Internal desynchronization of the circadian activity and feeding rhythm in an owl monkey (Aotus lemurinus griseimembra): a case study.

In the free-running circadian locomotor activity rhythm of a 7-year-old male owl monkey (Aotus lemurinus griseimembra) kept under constant light and climatic conditions (LL 0.2 lux, 25 degrees C +/- 1 degrees C, 60 +/- 5% relative humidity [RH]), a second rhythm component developed that showed strong relative coordination with the free-running activity rhythm of 24.4h and a 24h rhythm. The simultaneously recorded feeding activity rhythm strongly resembled this rhythm component. Therefore, it seems justified to infer that there was an internal desynchronization between the two behavioral rhythms or their circadian pacemakers, that is, between the light-entrainable oscillator located in the suprachiasmatic nuclei (SCN) and a food-entrainable oscillator located outside the SCN. This internal desynchronization may have been induced and/or maintained by a zeitgeber effect of the (irregular) 24h feeding schedule on the food-entrainable oscillator. The weak relative coordination shown by the activity rhythm indicates a much weaker coupling of the light-entrainable oscillator to the food-entrainable oscillator than vice versa.

Effect of ambient temperature on the circadian activity rhythm in common marmosets, Callithrix j. jacchus (primates).

Whereas the (zeitgeber) effect of ambient temperature Ta and temperature cycles TaC's on circadian rhythmicity has been well documented for heterothermic mammals, inconsistent results have been obtained for strictly homeothermic species. Hence, it might be inferred that the susceptibility of the mammalian circadian timing system (CTS) to Ta and TaC's depends on the range of the animals' core and/or brain temperature rhythm. This hypothesis was tested in the common marmoset (Callithrix j. jacchus, n = 12), a small diurnal primate with an amplitude in body temperature rhythm that is larger than for other homeothermic primates studied so far. Within the range 20-30 degrees C, no systematic effects of constant Ta on most parameters of the marmosets' light-dark (LD)-entrained and free-running circadian activity rhythm (CAR) were found. Significant differences could be established in the average amount of activity per circadian cycle. It was highest at Ta 25 degrees C (LD) and 20 degrees C (light-light, LL) and most probably reflected a temperature-induced masking effect. A 24 h trapezoidal TaC of 20:30 degrees C entrained the free-running CAR in two of six marmosets and produced relative coordination in all others. Accordingly, in all animals tested, it had an effect on the CTS. In marmosets free running in LL at a Ta of 20 degrees C or 30 degrees C, 3 h warm and cold pulses of 30 degrees C and 20 degrees C, respectively, produced neither systematic phase responses nor period responses of the CAR. So, there is no evidence of a phase-response mechanism underlying circadian entrainment. The results show that large-amplitude TaC's function as a weak zeitgeber for the marmosets' CTS. Since this zeitgeber effect is significantly larger than that found in owl monkeys, the results are consistent with the starting hypothesis that the zeitgeber effect of a given TaC on the mammalian CTS may be related to the amplitude of the species' core and/or brain temperature cycle.

Infradian alteration of circadian rhythms in owl monkeys (Aotus lemurinus griseimembra): an effect of estrous?

Long-term recordings of locomotor activity, feeding activity and core temperature carried out in 7 male and 7 female adult owl monkeys (Aotus lemurinus griseimembra) revealed sex-specific infradian alterations in the level of these circadian functions when the monkeys were housed under lighting conditions which neither inhibited nor enhanced (i.e., "masked,") their circadian activity rhythms. Such nonmasking lighting conditions were: constant dim light (LL) at 0.1-0.5 lx, photoperiods consisting of 0.5 h light (L) at 80 lx and 23.5 h darkness (D) at 0.5 lx, and skeleton photoperiods consisting of two 80-lux light pulses of 0.5 h applied at intervals of 12:12 h and 9:15 h, respectively. In 5 of the female and none of the male owl monkeys, the amount of locomotor activity per day or per circadian cycle, increased at an average interval of 14.0 +/- 2.3 days to 198.4 +/- 48.2%, while the feeding activity was concomitantly reduced to 53.7 +/- 11.2%, and the core temperature level dropped by 0.3 +/- 0.1 degrees C, as compared to the respective preceding level of these parameters. The period of this infradian periodicity superimposed on the circadian rhythms corresponds approximately to the ovarian cycle length of Aotus (6,7). As food deprivation for one day resulted in a drop in core temperature is probably the result of reduced food intake. The infradian rise in activity and the decrease in food intake might be an effect of the ovarian cyclic variation in estrogen level.

Characteristics of the light-induced phase response of circadian activity rhythms in common marmosets, Callithrix j. jacchus [primates-Cebidae].

Phase-response experiments using 1-h light pulses (LPs) of 1,100 lux applied under constant dim light of 0.3 lux were conducted with common marmosets, Callithrix j. jacchus, in order to obtain a complete phase-response curve established according to the common experimental procedure in a diurnal primate. Maximal phase delays of the free-running circadian activity rhythm (-90 min) were induced by LPs delivered at circadian time (CT) 12; e.g., during the beginning of the marmosets' rest time, maximal advances (+25 min) were elicited by pulses administered during the late subjective night at CT 21. In contrast to rodents, neither regular transient cycles nor regular period responses resulted from LP applications at different phases. To check whether the underlying period length affects the phase response in primates as well, the marmosets' circadian timing system was entrained to 25 h by a light:dark (LD) cycle of 12.5:12.5 h. The 1-h LPs were delivered during the first circadian cycle produced under constant dim light after the entraining LD periods. Here, LPs applied at CT 21 led to phase advances exceeding those measured during the steady-state free run. At CT 12, minor or no phase delays could be elicited. These findings show that the phase-shifting effect of LPs on the circadian system of marmosets is similar to that observed in other diurnal mammals. Some of the results indicate that in this diurnal primate, LP-induced phase shifts may be mediated in part by a light-induced increase in locomotor activity (arousal).

Resynchronization of the circadian corticosterone rhythm after a light/dark shift in juvenile and adult mice.

Most of the extensive literature concerning the resynchronization of circadian rhythms after a Zeitgeber shift is devoted to the dependence of resynchronization on the mode of the shift and the strength of the Zeitgeber, as well as on the circadian function investigated. Ontogenetic influences have rarely been investigated. Therefore, we studied the resynchronization of several circadian rhythms in juvenile and adult female laboratory mice. We present here the results concerning the corticosterone rhythm. The daily rhythms were determined as transverse profiles (2-h intervals) before as well as 3, 7, and 14 days after an 8-h phase delay of the light/dark cycle produced by a single prolongation of dark time. The corticosterone concentration in serum was determined radioimmunologically. In the control animals the daily patterns were bimodal, with main maxima at the end of the light time and secondary ones just after lights on. Ontogenetic differences were small. In adult mice the amplitude was slightly increased due to an increase in the maximum values, and the time of highest hormone concentrations was slightly phase advanced. In juvenile mice, a distinct daily pattern with a phase position in relation to the light/dark cycle corresponding to that of control animals was present on the 3rd day after the Zeitgeber shift. The daily mean as well as the minimum and maximum values increased initially and reached the values of control animals during the second week. In adult animals, a pronounced daily rhythm with the normal phase position was present only at the 7th postshift day. The amplitude, daily mean, and maximum values were decreased, and the minimum values were increased. The initial values were not reached even after 2 weeks. The results show that resynchronization was faster in juvenile mice compared with adult mice. As a possible cause for the observed age-related differences, a not yet stabilized phase-coupling between various circadian rhythms is supposed.

Urinary estradiol-17 beta excretion in common marmosets, Callithrix jacchus: diurnal pattern and relationship between creatinine-related values and excreted amount.

1. The diurnal pattern of urinary estradiol and creatinine excretion was investigated in order to evaluate the relationship between total estradiol excretion per day and the estradiol concentration or the estradiol-to-creatinine ratio from single urine samples in female common marmosets (Callithrix j. jacchus). 2. During a 36-day period, urine was collected from five adult female marmosets in 3-hr intervals during the light time of an LD 12:12 (400:0.1 lx) which corresponded to the animals' activity time. 3. Estradiol concentration was determined by radioimmunoassay after glucuronidase treatment and creatinine concentration was measured photometrically. 4. Concentration and amount of excreted estradiol, and the creatinine concentration showed a distinct diurnal pattern with significantly higher levels at the beginning of the activity time compared to later sampling times. 5. No diurnal pattern was present in the estradiol-to-creatinine ratio, but the difference between lower follicular and higher luteal phase levels of estradiol excretion remained significant in the 36-day period. 6. Correlation analyses revealed significantly positive correlations between the total estrogen mass excreted per day and the estradiol-to-creatinine ratio in "morning urine" samples. 7. Thus the estradiol-to-creatinine ratio of single urine samples collected at the beginning of the activity time provides a reliable estimate of total estrogenic output in this species. 8. Studies of the circadian pattern of urinary hormone excretion, however, require total urine sampling.

Alteration of circadian period length does not influence the ovarian cycle length in common marmosets, Callithrix j. jacchus (primates).

To investigate the coupling between the circadian system and the regulation of the ovarian cycle in nonhuman primates, the effect of Zeitgeber-induced alterations of the circadian period (23 vs 26 h) on the ovarian cycle length was studied in the long-cycling polyestrous common marmoset, Callithrix j. jacchus. For that purpose, six female marmosets were isolated for approximately 4 months each under artificial lighting regimens of 23 h [light-dark (LD) 11.5:11.5] and of 26 h (LD 13:13; 300:0.03 lx). Samples of "morning urine" were collected in each circadian period and analyzed by radioimmunoassay for their estrone (E1) and estradiol-17 beta (E2) concentrations. Clear ovarian cyclic variations of the creatinine related urinary E1 and E2 concentrations were ascertained in each individual, with the E2 concentrations being 5-10 times higher than the E1 concentrations. In a total of 48 recorded ovarian cycles, the cycle length varied between 16 and 39 days and was 28.3 +/- 4.1 days on average. As measured in circadian periods, the marmosets' ovarian cycle was significantly longer (p < 0.05) under entrainment to LD 11.5:11.5 than under entrainment to LD 13:13. When measured in objective days, however, no difference in cycle length was demonstrated. Hence, in Callithrix, the mechanisms regulating the ovarian cycle length do not seem to be closely coupled to the circadian system, but rather corroborate the more classic hypothesis presuming that in polyestrous mammals different (at most weakly coupled) timing mechanisms or oscillator systems are responsible for the regulation of the circadian and the ovarian cycles.

Significance of nonparametric light effects in entrainment of circadian rhythms in owl monkeys (Aotus lemurinus griseimembra) by light-dark cycles.

In a total of 12 adult Colombian owl monkeys, Aotus lemurinus griseimembra, the significance of nonparametric light effects for the entrainment of the circadian system by light-dark (LD) cycles was studied by carrying out (a) phase-response experiments testing the phase-shifting effect of 30-min light pulses (LPs) of 250 lx applied at various phases of the free-running circadian activity rhythm (LL 0.2 lx) and (b) synchronization experiments testing the entraining effect of 24-h single LP photoperiods consisting of 30-min L of 80 lx and 23.5-h D of 0.5 lx (sP 0.5) and skeleton photoperiods consisting of two 30-min LPs of 80 lx, given against a background illuminance of 0.5 lx either symmetrically at 12-h intervals (PP 12:12) or asymmetrically at 9- and 15-h intervals (PP 9:15). The phase-response characteristics in Aotus, as evidenced by the phase-response curve, generally correspond to those of nocturnal rodents, providing that this neotropical simian primate chronobiologically is a genuine nocturnal species. When free-running with a spontaneous period close to 24 h (24.3 +/- 0.1 h), the PP 12:12 produced entrainment in only two of five owl monkeys, whereas the sP 0.5 entrained four of them. The PP 9:15, however, brought about stable entrainment of the circadian rhythms of locomotor activity, feeding activity, and core temperature in all animals tested (n = 8). Changes in phase position of the activity time with the endogenous rhythm entrained by a PP 12:12, by an sP 0.5, or by a PP 9:15 give evidence that both LPs of a skeleton photoperiod contribute to the phase setting of the circadian system. When free-running with a considerably lengthened spontaneous period (tau greater than or equal to 25.5 h), even the sP 0.5 and the PP 9:15 failed to entrain the owl monkeys' circadian rhythms, whereas a 24-h photoperiod with a very long LP of 3 h caused entrainment. The results indicate that in Aotus lemurinus griseimembra, in addition to the nonparametric light effects, parametric light effects play a significant role in the entrainment of circadian rhythms by LD cycles.

Splitting of the circadian activity rhythm in common marmosets (Callithrix j. jacchus; primates).

Long-term recordings of the free-running circadian activity rhythm in common marmosets, Callithrix j. jacchus, living under constant environmental conditions (LL 200-470 lx) provided evidence of rhythm splitting in nonhuman primates. In two out of ten test animals two different types of splitting occurred; spontaneous persistent splitting and temporary splitting. Neither a reduction of the illumination intensity nor the application of dark pulses had any effect on the two activity components of the persistently split rhythm.

Direct modulation of activity and body temperature of owl monkeys (Aotus lemurinus griseimembra) by low light intensities.

The activity pattern of Aotus lemurinus griseimembra can be predictably altered by varying the illuminance during the dark phase of a 12:12-hour light:dark rhythm. Intensities well below full-moon brightness (0.1-0.5 lx) severely inhibit activity. This modulation is not the result of a light-induced phase shift of the circadian rhythm, but it is primarily caused by masking due to direct effects of light on the motor system. Both proportional and differential effects of light are involved. Miniature transmitters were implanted intraperitoneally in two Aotus females so that the core temperature could be measured in parallel with locomotor activity. The responses to brief reductions of the dark-phase illuminance, from 10(-1) to 10(-3) lx, 10(-5) lx or physiological darkness, indicate that the direct effects of light that modulate the activity of the owl monkeys also affect their temperature time-course. The influence on the temperature rhythm, unlike that on the activity rhythm, varies greatly over the circadian period. The finding that the core temperature does not always change in parallel with locomotor activity and, to some extent, reacts differently to the light:dark alternation indicates that temperature does not simply follow activity passively, but rather is partially subject to a 'direct' masking influence of the light.

Diurnal variation of several blood parameters in the owl monkey, Aotus trivirgatus griseimembra.

Diurnal variations in normal hemogram, total serum protein and serum iron are documented in 6 adult owl monkeys, Aotus trivirgatus griseimembra, maintained in an artificial LD 12:12 (35:0.08 lx) with light phase from 03.00 to 15.00 h Central European time. Statistically significant high amplitude rhythms occurred in total leukocyte and in eosinophil numbers with acrophases at 06.35 and 09.53 h, respectively. Erythrocyte numbers and hemoglobin concentration showed statistically significant low amplitude rhythms with almost identical acrophases. Total serum protein exhibited a 10% daily fluctuation. Serum iron concentration showed high amplitude daily variations with a 60% mean range of oscillation.

Dark switch in the entrainment of circadian activity rhythms in night monkeys. Aotus trivirgatus humboldt.

1. The locomotor activity of the night monkey (Aotus trivirgatus) has been shown to be related to light intensity by an optimum function; here entrainment by LD cycles is examined to see whether the mechanism of synchronization of circadian periodicity in Aotus is based on this function. 2. Eleven night monkeys of various ages, previously in either a free-running phase or in LD 12:12 (10(2):10(-1) lux), were recorded in LD 12:12 with the optimal intensity (10(-1) lux) in the light part of the cycle and a suboptimal intensity (10(-3) lux) in the dark part. 3. In all cases the monkeys synchronized in such a way that their activity phase fell in the dark part of the LD cycle. 4. The implication is that Aotus is a true dark-active species, that the illumination-dependent activity maximum at 10(-1) lux does not affect the synchronization mechanism, and that the differential (direction of change) rather than proportional (absolute level) actions of light provide the decisive cue for synchronization of the circadian activity rhythm.

Effect of the Zeitgeber pattern on the resynchronization behaviour of dark-active mammals.

The activity of 12 Egyptian fruit bats, Rousettus aegyptiacus, was synchronized by 24-h illumination cycles varying in light/dark (L/D) ratios, and the effect of these ratios on the resynchronization following phase shifts of the Zeitgeber signal (+8 h and -8 h) was observed. The resynchronization time in L/D:16/8 was the same as that in L/D:12/12, but that in L/D:8/16 was significantly increased. After an advance-shift, some of the bats (2 of 6 in L/D:16/8 and 6 of 12 in L/D:8/16) resynchronized 'antidromically', by lengthening the activity period. The tendency toward antidromic resynchronization appears to increase with the age of the animal. Two ways of interpreting these results are: (1) as a consequence of a reduction in the strength of the Zeitgeber signal due to the altered L/D ratio; and (2) in terms of a modification of the phase response. Among the implications for human circadian periodicity is the possibility that resynchronization following long west-east flights at high latitudes might be affected by the time of year.

Zeitgeber-schedule dependent resynchronization of circadian rhythms in nocturnal mammals (Primates and Chiroptera).

Changing the L:D time ratio of an entraining light-dark regime leads to characteristic alterations of the resynchronization behaviour of the circadian activity rhythms in night monkeys (Aotus trivirgatus) and African fruit bats (Rousettus aegyptiacus) after 8 h advance and delay shifts of the LD-Zeitgeber. Reduced speed of re-entrainment and occurrence of antidromic resynchronization point to a lower Zeitgeber strength of 24-h LD-cycles with a prolonged D-phase.

Zeitgeber induced modulation of activity patterns in nocturnal mammals (Chiroptera).

Changing the L:D intensity ratio of a synchronizing dark regime leads to characteristic modulations of the activity pattern of Chiroptera species. These modulations fit the predictions of WEVER'S oscillator model.

[Light-induced activity optimum in night monkeys (Aotus trivirgatus)]. / Beleuchtungsabhängiges Aktivitätsoptimum bei Nachtaffen (Aotus trivirgatus)

It is shown that the amount of locomotor activity of night monkeys (Aotus trivirgatus) depends very markedly on the intensity of illumination in the darkness phase of an artificial light/darkness cycle 12:12 h. Maximum activity occurs with the degree of brightness of full moon at approximately 0.1 lx. Lesser as well as higher light intensities have an inhibiting effect on the activities of Aotus. These findings are in accordance with the results of activity measurements on the Aotus under natural illumination conditions in the vicinity of the equator.

Lunarperiodic variation of the phase-angle difference in nocturnal animals under natural Zeitgeber-conditions near the equator.

Several months' studies under natural illumination conditions in the vicinity of the equator show that night monkeys (Aotus trivirgatus), and leaf-nosed bats (Artibeus lituratus) exhibit species-specific lunarperiodic changes of the phase position of their activity rhythm to the Zeitgeber rhythm (Figures 1-3). These changes are closely to nightly illumination conditions. In Aotus the phase-angle differences (p.a.ds) of the onset and end of the activity phase, and in Artibeus the p.a.ds of the midpoint and end of the activity phase are significantly dependent upon the phases of the moon. In the African fruit bat Rousettus aegyptiacus, and in the leaf-nosed bat Phyllostomus hastatus no statistically significant lunarperiodic changes of the p.a.ds could be detected. These results cannot be explained by means of current models concerning the mechanism of synchronisation of biological oscillation. They appear to be, instead, expressions of a periodic masking of the real phase-position due to direct effects of light intensity on the level of activity which which itself is determined by the circadian rhythm. Aschoff's rule, which states that the earlier a species or an individual awakes the later it terminates its daily phase of activity, is partly confirmed for the nocturnal mammals examined in the present study.