REM sleep phase preference in the crepuscular Octodon degus assessed by selective REM sleep deprivation

Abstract

Study objectives: To determine rapid eye movement (REM) sleep phase preference in a crepuscular mammal (Octodon degus) by challenging the specific REM sleep homeostatic response during the diurnal and nocturnal anticrepuscular rest phases.

Design: We have investigated REM sleep rebound, recovery, and documented REM sleep propensity measures during and after diurnal and nocturnal selective REM sleep deprivations.

Subjects: Nine male wild-captured O. degus prepared for polysomnographic recordings.

Interventions: Animals were recorded during four consecutive baseline and two separate diurnal or nocturnal deprivation days, under a 12:12 light-dark schedule. Three-h selective REM sleep deprivations were performed, starting at midday (zeitgeber time 6) or midnight (zeitgeber time 18).

Measurements and results: Diurnal and nocturnal REM sleep deprivations provoked equivalent amounts of REM sleep debt, but a consistent REM sleep rebound was found only after nocturnal deprivation. The nocturnal rebound was characterized by a complete recovery of REM sleep associated with an augment in REM/total sleep time ratio and enhancement in REM sleep episode consolidation.

Conclusions: Our results support the notion that the circadian system actively promotes REM sleep. We propose that the sleep-wake cycle of O. degus is modulated by a chorus of circadian oscillators with a bimodal crepuscular modulation of arousal and a unimodal promotion of nocturnal REM sleep

Keywords: Octodon degus; REM sleep; REM sleep homeostasis; REM sleep rebound; crepuscular chronotype.

Figure 1

Mean curve of sleep-wake states. Circles correspond to the hourly mean time of each state (± standard error of the mean) obtained during 4 undisturbed days in nine male O. degus. For clarity, the initial and final 6 h are double-plotted. Horizontal black bars indicate dark phase. Hatcheds bar in upper abscissa indicate diurnal (RH06) and nocturnal (RH18) deprivation time. NREM, nonrapid eye movement; REM, rapid eye movement.

Figure 2

REM sleep transition index during diurnal (closed circles) and nocturnal (closed squares) deprivation. Symbols correspond to hourly means (± standard error of the mean). Horizontal dashed lines represent mean baseline values for the corresponding deprivation octant (^aP = 0.0375, ^bP = 0.0875, two-tailed paired t-test with respect to the first and second hour of RH18 deprivation interval, respectively). NREM, nonrapid eye movement; REM, rapid eye movement.

Figure 3

REM sleep homeostasis in response to 3-h diurnal and nocturnal deprivation. The panel compares REM/TST (left) and consolidation rate (right) baseline values (open circles) to diurnal (closed circles) and nocturnal (closed squares) deprivation protocols. The entire day is presented at 3-h time resolution (upper graphs). Collapsed data for the two recovery octants and respective baseline after diurnal and nocturnal deprivation are also shown (lower graphs). Values correspond to the means (± standard error of the mean) obtained in nine O. degus animals in the corresponding octant. *P < 0.05; **P < 0.01, posthoc two-tailed paired t-test with respect to baseline. A hatched bar on the abscissa identifies the diurnal and nocturnal deprivation octants. Horizontal black bars indicate dark phase. REM, rapid eye movement; TST, total sleep time.

Figure 4

Compensation for REM sleep debt after diurnal and nocturnal deprivation. Values correspond to the mean (± standard error of the mean) cumulative difference with respect to baseline values starting at the first hour of REM sleep deprivation and including 6 h of recovery. Diurnal deprivation: closed circles; nocturnal deprivation: closed squares. *P = 0.0435, two-tailed paired t-test of RH18 versus RH06 protocol. Horizontal hatched bars represent deprivation intervals. REM, rapid eye movement.

Figure 5

Comparisons of the REM sleep homeostatic response after diurnal and nocturnal deprivations. Values correspond to the mean (± standard error of the mean) obtained in nine O. degus and are expressed as differences with respect to baseline. Diurnal (closed circles) and nocturnal (closed squares) data were aligned to deprivation interval (hatched bar): preceding octant (Pre), deprivation octant (D, hatched bar), and recovery octants (R1, R2, and collapsed recovery octants R1 + 2). *P < 0.05, **P < 0.01 two-tailed paired t-test of nocturnal versus diurnal differences. REM, rapid eye movement; TST, total sleep time.

Figure 6

Choral model of the sleep-wake cycle (explanation in Discussion section). REM, rapid eye movement.