The relationship of sleep with temperature and metabolic rate in a hibernating primate

Abstract

Study objectives: It has long been suspected that sleep is important for regulating body temperature and metabolic-rate. Hibernation, a state of acute hypothermia and reduced metabolic-rate, offers a promising system for investigating those relationships. Prior studies in hibernating ground squirrels report that, although sleep occurs during hibernation, it manifests only as non-REM sleep, and only at relatively high temperatures. In our study, we report data on sleep during hibernation in a lemuriform primate, Cheirogaleus medius. As the only primate known to experience prolonged periods of hibernation and as an inhabitant of more temperate climates than ground squirrels, this animal serves as an alternative model for exploring sleep temperature/metabolism relationships that may be uniquely relevant to understanding human physiology.

Measurements and results: We find that during hibernation, non-REM sleep is absent in Cheirogaleus. Rather, periods of REM sleep occur during periods of relatively high ambient temperature, a pattern opposite of that observed in ground squirrels. Like ground squirrels, however, EEG is marked by ultra-low voltage activity at relatively low metabolic-rates.

Conclusions: These findings confirm a sleep-temperature/metabolism link, though they also suggest that the relationship of sleep stage with temperature/metabolism is flexible and may differ across species or mammalian orders. The absence of non-REM sleep suggests that during hibernation in Cheirogaleus, like in the ground squirrel, the otherwise universal non-REM sleep homeostatic response is greatly curtailed or absent. Lastly, ultra-low voltage EEG appears to be a cross-species marker for extremely low metabolic-rate, and, as such, may be an attractive target for research on hibernation induction.

Figure 1. Four 30 second segments of EEG Data.

A. Two segments of data recorded in non-torpid sleep in Duke Lemur Center. The top segment displays EEG data during a period of REM sleep. The display scale is 250 µV from the top to the bottom. The bottom segment displays EEG data during a period of Non-REM sleep. The display scale is 150 µV from the top to the bottom. b. Two 30 second segments of EEG data recorded during torpor in the wild verified by decreased metabolic rate. The top segment includes REMs. The display scale is 250 µV from the top to the bottom. The bottom segment is typical monotonous very low-voltage activity seen through much of these recordings and the display scale is 75 µV from the top to the bottom.

Figure 2. Data from recordings carried out for a torpid C.

medius studied in the Duke Lemur Center. Simultaneous EEG, Temperature and Metabolic Rate recordings were obtained. a. Ambient Temperature, Skin Temperature, and Metabolic Rate vs Time of Day in Hours. Arousal from torpor is evident at approximately 13.5 hours. b. State (derived from visual scoring of the data in 30 second epochs) and Metabolic Rate vs. Time of Day in Hours.

Figure 3. Data collected in a C. medius Studied in a Nest Box in the Wild in Madagascar With Continuous Torpor Verified by Metabolic Rate.

The gray shading indicates periods of darkness. a. Ambient Temperature and Metabolic Rate vs Time of Day in Hours. b. State scored for each 30 seconds during the period of monitoring (it was either a monotonous ultra-low voltage state, a REM-like state, or brief periods of movement which obscured making a state determination designated as “movement” epochs) vs Metabolic Rate vs Time of Day in Hours. c. Rapid eye movements (REMs) per 30 second epoch and Metabolic Rate vs. time in hours. c. Beta power (16.5–30 Hz) per 30 second epoch and Metabolic Rate vs. time in hours d. Delta power (0.5–3.5 Hz) per 30 second epoch and Metabolic Rate vs. time in hours. For reference, the mean basal metabolic rate of resting lemurs that are not in torpor in the field is 133 ml O2/h. This is based on the mean of data collected from 14 post-absorptive resting lemurs while awake. The lowest basal metabolic rates we measured in non-hibernating lemurs were ≥115 ml O2/hr²⁶.

Figure 4. REMs per 30 second epoch and Ambient Temperature vs Time of Day in Hours in 6 C. medius studied in the wild in Madagascar.

The top panel of the figure represents data from the animal documented to be in torpor with metabolic measurement. Note: the periods where EEG data were available for each animal coincides with the time-points where Ambient Temperature data is included in the graphs. Graphs a-f depict these data for Lemurs 1–6 respectively as designated in Table 1. Note: Because we have plotted a data point for every 30 second period over the roughly 4 days of data depicted, data from adjacent 30 second epochs which have the same or nearly the same value will appear to be on top of each other.