Patterns of respiration and heart rate during wakefulness and sleep in elephant seal pups

Abstract

Although breath holding during diving has been studied extensively in seals, the recent observation that these mammals also exhibit long-duration apnea while apparently sleeping has not been systematically examined. This project examined sleep apnea in northern elephant seal pups (Mirounga angustirostris). The animals exhibited a sequential sleep pattern of wakefulness-slow-wave sleep (SWS)-rapid eye movement (REM) sleep that resembled the normal pattern of mammalian sleep. The typical respiratory pattern during sleep in 4-mo-old pups consisted of short periods of continuous breathing separated by periods of apnea of up to 12 min. Several cycles of apnea and eupnea could occur during a single sleep episode. Breathing during a sleep cycle occurred only in SWS, never during REM sleep. The eupneic heart rate was characterized by significant sinus arrhythmia, and the apneic heart rate was similar to the minimum value during normal sinus arrhythmia. Patterns of change in breathing and heart rate associated with wakefulness and sleep were similar in seals sleeping underwater and on land. When sleeping underwater, the seals raised their heads to the surface to breathe without awakening. The changes in heart rate associated with normal sinus arrhythmia, sleep apnea, and diving apnea appear to be similar, suggesting regulation by a common homeostatic control mechanism.

Sleep alterations in mammals: Did aquatic conditions inhibit rapid eye movement sleep?

“…Although this could be true, an important interesting fact is that the majority of both [44][45][46][47][48] . Some pinnipeds, such as Caspian seals (Phoca caspica) [49] , harp seals (Pagophilus groenlandica) [50] and elephant seals (Mirounga angustirostris) [51] , do not exhibit inter-hemispheric asymmetry in slow-wave generation during NREM sleep, suggesting that unihemispheric sleep is typical of fur seals and sea lions but not of all semi-aquatic pinnipeds.…”

“…When harp seals sleep on land, they exhibit ~3.2% REM sleep, but in water they barely go into REM (0.5%) [50] . Castellini et al compared sleep in northern elephant seal pups under dry and wet conditions and demonstrated that the length of REM sleep episodes significantly decreases under wet conditions [51] . Similar characteristics have also been recorded in northern fur seals [55] .…”

“…Among these, the sleep-wakefulness pattern has been studied in only 8, and REM sleep has been reported in all of these. Most of these animals [walrus [47] (Odobenidae), elephant seal [51] and harp seal [50] (Phocidae), and northern fur seal [55] (Otariidae)] exhibit either less REM sleep or shorter REM episodes in water than on land. In another four pinnipeds: gray seal [52] and…”

Apnea stimulates the adaptive response to oxidative stress in elephant seal pups

“…For the purposes of this paper, rest-associated apneas were characterized by breath-holds with eyes closed, occasional facial twitching and lack of body movements (Castellini et al, 1994;Ponganis et al, 2006;Stockard et al, 2007). Following the restassociated apnea trials, animals were then transferred to a shallow water tank and allowed to submerge freely for another 6h.…”

“…Apnea in seals is characterized by a series cardiovascular adjustments (reduction in cardiac output, bradycardia, peripheral vasoconstriction) that allow seals to maximize the use of their oxygen stores but at the same time result in blood oxygen depletion and blood flow redistribution towards obligatory oxygendependent tissues, exposing seals to critical levels of ischemia and hypoxemia (Castellini et al, 1994;Elsner, 1999;Kooyman and Ponganis, 1998;Stockard et al, 2007). At the end of an apnea bout, an increase in cardiac output and ventilation restores blood flow to tissues and blood oxygen content, presenting seals with potential increases in oxidant production and oxidative stress (Elsner et al, 1998;Zenteno-Savín et al, 2002).…”