Unihemispheric slow wave sleep and the state of the eyes in a white whale

Abstract

We recorded electroencephalogram (EEG) and simultaneously documented the state of both eyelids during sleep and wakefulness in a sub-adult male white whale over a 4-day-period. We showed that the white whale was the fifth species of Cetaceans, which exhibits unihemispheric slow wave sleep. We found that the eye contralateral to the sleeping hemisphere in this whale was usually closed (right eye, 52% of the total sleep time in the contralateral hemisphere; left eye, 40%) or in an intermediate state (31 and 46%, respectively) while the ipsilateral eye was typically open (89 and 80%). Episodes of bilateral eye closure in this whale occupied less than 2% of the observation time and were usually recorded during waking (49% of the bilateral eye closure time) or low amplitude sleep (48%) and rarely in high amplitude sleep (3%). In spite of the evident overall relationship between the sleeping hemisphere and eye state, EEG and eye position in this whale could be independent over short time periods (less than 1 min). Therefore, eye state alone may not accurately reflect sleep state in Cetaceans. Our data support the idea that unihemispheric sleep allows Cetaceans to monitor the environment.

Fig. 1.

Relationship between EEG and the state of eyes in a white whale. (A) The state of eyelids and EEG spectral power (1–3 Hz; 5-s epochs) from the two hemispheres (R, right; L, left) in a white whale recorded over a 3-h period. EEG power was normalized as a percentage of the maximal power in each hemisphere during this period. The state of each eye (R, right; L, left) was scored in real time (O, open; I, intermediate; or C, closed) and then categorized for 5-s epochs as described in the text. Note that this compressed figure does not show short lasting changes in eye state. (B) Expansion of the two 2.5-min recordings of the EEG and the state of both eyes. The examples show the EEG asynchrony and parallel changes in eye state recorded in this whale at the times marked as 1 and 2 in Fig. 1A. Note that the EEG does not change immediately with changes in eye position. The right eye did not close during episode 1 and the left eye did not close during episode 2. (C) The average EEG spectral power in the two hemispheres during episodes with unilateral eye opening (LO/RC, left open and right closed; LC/RO, left closed and right open). EEG power was normalized as a percent of the average 1–3 Hz power recorded in each hemisphere during SWS with the contralateral eye closure. Reported values are the means ±S.E. (LO/RC, n = 238 epochs; LC/RO, n = 441 epochs).

Fig. 2.

The state of the eyes during waking and sleep in a white whale. The EEG stage in each hemisphere was scored visually in 30 s. The state of the eyes was sampled in 5-s epochs and then extrapolated for consecutive 30-s epochs. Right and left hemispheric sleep represents unihemispheric SWS or asymmetrical bilateral SWS with a higher voltage EEG in the corresponding hemisphere. Reported values are the numbers of 30-s epochs with a given state of the eyes documented over 2 consecutive days.