For many decades, sleep researchers have sought to determine which species ‘have’ rapid eye movement (REM) sleep. In doing so, they relied predominantly on a template derived from the expression of REM sleep in the adults of a small number of mammalian species. Here, we argue for a different approach that focuses less on a binary decision about haves and have nots, and more on the diverse expression of REM sleep components over development and across species. By focusing on the components of REM sleep and discouraging continued reliance on a restricted template, we aim to promote a richer and more biologically grounded developmental–comparative approach that spans behavioral, physiological, neural, and ecological domains.
Reaching Further Back in Evolutionary Time for the Origins of REM Sleep
There is broad consensus today that both mammals and birds
exhibit REM sleep. If this consensus is correct, we would next
want to know how the similar sleep patterns in such distantly
related groups evolved. Mammals and birds have not shared a
common ancestor for over 300 million years. Did REM sleep
evolve independently in the mammalian and avian lineages, or
was REM sleep present in a common ancestor? Researchers
have long tried to answer this question by recording sleep
behavior and brain activity in non-avian reptiles, amphibians,
and fishes. Unfortunately, this work has often yielded contradictory results [110–112].
Two recent studies in lizards suggest that contradictions in the
earlier literature reflect genuine diversity in the way sleep manifests across reptiles. Shein-Idelson and colleagues [18] recently
reported the existence of REM sleep in the Australian bearded
dragon. Brain activity in this sleeping lizard alternates with astonishing regularity — every 80 seconds — between equal-length
periods composed of sharp waves and wake-like brain activity
with isolated eye movements (called ‘eye twitches’) under closed
eyelids. Limb twitches were not reported. Shortly after this initial
description of REM-like sleep in the dragon, these findings were
replicated in the same species by another research group [113].
This second team also found that another lizard, the tegu (Salvator merianae), exhibits a REM-like sleep state, including distinct
brain activity associated with eye movements (rare limb twitches
were observed but were not unambiguously related to the state).
However, the two species showed marked differences in the
REM-like sleep state. Whereas brain activity in the dragon was
characterized by high power across a broad range of frequencies (10–30 Hz), similar to that observed during wakefulness, brain activity in the tegu exhibited a distinct 15-Hz peak
not found during wake. Moreover, in contrast to the precisely
regular alternation between sleep states in dragons, tegus
showed no such regularity.
Although the reasons for the stark differences in the two lizards
are unknown, the studies further underscore the challenge of
finding consensus on the defining features of REM sleep: if these
two lizard species exhibit such diversity, what should we expect
as more reptiles are studied? Will their sleep patterns converge
on a shared set of characteristics that resemble REM sleep in
mammals and birds? And how should we interpret previous
studies that failed to detect a REM-like state in crocodilians,
the closest living relatives to birds, and in turtles, the sister
group to birds and crocodilians [110,111]? Although it is possible
that the earlier studies in crocodilians and turtles were somehow
flawed, we should not simply ignore these exceptions. In the
end, when attempting to trace the evolution of REM sleep, we
must account for the full taxonomic diversity of sleep and its
seemingly patchy phylogenetic distribution.
But now, again, yet another recent paper claims to have
pushed the evolutionary origins of REM and non-REM sleep
even further back in time — to 450 million years ago. Using
larval zebrafish (Danio rerio), Leung and colleagues [9] developed an impressive whole-body fluorescence method to measure neural activity throughout the brain of these transparent
animals while restrained in agar. In addition to brain activity,
they measured muscle activity, eye movements, and heart
rate. Two sleep states were reported: the first state, most
clearly defined after sleep deprivation, is characterized by
synchronous bursts of activity alternating with periods of
silence in the dorsal pallium (a homologue of neocortex), reminiscent of the bursts of activity during mammalian and avian
non-REM sleep (albeit on a much slower timescale). The onset
of the second spontaneous state is characterized by a single
contraction of the trunk muscles lasting 10–15 seconds and a
single, prolonged (up to 5 min) burst of activity that propagates
through the central nervous system. The authors call this state
propagating wave sleep (PWS). It should be noted that the longlasting muscle contractions that occur at the onset of brain
activation are unlike the brief twitches that characterize
mammalian REM sleep. Also, brain activity after a burst in the
zebrafish was suppressed below waking levels for more than
20 minutes. Another peculiarity is that rapid eye movements
did not occur during spontaneous PWS, even though the eyes
moved freely during wakefulness. Thus, although these bursts
of activation are fascinating, it is unclear if and how they relate
to REM sleep in mammals and birds.
Additional hints suggest that components of REM sleep
emerged even farther back in evolutionary time. For example,
a variety of insects — from larval flies to adult bees — twitch their
antennae during states that resemble sleep [114–117]. But such
observations alone do not constitute clear evidence of homology
between invertebrate and vertebrate sleep states. After all, not all
movements during sleep are twitches; nor do we have sufficient
information about the nervous systems of sleeping insects to understand what these twitch-like movements represent.
Twitching is also apparent in resting cuttlefish (Sepia officinalis), but in a way that is remarkable and unique. When awake and
swimming, cuttlefish exhibit choreographed patterns of coloration for communication and camouflage [118]. The changes
in color and pattern are mediated by chromatophores —
pigment-containing skin cells that are controlled by striated
muscle. While apparently asleep, cuttlefish initially rest motionless on the seafloor with their pupils constricted and their coloration cryptically matching the surrounding substrate [119,120].
Such periods of quiet rest are occasionally interrupted by prolonged (2–3 minute) bouts of twitching of the tentacles, eyes,
and — astoundingly — the chromatophores, resulting in rapid
changes in coloration and patterning that announce, rather
than conceal, their presence (similar patterns of chromatophore
activation during apparent sleep have been reported in the
octopus [121,122]). Although arousal thresholds have not been
assessed to rule out the possibility that the cuttlefish behaviors
reflect brief awakenings, the patterns of chromatophore activation bear little resemblance to what is observed when cuttlefish
are clearly awake. If, in fact, they are asleep, further work on cuttlefish may provide novel insights into the evolution of REM-like
sleep states, especially given the independent evolution of complex brains, behavior, and cognition in cephalopods [123]. When
combined with research on relatively ‘simple’ mollusks [124], this
research raises the hope of revealing the independent and
convergent evolution of individual components that comprise
REM sleep.
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