Aging-related changes on social synchronization of circadian activity rhythm in a diurnal primate (Callithrix jacchus)

ABSTRACT

The input of environmental time cues and expression of circadian activity rhythms may change with aging. Among nonphotic zeitgebers, social cues from conspecific vocalizations may contribute to the stability and survival of individuals of social species, such as nonhuman primates. We evaluated aging-related changes on social synchronization of the circadian activity rhythm (CAR) in a social diurnal primate, the common marmoset. The activity of 18 male marmosets was recorded by actiwatches in two conditions. (1) Experimental – 4 young adult (5 ± 2 yrs of age) and 4 older (10 ± 2 yrs of age) animals maintained under LD 12/12 h and LL in a room with full insulation for light but only partial insulation for sound from vocalizations of conspecifics maintained outdoors in the colony; and (2) Control – 10 young adult animals maintained outdoors in the colony (5 animals as a control per age group). In LL, the CAR of young adults showed more stable synchronization with controls. Among the aged marmosets, two free-ran with τ > 24 h, whereas the other two showed relative coordination during the first 30 days in LL, but free-ran thereafter. These differences were reflected in the “social” phase angles (ψ_on and ψ_off ) between rhythms of experimental and control animal groups. Moreover, the activity patterns of aged animals showed lower social synchrony with controls compared to young adults, with the time lags of the time series between each experimental group and control group being negative in aged and positive in young adult animals (t-test, p < 0.05). The index of stability of the CAR showed no differences according to age, while the intradaily variability of the CAR was higher in the aged animals during LD-resynchronization, who took additional days to resynchronize. Thus, the social modulation on CAR may vary with age in marmosets. In the aged group, there was a lower effect of social synchronization, which may be associated with aging-related changes in the synchronization and generation of the CAR as well as in system outputs.     

The effects of chronic marijuana use on circadian entrainment

Animal literature suggests a connection between marijuana use and altered circadian rhythms. However, the effect has not yet been demonstrated in humans. The present study examined the effect of chronic marijuana use on human circadian function. Participants consisted of current users who reported smoking marijuana daily for at least a year and non-marijuana user controls. Participants took a neurocognitive assessment, wore actigraphs and maintained sleep diaries for three weeks. While no significant cognitive changes were found between groups, data revealed that chronic marijuana use may act as an additional zeitgeber and lead to increased entrainment in human users.     

Spontaneous cryptococcosis of a squirrel monkey (Saimiri sciureus) in French Guyana

An old female squirrel monkey (Saimiri sciureus) with a tumor-like growth of the lower jaw died in shock after 2 months of illness. Histological studies of different tissue samples demonstrated that the pathological agent was Cryptococcus. Multiple foci of fungus existed in the thoracic cavity with essentially pulmonary and glandular localizations.     

Phase control of circadian activity in the antelope ground squirrel

Abstract

Wheel‐running activity of forty antelope ground squirrels, Ammospermophilus leucurus, was monitored for several months in both an outdoor cage and in the laboratory. The squirrels demonstrated a highly diurnal pattern which persisted in “constant conditions.” After removal from the field the initial free‐running period was close to 24 hrs, but typically lengthened in a nearly linear fashion at least for the first few months. There was no evidence of any difference in this trend for squirrels, in D/D, L/L 100 lx, 250 lx or 1200 lx. Eventually, about 90 percent of the squirrels had periods longer than 24 hrs.

The synchronizing capacity of the natural photoperiod was used to “catch the free‐running rhythm” and thereby demonstrate a response curve. Synchronization occurred by a shortening of the period when the time of sunrise was between 125° and 0° (subjective night) and by a lengthening of the period when the time of sunrise was between 0° and 125° (subjective day).

To more thoroughly examine the underlying mechanisms of phase control, phase‐response curves based on sixty one light‐pulse experiments were constructed. Comparisons of curves based on 6‐hr and 15‐min pulses, showed that the integral action of light is important (i.e., the entire pulse is involved in phase shifting). It was found that light pulses not only affected the phase of the rhythm but also the phase. Large phase shifts were usually associated with decreases in free‐running period. Several hypotheses on the controlling mechanisms were advanced.     

Capacitation and the acrosome reaction in squirrel monkey (Saimiri sciureus) spermatozoa evaluated by the chlortetracycline fluorescence assay

Capacitation and the acrosome reaction in squirrel monkey seminal spermatozoa diluted in Tyrode's medium (TALP) and TC-199 were monitored by a chlortetracycline (CTC) fluorescence assay. Four CTC patterns, similar to those found in human sperm, were readily characterized by fluorescent staining on the heads of the spermatozoa. The appearance of the capacitated (CP) pattern was dependent on the concentration of the bovine serum albumin. Acrosomal loss was observed in a maximum of 15% of the sperm in the populations studied here. Calcium ionophore A23187 (5 μM to 20μM) induced acrosomal loss in 60–70% of capacitated spermatozoa. However in freshly ejaculated sperm incubated under capacitating conditions or in spermatozoa incubated in Ca^{+ +}-free medium, A23187 failed to induce acrosomal loss. Furthermore, spermatozoa incubated in the presence of seminal plasma or spermatozoa obtained following a 1-hour “swim-up” procedure showed an identical timecourse of appearance of the CP pattern, indicating the lack of effect of seminal plasma on capacitation in the squirrel monkey.     

The development of circadian rhythm of human body temperature

Abstract

Daily periodic changes of body temperature were examined in 138 subjects ranging in age between 5 days and 44 years. Whereas the circadian rhythm of human body temperature was not discerned in newborn babies, body temperatures were higher during daytime than during nighttime in infants over one month. Temperature rhythm similar to that of adults, with respect to phase, was observed in the age groups of ten to eleven months and over, earlier than previously reported. The amplitude in circadian oscillation was, however, significantly larger in children between 7 months and 7 years of age than in adults. Thus, it is concluded that the adult type of circadian rhythm of human body temperature is fully established with respect to phase and amplitude after 7 years of age.     

生物钟机制研究进展

由生物体内源性生物钟所产生的昼夜节律是近年来生命科学的研究热点之一。几种模型生物（蓝细菌、脉孢菌、拟南芥、果蝇、小鼠）的生物钟相关基因相继被克隆和鉴定,为理解昼夜节律的分子机制奠定了基础。振荡器蛋白对其编码基因的负反馈调控可能是不同生物的生物运作普遍机制,在此基础上,不同生物有不尽相同的调控方式;隐色素可能是高等生物的共同生物钟光受体。     

Evidence of a diurnal rhythm in implicit reward learning

Many aspects of hedonic behavior, including self-administration of natural and drug rewards, as well as human positive affect, follow a diurnal cycle that peaks during the species-specific active period. This variation has been linked to circadian modulation of the mesolimbic dopamine system, and is hypothesized to serve an adaptive function by driving an organism to engage with the environment during times where the opportunity for obtaining rewards is high. However, relatively little is known about whether more complex facets of hedonic behavior – in particular, reward learning – follow the same diurnal cycle. The current study aimed to address this gap by examining evidence for diurnal variation in reward learning on a well-validated probabilistic reward learning task (PRT). PRT data from a large normative sample (N = 516) of non-clinical individuals, recruited across eight studies, were examined for the current study. The PRT uses an asymmetrical reinforcement ratio to induce a behavioral response bias, and reward learning was operationalized as the strength of this response bias across blocks of the task. Results revealed significant diurnal variation in reward learning, however in contrast to patterns previously observed in other aspects of hedonic behavior, reward learning was lowest in the middle of the day. Although a diurnal pattern was also observed on a measure of more general task performance (discriminability), this did not account for the variation observed in reward learning. Taken together, these findings point to a distinct diurnal pattern in reward learning that differs from that observed in other aspects of hedonic behavior. The results of this study have important implications for our understanding of clinical disorders characterized by both circadian and reward learning disturbances, and future research is needed to confirm whether this diurnal variation has a truly circadian origin.     

Osmotic fragility of erythrocytes in Bolivian and Brazilian squirrel monkeys (Saimiri sciureus).

Median corpuscular fragility of erythrocytes does not differ significantly between fed and fasted Bolivian and Brazilian squirrel monkeys and are similar to values reported in humans and rhesus monkeys. This report further confirms that the fasting hyperbilirubinemia present only in Bolivian squirrel monkeys with a Gilbert-like syndrome is not due to an increased fragility of erythrocytes and should be classified as a nonhemolytic hyperbilirubinemia.     

The effect of neonatal administration of monosodium glutamate on the circadian control of food intake in the rat

Abstract

Neonatal treatment with monosodium glutamate (MSG) results in a substantial degeneration of the inner layer of the retina and a decreased diameter of the optic nerves. Nevertheless, MSG‐treated animals entrain and re‐entrain to a light dark cycle. The question arises whether MSG selectively destroys the optic pathways which are involved in vision but not the retinohypothalamic trart that mediates entrainment. In these experiments not only entrainment and re‐entrainment of the circadian food intake rhythm of MSG‐treated rats was investigated but also the freerunning period under continuous bright and dim light It appears that MSG‐treated rats have shorter freerunning periods under continuous illumination than controls. Therefore, these results suggest that also those pathways involved in entrainment of the circadian food intake rhythm are affected by neonatal treatment with MSG.     

Effect of different lighting conditions on circadian developmental rhythms and behaviour in Ephestia kuehniella Zell

Abstract

A study was made on the developmental rhythms of Ephestia kuehniella during different photoperiods: constant lighting (L/L), under conditions of 12 hours light per day (L/D) and in constant darkness (D/D). Observations were made every 2 hrs, for 3 successive 24‐hr periods, of the number of wandering larvae emerging from food, the number of pupations and of imaginai moults. Emergence of wandering larvae is rhythmic only under L/D conditions, and in addition this is also affected by the density of the larvae. Rhythm is least apparent with greatest density of the larvae. Pupation in E. kuehniella is a non‐rhythmic process with each of the photoperiods examined, whereas the imaginai moult is characterized by an endogenous (existing under D/D conditions) rhythm. Emergence of imagines is non‐rhythmic under L/L, and also when pupae under L/D fail to receive the final period of darkness. The rhythm of the imaginai moult is possibly controlled by the biological clock, which stops under conditions of constant light.     

Parametric and nonparametric entrainment of circadian locomotor rhythm in the Japanese honeybee Apis cerana japonica

The circadian rhythm of locomotor activity in the Japanese honeybee Apis cerana japonica was studied to determine the involvement of parametric and/or nonparametric entrainment. The rhythm was entrained to a skeleton photoperiod in which a 1-h first light pulse was imposed in the morning along with a second light pulse in the evening, as well as to a complete photoperiodic regime (LD 12:12). However, the timing of peak activity relative to the lights-off in the evening in the skeleton photoperiod was earlier than that in the complete photoperiod. A single daily light pulse in the evening entrained the rhythm, whereas a daily light pulse in the morning allowed free-running as in constant darkness. The free-running period (τ) of locomotor activity in constant light became longer as the light intensity increased. A Winfree's type I phase response curve of the locomotor activity rhythm was obtained using a single 1-h light pulse. The results suggest that both parametric and nonparametric entrainment are involved in the circadian rhythm of individual locomotor activity in this honeybee.     

Circadian range of entrainment in the semilunar eclosion rhythm of the marine insect clunio marinus

The semilunar eclosion of the intertidal chironomid Clunio is controlled by a semilunar timing of pupation in combination with a daily timing of emergence. This results in reproductive activities of a laboratory population every 15 days at a distinct time of day (in nature mostly in correlation with the afternoon low water time on days with spring tides). The entrainment of the timing processes has been tested under various periods of the daily light-dark cycle in order to check the circadian organization of the timing mechanisms as suggested for the perception of the semilunar zeitgeber situation (a distinct phase relationship between the 24 h light-dark cycle and the 12.4 h tidal cycle recurring after every 15th light-dark cycle, named semimonthly zeitgeber cycle) as well as for the daily zeitgeber (the 24 h light-dark cycle). With respect to the semilunar timing, a strong entrainment was only possible in semimonthly zeitgeber cycles with light-dark cycle periods close to the 24-h day (light-dark cycles of 10:10 to 14:14). This limited circadian range of entrainment of an endogenous circasemilunar long-term rhythm (syn. oscillator) conforms with the hypothesis for a circadian clock component as an intrinsic part of the semilunar zeitgeber perception.The range of entrainment for the daily timing was obviously wider which may be discussed either in relation to a multioscillatory circadian organization of the midges or in relation to different coupling characteristics of one circadian oscillator during semilunar and daily timing.     

Seasonal changes of serum concentrations of estradiol and progesterone in Bolivian squirrel monkeys (Saimiri sciureus)

Serial measurements of estradiol (E2) and progesterone (P) were used to describe the ovarian cycle of the Bolivian squirrel monkey. Group-caged, sexually mature female squirrel monkeys, housed with males, were sampled daily between 0900 and 1100 hr. Sampling was carried out during the breeding and nonbreeding seasons, for periods of 19–20 days from September 1981 to May 1982. Seasonal differences in serum concentrations of E2 and P were found with low levels of E2 and P and an absence of preovulatory surges of E2 during the nonbreeding season. This pattern was also observed in some animals during the breeding season. An abrupt increase in serum P concentrations in December appeared to signal the onset of cycling. Cycling animals had well-defined peaks of E2 (450–9,500 pg/ml) followed by increasing levels of P, which were >200 ng/ml in some animals. After the breeding season, E2 and P levels returned to their initially low levels. Levels of both steroids in cycling animals were higher than those reported for other primates and for previous measurements made in squirrel monkeys. Cycle length based on time interval between consecutive E2 peaks varied from 6–12 days.     

The influence of timeshift on circadian rhythm of sensitivity to X-irradiation in mice

For two groups of male C3H mice an eastbound transmeridional flight was simulated by inducing a time shift of the L:D schedule of 8 hr. The assumed flight brought about a maximal reduction of the daily light and dark span, respectively. A third group remained unshifted. At seven different times during the following day, subgroups of the time shifted mice as well as of the group with unchange schedule were exposed to whole body X-irradiation. Mortality and body temperature of each animal were registered for 30 days following exposure and were regarded as indicators of radiation response. Radioresistance was found to be highest during the second half of the daily light span, confirming earlier reports by other authors. Weil defined effects of the time shift and a corresponding shift of the acrophase of radioresistance could be demonstrated. There was no significant difference between the two time shifted groups, but there was a consistent slight trend towards an advantage for the group whose L:D shift resulted in a maximally reduced dark span.     

Freerunning and entrained circadian rhythms in activity,eating and drinking in the cat

Abstract

Because cats with pontile lesions exhibit an abnormal behavior that is under photoperiodic control, and because circadian rhythms are implicated in photoperiodic control mechanisms, an effort was made to detect circadian rhythms in the cat. Cats were isolated from all extraneous stimuli in soundproof chambers for extended periods of time. Photocells were used to monitor activity, eating and drinking in different LD cycles, in constant light at two intensities, and in constant dark. Freerunning circadian rhythms were found in the constant conditions, and entrained nocturnal patterns occurred in most of the LD cycles. The higher intensities of ambient illumination disrupted the freerunning rhythms. The freerunning rhythms were always greater than 24 h, ranging from 24.2 to 25 h. Measurements of food intake of cats living in a large colony room, obtained by weighing the food, revealed that a nocturnal pattern of entrainment was not present in the majority of the cats. Instead, most cats in the colony exhibited a random pattern of eating throughout the light and dark period of the LD cycle. However, the variation among the cats in the colony was considerable, extending from nocturnal to diurnal patterns of eating. A diurnal pattern of human activity was present in the colony and may account for the disruption of a basic nocturnal pattern. The presence of circadian rhythms in the cat leads us to consider the coincidence models for photoperiodic induction as possible explanations of the photoperiodic control of the lesion‐induced abnormal behavior.     

Lack of a circadian rhythm in the ability of the gametocytes of Plasmodium falciparum to infect Anopheles gambiae

Batches of Anopheles gambiae were fed once during the day or once or twice during the night on 12 carriers naturally infected with gametocytes of P. falciparum. No overall difference was noted in the oocyst numbers in batches of mosquitoes fed during the night as compared to the daytime.     

Phytochrome A resets the circadian clock and delays tuber formation under long days in potato

Transgenic potatoes (Solanum tuberosum) with either increased (sense transformants) or reduced (antisense transformants) phytochrome A (phyA) levels were used, in combination with specific light treatments, to investigate the involvement of phyA in the perception of signals that entrain the circadian clock. Far-red or far-red plus red light treatments given during the night reset the circadian rhythm of leaf movements in wild-type plants and phyA over-expressors, but had little effect in phyA under-expressors. Far-red light was also able to reset the rhythm of leaf movement in wild-type Arabidopsis thaliana but was not effective in mutants without phyA. Blue light was necessary to reset the rhythm in phyA-deficient potato plants. Resetting of the rhythm by far-red plus red light was only slightly affected in transgenic plants with reduced levels of phytochrome B. The production of tubers was delayed by day extensions with far-red plus red light, but this effect was reduced in transgenic lines deficient in phyA. We conclude that phyA is involved in resetting the circadian clock controlling leaf movements and in photoperiod sensing in light-grown potato plants.     

The effects of natural substrate discontinuities on the quadrupedal gait kinematics of free‐ranging Saimiri sciureus

Wild primates encounter complex matrices of substrates that differ in size, orientation, height, and compliance, and often move on multiple, discontinuous substrates within a single bout of locomotion. Our current understanding of primate gait is limited by artificial laboratory settings in which primate quadrupedal gait has primarily been studied. This study analyzes wild Saimiri sciureus (common squirrel monkey) gait on discontinuous substrates to capture the realistic effects of the complex arboreal habitat on walking kinematics. We collected high‐speed video footage at Tiputini Biodiversity Station, Ecuador between August and October 2017. Overall, the squirrel monkeys used more asymmetrical walking gaits than symmetrical gaits, and specifically asymmetrical lateral sequence walking gaits when moving across discontinuous substrates. When individuals used symmetrical gaits, they used diagonal sequence gaits more than lateral sequence gaits. In addition, individuals were more likely to change their footfall sequence during strides on discontinuous substrates. Squirrel monkeys increased the time lag between touchdowns both of ipsilaterally paired limbs (pair lag) and of the paired forelimbs (forelimb lag) when walking across discontinuous substrates compared to continuous substrates. Results indicate that gait flexibility and the ability to alter footfall patterns during quadrupedal walking may be critical for primates to safely move in their complex arboreal habitats. Notably, wild squirrel monkey quadrupedalism is diverse and flexible with high proportions of asymmetrical walking. Studying kinematics in the wild is critical for understanding the complexity of primate quadrupedalism.