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. 2011;6(8):e23203.
doi: 10.1371/journal.pone.0023203. Epub 2011 Aug 24.

Ostriches sleep like platypuses

Affiliations

Ostriches sleep like platypuses

John A Lesku et al. PLoS One. 2011.

Abstract

Mammals and birds engage in two distinct states of sleep, slow wave sleep (SWS) and rapid eye movement (REM) sleep. SWS is characterized by slow, high amplitude brain waves, while REM sleep is characterized by fast, low amplitude waves, known as activation, occurring with rapid eye movements and reduced muscle tone. However, monotremes (platypuses and echidnas), the most basal (or 'ancient') group of living mammals, show only a single sleep state that combines elements of SWS and REM sleep, suggesting that these states became temporally segregated in the common ancestor to marsupial and eutherian mammals. Whether sleep in basal birds resembles that of monotremes or other mammals and birds is unknown. Here, we provide the first description of brain activity during sleep in ostriches (Struthio camelus), a member of the most basal group of living birds. We found that the brain activity of sleeping ostriches is unique. Episodes of REM sleep were delineated by rapid eye movements, reduced muscle tone, and head movements, similar to those observed in other birds and mammals engaged in REM sleep; however, during REM sleep in ostriches, forebrain activity would flip between REM sleep-like activation and SWS-like slow waves, the latter reminiscent of sleep in the platypus. Moreover, the amount of REM sleep in ostriches is greater than in any other bird, just as in platypuses, which have more REM sleep than other mammals. These findings reveal a recurring sequence of steps in the evolution of sleep in which SWS and REM sleep arose from a single heterogeneous state that became temporally segregated into two distinct states. This common trajectory suggests that forebrain activation during REM sleep is an evolutionarily new feature, presumably involved in performing new sleep functions not found in more basal animals.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Four of the ostriches in the naturalistic reserve in South Africa (left).
Photograph by J.A.L. Movement data (green tracks, sampled once per second) from one ostrich for its first 8 d in the reserve (right); outline of the tracks shows the boundary of the reserve. Satellite map from Google Earth (www.google.com/earth).
Figure 2
Figure 2
(A) Representative slow wave sleep (SWS, blue bar) in the ostrich 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 muscle tone (electromyogram, EMG). Here, SWS is interrupted by a brief awakening (green bar) characterized by low amplitude, high frequency EEG activity, and a fast (200 ms) lateral sweep of the head, perhaps as a quick scan of the local environment, followed by a re-entrance into SWS. (B) Representative rapid eye movement (REM) sleep (red bar). Note that the EEG during REM sleep shows either 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 a positive slope denoting downward movement, Sway ACC: lateral axis with positive denoting movement to the right, Surge ACC: anterior-posterior axis with negative denoting movement forward. Vertical bars to the right of each EEG, EOG and EMG trace denote 100 µV, and 100 milli g-forces to the right of each ACC trace. Trace duration: 60 s.
Figure 3
Figure 3. Plot of data from an ostrich illustrating the distinctiveness of wakefulness (green), slow wave sleep (SWS, blue) and rapid eye movement (REM) sleep (red) based on differences in eye movements (measured via electrooculogram, EOG), head movements (accelerometer, ACC) and neck muscle tone (electromyogram, EMG).
SWS is associated with few eye movements, a relatively motionless head and moderate muscle tone; REM sleep is associated with rapid eye movements, head movements and moderate-to-low muscle tone. During wakefulness, muscle tone is generally highest with large head and eye movements. Variables calculated as the logarithm of power density (EOG: 0.4–9.8 Hz using the larger value between the left and right eye for each epoch, surge axis of the ACC: 0.0–9.8 Hz, EMG: 9.8–69.9 Hz). See Figure S2 for the three 2-dimensional plots that constitute this 3-dimentional figure.
Figure 4
Figure 4. The percentage of time (mean, s.e.m.) spent in wakefulness (green), slow wave sleep (SWS, blue) and rapid eye movement (REM) sleep (red) for each hour of the day (sunrise-to-sunset, yellow shading) and night (grey shading).
Brain temperature (°C) is given at the bottom of the panel.

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