Local Aspects of Avian Non-REM and REM Sleep

Abstract

Birds exhibit two types of sleep that are in many respects similar to mammalian rapid eye movement (REM) and non-REM (NREM) sleep. As in mammals, several aspects of avian sleep can occur in a local manner within the brain. Electrophysiological evidence of NREM sleep occurring more deeply in one hemisphere, or only in one hemisphere - the latter being a phenomenon most pronounced in dolphins - was actually first described in birds. Such asymmetric or unihemispheric NREM sleep occurs with one eye open, enabling birds to visually monitor their environment for predators. Frigatebirds primarily engage in this form of sleep in flight, perhaps to avoid collisions with other birds. In addition to interhemispheric differences in NREM sleep intensity, the intensity of NREM sleep is homeostatically regulated in a local, use-depended manner within each hemisphere. Furthermore, the intensity and temporo-spatial distribution of NREM sleep-related slow waves varies across layers of the avian hyperpallium - a primary visual area - with the slow waves occurring first in, and propagating through and outward from, thalamic input layers. Slow waves also have the greatest amplitude in these layers. Although most research has focused on NREM sleep, there are also local aspects to avian REM sleep. REM sleep-related reductions in skeletal muscle tone appear largely restricted to muscles involved in maintaining head posture. Other local aspects of sleep manifest as a mixture of features of NREM and REM sleep occurring simultaneously in different parts of the neuroaxis. Like monotreme mammals, ostriches often exhibit brainstem-mediated features of REM sleep (muscle atonia and REMs) while the hyperpallium shows EEG slow waves typical of NREM sleep. Finally, although mice show slow waves in thalamic input layers of primary sensory cortices during REM sleep, this is not the case in the hyperpallium of pigeons, suggesting that this phenomenon is not a universal feature of REM sleep. Collectively, the local aspects of sleep described in birds and mammals reveal that wakefulness, NREM sleep, and REM sleep are not always discrete states.

Keywords: atonia; bird; evolution; mammal; propagation; sleep; slow wave; unihemispheric.

FIGURE 1

Sleep in flight. (A) Female great frigatebird with a head mounted data logger for recording the EEG from both cerebral hemispheres and triaxial acceleration. A GPS logger mounted on the back recorded position and altitude. (B) Electroencephalogram (EEG) and accelerometry (sway, surge, and heave) recording from a frigatebird sleeping while circling in rising air currents. When the bird circled to the left (as indicated by centripetal acceleration detected in the sway axis) the bird showed asymmetric NREM sleep (ANREM) with the left hemisphere sleeping deeper (larger slow waves) than the right (ANREM-L), and when the bird circled to the right the right hemisphere slept deeper than the left (ANREM-R); during the other recording segments the bird was awake. (C) The relationship between interhemispheric asymmetries in slow wave activity (SWA, 0.75–4.5 Hz) and gamma activity (30–80 Hz) during NREM sleep for all birds combined (N = 14). During ANREM, the birds usually circled toward the side with greater SWA and lower gamma activity. By contrast, during bihemispheric NREM (BNREM) without asymmetries in SWA or gamma (BGamma), the birds showed no preference for circling in one particular direction. AGamma-L and AGamma-R indicate NREM with greater gamma in the left and right hemispheres, respectively. (D) Illustration showing a bird circling to the right while sleeping with the right hemisphere. Although the birds’ eye state is not known, based on studies from other birds, the EEG asymmetries suggest that the frigatebirds kept the eye connected to the more awake (lower SWA and higher gamma) hemisphere open and facing the direction of the turn. Panels (A–C) reproduced with permission from Rattenborg et al. (2016). Photo by Bryson Voirin. Illustration by Damond Kyllo.

FIGURE 2

Local sleep homeostasis in the avian brain. (A) Experimental design: a 12 h baseline night, 8 h period of bihemispheric sleep deprivation with unilateral visual stimulation (SD) and a 12 h recovery night. Photograph shows the experimental environment during the treatment. (B) Spectral power density (0.78–25.00 Hz) during NREM sleep for the first quarter of the baseline and recovery nights for the stimulated (dark blue) and visually deprived (light blue) hyperpallia and mesopallia. Data are presented as mean ± SE. Colored squares at the bottom of each recovery night plot reflect a significant pairwise comparison between the baseline and recovery night of the stimulated (dark blue) and visually deprived (light blue) hyperpallia; red squares denote a significant asymmetry between the left and right brain region during recovery sleep. Although the experimental treatment induced interhemispheric asymmetries across a wide range of frequencies, slow wave activity (yellow shading) in the hyperpallium showed the largest asymmetry. Insets: frontal view of a transverse section through the cerebrum of a pigeon highlighting the hyperpallium (H) and mesopallium (M). (C) Up slope of NREM sleep slow waves in the hyperpallium and mesopallium contralateral to the stimulated eye (dark blue) and deprived eye (light blue) during the first quarter of the baseline and recovery night. Data are presented as mean ± SE. Significant changes in slope between the baseline and recovery nights are marked with an asterisk (contralateral to the stimulated eye in dark blue; contralateral to the deprived eye, non-significant); significant asymmetries between the left and right hemisphere for a given brain region are denoted by a red asterisk. Note the asymmetry between the stimulated and visually deprived hyperpallia during recovery sleep, with the stimulated hyperpallium showing steeper slopes, and the symmetric mean increase in the mesopallium. Reproduced with permission from Lesku et al. (2011b).

FIGURE 3

Neurophysiology of the avian hyperpallium during natural sleep. (A) Position of a 32-channel silicon electrode probe in the hyperpallium of a pigeon. The orientation of the electrode grid (red) is always depicted with the medial side to the left and the surface of the brain on top. Input from the avian lateral geniculate nucleus (LGN) projects primarily to the interstitial part of hyperpallium apicale (IHA) and the hyperpallium intercalatum (HI). The underlying hyperpallium densocellulare (HD) receives relatively little input from the LGN. The hyperpallium overlies and is interconnected with the dorsal and ventral mesopallium (MD and MV) and nidopallium (N). (B) Five-second example of local field potentials showing the spatial distribution of slow waves in the hyperpallium during NREM sleep. (C) Mean slow wave activity (SWA; 1.5–4.5 Hz; N = 4 birds) over all episodes of NREM and REM sleep reveals greater SWA recorded from the electrodes positioned along the diagonal corresponding to the primary thalamic input layers, IHA and HI. SWA during REM sleep decreases from NREM sleep levels across all layers of the hyperpallium. White squares indicate missing data for some birds. (D) Propagating slow waves during NREM sleep. Red underlined episode from panel (B) is visualized in a sequence of image plots where pixels represent electrode sites and electrical potential is coded in color. (E) Trajectories and net propagation of the negative (red) and positive (blue) components of slow waves from a pigeon during NREM sleep. Left: trajectories for 50 randomly selected negative and positive waves (plus signs depict electrode sites). Right: net wave propagation calculated for every negative and positive wave in a 2 h recording; the black dot shows the mean propagation for negative and positive waves. Panels (D,E) demonstrate that both negative and positive potentials propagate most prominently along the thalamic input layers, and slightly into the overlying hyperpallium apicale (HA). E, entopallium; LSt, striatum lateral; MSt, striatum medial. Reproduced with permission from van der Meij et al. (2019a).

FIGURE 4

Sleep states in an ostrich. The recording begins and ends with periods of NREM sleep (blue bar) characterized by high amplitude, slow waves in the electroencephalogram (EEG), the absence of rapid eye movements (measured via electrooculogram, EOG), and head movements (accelerometer, ACC), and moderate neck muscle tone (electromyogram, EMG). NREM sleep is interrupted by a period of REM sleep (red bar) with either EEG activation (red shading) or slow waves (blue shading). Irrespective of the type of EEG activity, rapid eye movements, a forward falling and swaying head with moderate-to-low muscle tone occurred invariably during REM sleep in the ostrich. Heave ACC: movement along the dorso-ventral axis with an upward slope denoting downward movement, Sway ACC: lateral axis with up denoting movement to the right, Surge ACC: anterior-posterior axis with down denoting movement forward. Vertical bars to the right of each EEG, EOG, and EMG trace denote 100 μV, and 100 mg-forces to the right of each ACC trace. Trace duration: 60 s. Reproduced with permission from Lesku et al. (2011a).