Natural sleep and its seasonal variations in three pre-industrial societies

Abstract

How did humans sleep before the modern era? Because the tools to measure sleep under natural conditions were developed long after the invention of the electric devices suspected of delaying and reducing sleep, we investigated sleep in three preindustrial societies [1-3]. We find that all three show similar sleep organization, suggesting that they express core human sleep patterns, most likely characteristic of pre-modern era Homo sapiens. Sleep periods, the times from onset to offset, averaged 6.9-8.5 hr, with sleep durations of 5.7-7.1 hr, amounts near the low end of those industrial societies [4-7]. There was a difference of nearly 1 hr between summer and winter sleep. Daily variation in sleep duration was strongly linked to time of onset, rather than offset. None of these groups began sleep near sunset, onset occurring, on average, 3.3 hr after sunset. Awakening was usually before sunrise. The sleep period consistently occurred during the nighttime period of falling environmental temperature, was not interrupted by extended periods of waking, and terminated, with vasoconstriction, near the nadir of daily ambient temperature. The daily cycle of temperature change, largely eliminated from modern sleep environments, may be a potent natural regulator of sleep. Light exposure was maximal in the morning and greatly decreased at noon, indicating that all three groups seek shade at midday and that light activation of the suprachiasmatic nucleus is maximal in the morning. Napping occurred on <7% of days in winter and <22% of days in summer. Mimicking aspects of the natural environment might be effective in treating certain modern sleep disorders.

Fig 1. Location of recording sites

(A) (Left to right, Tsimané, San, Hadza). (B) Representative Actograms from Hadza, Tsimané and San subjects (the bottom 2 sets show the same San participant in summer (upper set) and winter (lower set)). Sleep onset time is highly variable and occurred several hours after sunset in all groups. Awakening time was relatively regular and occurred before sunrise, except in the San in summer. Naps may have occurred on up to 7% of days in winter and up to 22% of days in summer. Extended periods of nocturnal waking were rare. Yellow line is a log plot of light level; red, 1-min intervals with movement; black number of movements in each 1-min interval; light blue=Actogram scored rest; dark blue=Actogram scored sleep period. Sleep period, defined as interval between sleep onset and offset is greater than sleep time, defined as sleep period minus waking after sleep onset (WASO). Sleep efficiency (sleep time divided by “bed” time) was between 81 and 86%, similar to that in industrial populations. See Table S1).

Fig. 2. Seasonal effects on sleep

(A) Sleep duration decreased from winter to summer. (Note that the Hadza, San and Tsimane live in the southern hemisphere.) The Tsimané data were from 6 separate groups recorded over the 4 month period. Each group consisted of 7–12 individuals recorded for 7 days. A parallel study in the San recorded from 10 individuals, each for 21 days in May-June. An additional 5 San individuals were recorded for 11 days in August and 13 of the initial 15 were recorded for 28 days in Jan-February of the next year (two of the original 10 participants had migrated out of Den/ui). (B) Change in sleep onset and offset times across the seasons. The same San individuals were sampled for a 28 day period in summer and a 21 day period in winter (a total of 1260 sleep onsets and offsets). Note the much later sleep onset in the summer and the later wake onset in the summer relative to winter, despite shorter sleep times. Bin size is 0.4-h (24 min). Blue vertical line marks solar noon.

Fig. 3. Light and activity plots

(A, B) Average light and activity level in plots centered at midnight: Two participants (T3 and T5) are shown. Both have shorter sleep time in the summer despite later awakening. Participant data is their average sleep parameters over the summer or winter recording periods. Yellow line indicates subject light exposure as measured by the Actiwatch. Sunset, identifiable by the vertical interrupted black line, is not tightly linked to sleep onset. Interrupted blue bars indicates sleep periods. Red line at the bottom of each graph plots average of 1 min epochs with (+1) and without (0) activity. Note maintained and even increased activity (Black) with sunset, location of inactivity linked to sleep at the end of the dark period, awakening before dawn in winter, lack of period of activity within sleep and differences between duration of summer and winter nighttime inactivity period. The duration of these inactivity epochs are used in the algorithm that identifies sleep (Fig. 1). Sleep onset occurs from 2.5 to 4.4-h after sunset in all of the groups examined (mean = 3.3h). (C) Staying out of the midday sun. Plots centered at noon. Light levels recorded by Actiwatch drop steeply and consistently at midday, despite the increase of the ambient light level from morning (9 AM) to noon levels. Figure shows average of 60 days of data from the 10 Hadza recorded in Tanzania. It shows the reduction in light exposure during the afternoon, a lack of reduction in afternoon activity to sleep levels consistent with the lack of regular napping and the reduction in activity throughout the sleep period. No regular period of activity was seen in the night, consistent with the lack of a “second sleep” scored by the algorithm (also see fig S1). (D, E) Averaged data across all San recorded in summer and winter. Note the consistent pattern across groups and seasons. Time is local clock time.

Fig. 4. Relation of sleep to ambient temperature and skin temperature

Sleep offset, averaged across all subjects and all days, consistently occurs near the nadir of daily environmental temperature, in both summer and winter. In the San recorded in the summer, the temperature nadir occurred after sunrise, as did awakening. In the winter the nadir occurred near sunrise with awakening preceding sunrise. Note that the ambient temperature has a gradual fall at night and a rapid rise starting at sunrise, with sleep occurring during the period of slowly falling temperature. Vasoconstriction is seen upon awakening in both summer and winter. In the winter there are additional vasoconstrictions occurring during the day. These are likely related to food preparation or other similar activities exposing the hands to cold. Violet lines are environmental temperature, red line, abdominal temperature, blue line, finger temperature. Also see Fig. S2 for an example of individual subject data. All temperatures recorded by iButtons are synchronized to the actiwatch time ±2 min. Black bar=night, orange=waking, blue=sleep. Vertical lines at top of figures indicate light-dark transitions; those at bottom indicate sleep-wake transitions. Sleep measures are averages of 15 participants recorded in the summer and 13 of these participants recorded in winter (See Fig. 1, Table S1). Red arrows indicate onset of drop in finger temperature starting near the temperature nadir, indicative of peripheral vasoconstriction, serving to warm proximal regions with awakening.