Sleep in the rock hyrax, Procavia capensis

Abstract

We investigated sleep in therock hyrax, Procavia capensis, a social mammal that typically lives in colonies on rocky outcrops throughout most parts of Southern Africa. The sleep of 5 wild-captured, adult rock hyraxes was recorded continuously for 72 h using telemetric relay of signals and allowing unimpeded movement. In addition to waking, slow wave sleep (SWS) and an unambiguous rapid eye movement (REM) state, a sleep state termed somnus innominatus (SI), characterized by low-voltage, high-frequency electroencephalogram, an electromyogram that stayed at the same amplitude as the preceding SWS episode and a mostly regular heart rate, were identified. If SI can be considered a form of low-voltage non-REM, the implication would be that the rock hyrax exhibits the lowest amount of REM recorded for any terrestrial mammal studied to date. Conversely, if SI is a form of REM sleep, it would lead to the classification of a novel subdivision of this state; however, further investigation would be required. The hyraxes spent on average 15.89 h (66.2%) of the time awake, 6.02 h (25.1%) in SWS, 43 min (3%) in SI and 6 min (0.4%) in REM. The unambiguous REM sleep amounts were on average less than 6 min/day. The most common state transition pathway in these animals was found to be wake → SWS → wake. No significant differences were noted with regard to total sleep time, number of episodes and episode duration for all states between the light and dark periods.Thus, prior classification of the rock hyrax as strongly diurnal does not appear to hold under controlled laboratory conditions.

Fig. 1

Examples of EEG and EMG polygraphs demonstrating 2-min episodes of active wake, quiet wake, SWS, SI and REM states in the rock hyrax. Waking episodes were characterized by a low-voltage, high-frequency EEG. The EMG for active waking exhibited higher voltages compared to the quiet waking state, and high-voltage spikes that likely correspond with movements were evident during this state. SWS was characterized by a high-voltage, low-frequency EEG and an EMG that was lower in amplitude than during the waking states. The EEG for both SI and REM resembled that of waking; however, during SI the EMG remained at the same amplitude as the preceding SWS episode, while during REM the EMG was reduced in amplitude.

Fig. 2

EEG and EMG polygraphs demonstrating the transitions that occur between the different sleep states in the rock hyrax. The first set of polygraphs is an example of SWS transitioning to SI, which then leads to REM followed by waking. Note that the EMG during SI remains at the same amplitude as during the preceding SWS episode, and that when SI transitions to REM the EMG reduces in amplitude. The second set of polygraphs demonstrates transition from SWS to REM followed by waking.

Fig. 3

Plots representing the IHR during each of the sleep states and waking. The IHR rate during waking was irregular and more widely scattered compared to SWS, which exhibited a more regular pattern. The IHR of SI resembled that of waking while REM was even more irregular and widely distributed than waking. The left-hand column shows the IHR for an individual animal over a 2-min period in each of the states, while the graphs in the right-hand column represent compiled data from 3 individuals (2 min from each individual) for IHR plotted against the subsequent IHR.

Fig. 4

The spectral power and associated frequency band characteristics of waking, SWS, SI and REM in the rock hyrax during both the light (a) and the dark (b) periods.

Fig. 5

Hypnograms showing the physiological and correlated behavioral state transitions occurring over a 24-hour period for one hyrax (H06) starting at 9 a.m. The shaded area represents the dark period. The polycyclic nature of sleep is visible in the physiological hypnogram, with SWS equally represented during both the light and dark periods. The animal also appeared to be more active and was eating more during the dark periods compared to the light periods for the 24 h represented here.

Fig. 6

Histograms depicting the species means for the total amount of time spent in each of the physiological defined states as well as the average number of episodes and episode duration for 24 h (left row of graphs), the light period (middle row of graphs) and the dark period (right row of graphs) for both the scoring methods. Statistically significant differences between the two scoring methods are indicated by a star and the small bars represent standard error bars (t test for dependent variables, d.f. = 4, p < 0.05, please refer to the ‘Results’ section for respective t and p values).

Fig. 7

State transition probabilities in the rock hyrax during 24 h based on the data of all 5 animals studied. In most cases SWS was followed by waking, thus making this the most common sleep pathway observed in the rock hyrax. The next most common pathway would be when SWS is followed by SI which then predominantly transitions to waking; however, in some cases it also transitions to REM, which in turn is most commonly followed by waking.

Fig. 8

SWA (based on 2-hour intervals) for the 72-hour recording period during all states (a) and during SWS (b). SWA remained fairly constant during all 3 recording days and a statistically significant difference between SWA during SWS and SWA during all states was noted (SWA during SWS > SWA-all, t test for dependent variables, d.f. = 4, p < 0.05; please refer to the ‘Results’ section for respective t and p values). c Histogram illustrating the average spectral power for the 72-hour recording period for all states and during SWS during the light and dark period. For both SWA during all states and SWS there were no differences between the light and dark periods. However, when SWA during all states and SWA during SWS were compared for the light and dark periods, respectively, statistically significant differences were observed, with SWA during SWS being greater than SWA during all states during both the light and dark periods (t test for dependent variables, d.f. = 4, p < 0.05; please refer to the ‘Results’ sections for respective t and p values). d Line graph showing the average SWA during wake and sleep stages. SWA was the greatest during SWS and this feature was consistent throughout the recording period. Data obtained from all 5 animals were analyzed; however, for clarity graphs a and b represent 3 animals. Statistically significant results are indicated by a star.

Fig. 8

SWA (based on 2-hour intervals) for the 72-hour recording period during all states (a) and during SWS (b). SWA remained fairly constant during all 3 recording days and a statistically significant difference between SWA during SWS and SWA during all states was noted (SWA during SWS > SWA-all, t test for dependent variables, d.f. = 4, p < 0.05; please refer to the ‘Results’ section for respective t and p values). c Histogram illustrating the average spectral power for the 72-hour recording period for all states and during SWS during the light and dark period. For both SWA during all states and SWS there were no differences between the light and dark periods. However, when SWA during all states and SWA during SWS were compared for the light and dark periods, respectively, statistically significant differences were observed, with SWA during SWS being greater than SWA during all states during both the light and dark periods (t test for dependent variables, d.f. = 4, p < 0.05; please refer to the ‘Results’ sections for respective t and p values). d Line graph showing the average SWA during wake and sleep stages. SWA was the greatest during SWS and this feature was consistent throughout the recording period. Data obtained from all 5 animals were analyzed; however, for clarity graphs a and b represent 3 animals. Statistically significant results are indicated by a star.

Fig. 9

Histogram illustrating the species mean for the percentage of time occupied by each behavioral state for the 72-hour recording period during the light and dark period, respectively. There is no statistically significant difference in the distribution of immobility, quiet waking and eating/drinking behaviors between the light and dark periods; however, a statistically significant difference was noted with regard to active waking. More active waking was noted during the dark compared to the light period (t test for dependent variables, d.f. = 4, p < 0.05; please refer to the ‘Results’ section for respective t and p values). Although not statistically significant, there was also a tendency to more eating/drinking behavior during the dark period. Statistically significant results are indicated by a star.