A mammal and bird's-eye-view of the pupil during sleep and wakefulness.

Besides regulating the amount of light that reaches the retina, fluctuations in pupil size also occur in isoluminant conditions during accommodation, during movement and in relation to cognitive workload, attention and emotion. Recent studies in mammals and birds revealed that the pupils are also highly dynamic in the dark during sleep. However, despite exhibiting similar sleep states (rapid eye movement [REM] and non-REM [NREM] sleep), wake and sleep state-dependent changes in pupil size are opposite between mammals and birds, due in part to differences in the type (striated vs. smooth) and control of the iris muscles. Given the link between pupil dynamics and cognitive processes occurring during wakefulness, sleep-related changes in pupil size might indicate when related processes are occurring during sleep. Moreover, the divergent pupillary behaviour observed between mammals and birds raises the possibility that changes in pupil size in birds are a readout of processes not reflected in the mammalian pupil.

Wide-spread brain activation and reduced CSF flow during avian REM sleep.

Mammalian sleep has been implicated in maintaining a healthy extracellular environment in the brain. During wakefulness, neuronal activity leads to the accumulation of toxic proteins, which the glymphatic system is thought to clear by flushing cerebral spinal fluid (CSF) through the brain. In mice, this process occurs during non-rapid eye movement (NREM) sleep. In humans, ventricular CSF flow has also been shown to increase during NREM sleep, as visualized using functional magnetic resonance imaging (fMRI). The link between sleep and CSF flow has not been studied in birds before. Using fMRI of naturally sleeping pigeons, we show that REM sleep, a paradoxical state with wake-like brain activity, is accompanied by the activation of brain regions involved in processing visual information, including optic flow during flight. We further demonstrate that ventricular CSF flow increases during NREM sleep, relative to wakefulness, but drops sharply during REM sleep. Consequently, functions linked to brain activation during REM sleep might come at the expense of waste clearance during NREM sleep.

The evolution and diversification of sleep.

The evolutionary origins of sleep and its sub-states, rapid eye movement (REM) and non-REM (NREM) sleep, found in mammals and birds, remain a mystery. Although the discovery of a single type of sleep in jellyfish suggests that sleep evolved much earlier than previously thought, it is unclear when and why sleep diversified into multiple types of sleep. Intriguingly, multiple types of sleep have recently been found in animals ranging from non-avian reptiles to arthropods to cephalopods. Although there are similarities between these states and those found in mammals and birds, notable differences also exist. The diversity in the way sleep is expressed confounds attempts to trace the evolution of sleep states, but also serves as a rich resource for exploring the functions of sleep.

Pupillary behavior during wakefulness, non-REM sleep, and REM sleep in birds is opposite that of mammals.

Mammalian pupils respond to light1,2 and dilate with arousal, attention, cognitive workload, and emotions,3 thus reflecting the state of the brain. Pupil size also varies during sleep, constricting during deep non-REM sleep4-7 and dilating slightly during REM sleep.4-6 Anecdotal reports suggest that, unlike mammals, birds constrict their pupils during aroused states, such as courtship and aggression,8-10 raising the possibility that pupillary behavior also differs between mammals and birds during sleep. Here, we measured pupil size in awake pigeons and used their translucent eyelid to investigate sleep-state-dependent changes in pupil size. Male pigeons constricted their pupils during courtship and other male-female interactions but not while engaging in other waking behaviors. Unlike mouse pupils, the pigeons' pupils were dilated during non-REM sleep, while over 1,000 bursts of constriction and relaxation, which we call rapid iris movements (RIMs), occurred primarily during REM sleep. Consistent with the avian iris being composed largely of striated muscles,11-15 rather than smooth muscles, as in mammals, pharmacological experiments revealed that RIMs are mediated by nicotinic cholinergic receptors in the iris muscles. Despite receiving input from a parasympathetic nucleus, but consistent with its striated nature, the avian iris sphincter muscle behaves like skeletal muscles controlled by the somatic nervous system, constricting during courtship displays, relaxing during non-REM sleep, and twitching during REM sleep. We speculate that during wakefulness, pupillary constrictions are involved in social communication, whereas RIMs occurring during REM sleep might maintain the efficacy of this motor system and/or reflect the processing of associated memories.

Comparative Perspectives that Challenge Brain Warming as the Primary Function of REM Sleep.

Rapid eye movement (REM) sleep is a paradoxical state of wake-like brain activity occurring after non-REM (NREM) sleep in mammals and birds. In mammals, brain cooling during NREM sleep is followed by warming during REM sleep, potentially preparing the brain to perform adaptively upon awakening. If brain warming is the primary function of REM sleep, then it should occur in other animals with similar states. We measured cortical temperature in pigeons and bearded dragons, lizards that exhibit NREM-like sleep and REM-like sleep with brain activity resembling wakefulness. In pigeons, cortical temperature decreased during NREM sleep and increased during REM sleep. However, brain temperature did not increase when dragons switched from NREM-like to REM-like sleep. Our findings indicate that brain warming is not a universal outcome of sleep states characterized by wake-like activity, challenging the hypothesis that their primary function is to warm the brain in preparation for wakefulness.

Neurobiology: REM-Sleep-Promoting 'Goldilocks' Neurons.

REM sleep is a paradoxical state accompanied by suspended thermoregulation that is preferentially expressed under optimal ambient temperatures. Komagata and colleagues now demonstrate that activity in hypothalamic melanin concentrating hormone neurons is essential for the temperature-dependent modulation of REM sleep.

ONEIROS, a new miniature standalone device for recording sleep electrophysiology, physiology, temperatures and behavior in the lab and field.

BACKGROUND: Sleep is an inactive state of reduced environmental awareness shared by all animals. When compared to wakefulness, sleep behavior is associated with changes in physiology and brain activity. The nature of these changes varies considerably across species, and therefore is a rich resource for gaining insight into the evolution and functions of sleep. A major obstacle to capitalizing on this resource is the lack of a small device capable of recording multiple biological parameters for extended periods of time both in the laboratory and the field. NEW METHOD: ONEIROS is a new tool designed for conducting sleep research on small, freely moving animals. The miniature, standalone system is capable of recording up to 26 electrophysiological signals (electroencephalogram, electromyogram, electrooculogram, electrocardiogram), metabolic (3 temperature channels) and behavior via an accelerometer for several days. In addition, the device is equipped with a vibrating motor which can be used to assess arousal thresholds and to disrupt sleep. The system is available in telemetric or data-logger configuration useable in the field. RESULTS: To demonstrate the efficacy of this tool, we simultaneously recorded for the first time, electroencephalogram, hippocampal local field potential, electromyogram, electrooculogram, brain, body and ambient temperature, and 3D accelerometry. We also deprived rats of paradoxical sleep by triggering the vibrating motor after online recognition of the state. Finally, by successfully recording a pigeon in an 8 m3 aviary in a social context with the device in the logger configuration, we demonstrate the feasibility of using the device in the field.

Neuroethology: Fur Seals Don't Lose Sleep over REM Lost at Sea.

Northern fur seals forego large amounts of rapid eye movement (REM) sleep when sleeping in water, but remain healthy and do not recover this loss once back on land, challenging current theories for the function of REM sleep.