PM) revealed sleep deprivation (SD) effects on sleepiness

Sleep latencies were significantly decreased following 24h of SD (Panel A; 11AM-11AM). Sleep rebound was evident during the period of the rMSLT trials when the animal was left undisturbed. NREM sleep % (Panel B), REM sleep % (Panel C), and total sleep % amounts per hour (Panel 3D) were all elevated following SD, represented as percentages of total time per hour. Baseline data are represented by closed triangles, and post-SD values by crosses. The data plotted are means ±SEM. Each animal was used as its own control. Asterisks indicate significant pairwise post-hoc comparisons between baseline and post-SD values, Bonferroni corrected.