Loss of circadian organization of sleep and wakefulness during hibernation

Abstract

[851][852][853][854][855][856][857][858] 1997]. Animals maintained under constant conditions continued to display circadian rhythms in both sigma activity and brain temperature throughout euthermic intervals, whereas sleep and wakefulness showed no circadian organization. Instead, sleep and wakefulness were distributed according to a 6-h ultradian rhythm. SWA, NREM sleep bout length, and sigma activity responded homeostatically to the ultradian sleep-wake pattern. We suggest that the loss of sleep-wake consolidation in ground squirrels during the hibernation season may be related to the greatly decreased locomotor activity during the hibernation season and may be necessary for maintenance of multiday torpor bouts characteristic of hibernating species. slow-wave activity; sigma activity; circadian rhythms; circannual rhythms; Spermophilus lateralis THE PURPOSE OF THIS STUDY was to determine if there is a loss or a lessening of circadian control over sleep during the hibernation season in golden-mantled ground squirrels. The reason this question is posed is that torpor and hibernation appear to be evolutionary extensions of nonrapid eye movement (NREM) sleep (28,56). Torpid animals are predominantly in a NREM sleeplike state for many days at a time. In nonhibernators and in hibernators during the active season, sleep and wakefulness are organized into a daily cycle by the circadian system. It appears that the circadian system tends to consolidate wakefulness during a portion of the circadian cycle, thus creating a sleep need that is expressed when the circadian promotion of wakefulness is relaxed (2, 14). When an animal enters torpor, the inactive or rest phase of its daily cycle expands to the total exclusion of the active phase. Therefore, the circadian system may be suppressed or the wake-consolidating function of the circadian system may be inactivated to allow the multiday bouts of torpor that characterize hibernation.Cortical electroencephalographic (EEG) activity and other physiological variables such as body (T b ) and brain (T br ) temperatures reflect modulation by both sleep and circadian mechanisms, and therefore these variables were recorded in this study to investigate changes in sleep and circadian control associated with hibernation. Cortical EEG activity in the range of 10-15 Hz, called sigma activity, is the hallmark of NREM sleep spindles (44). Sigma activity is elevated in light NREM sleep during the active phase and is low in deep, consolidated sleep during the inactive or rest phase of the circadian cycle (50). Sigma activity is determined by both circadian and sleep homeostatic factors (9, 12).Cortical EEG activity in the range of 1-4 Hz, called delta activity or slow-wave activity (SWA), is the hallmark of the depth of NREM sleep. SWA is therefore the standard measure of sleep homeostasis because it is primarily determined by the duration of prior wakefulness (2) and is minimally influenced by the circadian system (9). Sleep deprivation results in elevated SWA during recovery sleep (11,19,...

Hibernation and Circadian Rhythms of Body Temperature in Free-Living Arctic Ground Squirrels

“…The persistence and potential function of circadian oscillators during hibernation is contentious (reviewed in Larkin et al 2002). Very low-amplitude (0.1Њ-0.2ЊC) circadian T b rhythms with a broad range of period lengths have been detected during deep torpor in hibernators held under constant dark in captive conditions (Grahn et al 1994;Florant et al 2000;Larkin et al 2002;Ruby et al 2002), whereas others have failed to detect persistent rhythms in either captive or free-living animals (Florant et al 2000;Hut et al 2002;Gür et al 2009;Tøien et al 2011;Williams et al 2012).…”

“…Very low-amplitude (0.1Њ-0.2ЊC) circadian T b rhythms with a broad range of period lengths have been detected during deep torpor in hibernators held under constant dark in captive conditions (Grahn et al 1994;Florant et al 2000;Larkin et al 2002;Ruby et al 2002), whereas others have failed to detect persistent rhythms in either captive or free-living animals (Florant et al 2000;Hut et al 2002;Gür et al 2009;Tøien et al 2011;Williams et al 2012). Florant et al (2000) found that T b rhythms were due to oscillations in T a within the chamber, whereas Ruby et al (2002) concluded that the T b oscillations were independent of T a .…”

Circadian Entrainment to Temperature, But Not Light, in the Isolated Suprachiasmatic Nucleus

“…Brains in organisms such as mice, bats, and ground squirrels can drop below 25°C during bouts of torpor or hibernation and may still express circadian rhythms in body temperature (Hut et al 2002;Ruby et al 2002). Recently, Larkin et al (2002) provided compelling evidence that the circadian regulation of brain temperature continues, albeit at much reduced amplitude, in the hibernating squirrel SCN at ambient temperatures as low as 9°C. These animals, however, lost their circadian rhythm in slow-wave sleep.…”

Homeostatic regulation of sleep in arrhythmic Siberian hamsters

“…SWA was normalized to the 24-h mean NREMS SWA in baseline for each animal. NREMS bouts were calculated according to previously published criteria (27). In short, an NREMS bout started with a first 10-s epoch scored as NREMS and lasted until three consecutive 10-s epochs of either wakefulness or REM sleep were encountered.…”