Symmetrical Serotonin Release during Asymmetrical Slow-Wave Sleep: Implications for the Neurochemistry of Sleep–Waking States

Abstract

On land, fur seals predominately display bilaterally synchronized electroencephalogram (EEG) activity during slow-wave sleep (SWS), similar to that observed in all terrestrial mammals. In water, however, fur seals exhibit asymmetric slow-wave sleep (ASWS), resembling the unihemispheric slow-wave sleep of odontocetes (toothed whales). The unique sleeping pattern of fur seals allows us to distinguish neuronal mechanisms mediating EEG changes from those mediating behavioral quiescence. In a prior study we found that cortical acetylcholine release is lateralized during ASWS in the northern fur seal, with greater release in the hemisphere displaying low-voltage (waking) EEG activity, linking acetylcholine release to hemispheric EEG activation (Lapierre et al. 2007). In contrast to acetylcholine, we now report that cortical serotonin release is not lateralized during ASWS. Our data demonstrate that bilaterally symmetric levels of serotonin are compatible with interhemispheric EEG asymmetry in the fur seal. We also find greatly elevated levels during eating and hosing the animals with water, suggesting that serotonin is more closely linked to bilateral variables, such as axial motor and autonomic control, than to the lateralized cortical activation manifested in asymmetrical sleep.

Fur Seals Suppress REM Sleep for Very Long Periods without Subsequent Rebound

“…Slow-wave sleep (SWS) and REM sleep on land occurred when fur seals were lying or sitting (Figures 1 and 2). In agreement with our prior studies [9][10][11], fur seals on land displayed REM and nonREM sleep. SWS includes both bilateral SWS (BSWS) and unihemispheric SWS (USWS; see Figure 1E and Table S2), the latter resembling the unihemispheric slowwave pattern seen in dolphins, with unilateral eye opening.…”

“…Two longer wires were implanted subcutaneously to record electrocardiogram (EKG). Surgical procedures were described in detail in our prior publications (e.g., [9,10,38]). After implantation, the seals were returned to the pool and allowed at least 5 days to recover before the experiments started.…”

“…The behavior of seals was scored in 20 s epochs. Behavioral features of active waking (AW), quiet waking (QW), slow wave sleep (SWS) and REM sleep in fur seals while on land have been described in our prior publications [8][9][10]38].…”

Neuronal Mechanisms for Sleep/Wake Regulation and Modulatory Drive

“…Northern fur seals (Callorhinus ursinus) show unihemispheric sleep preferentially while sleeping in the water (Lyamin et al, 2017). Acetylcholine release was found to be lateralized and tightly linked to the hemisphere that was awake, while histamine, serotonin, and noradrenaline were found to be synchronously released from both the awake and asleep hemispheres (Lapierre et al, 2013;Lapierre et al, 2007;Lyamin et al, 2016). These findings suggest that acetylcholine is responsible for unihemispheric EEG activation, and future studies modulating the activity of cholinergic neurons would provide causal evidence.…”

Sleep in the northern fur seal

“…In terrestrial animals cortical and subcortical release of monoamines (histamine, serotonin and noradrenaline) decreases at the transition from active wakefulness (the state with the greatest levels of both muscle tone and activity), to quiet wakefulness, bilateral SWS and then decreases further in REM sleep (the state of immobility with the most substantial reduction in muscle tone; [32-34]). This was also the case in the fur seal [35, 36]. Also similar to terrestrial mammals [37,38], cortical release of acetylcholine (Ach) in the seal during waking and REM sleep was greater than in bilateral SWS [39].…”