A circadian pacemaker in free-living chipmunks: essential for survival?

The importance of circadian timing was evaluated for 18 months from late-April 1997 through October 1998 in a high-density population of free-living eastern chipmunks, Tamias striatus, at a 4-ha forest site in the Allegheny Mountains. Included in the radiocollared field group were 30 chipmunks with supra-chiasmatic nucleus-targeted lesions, 24 surgical controls, and 20 intact controls. An additional 17 chipmunks were used in a laboratory study as lesion-calibration controls to correlate degree of circadian arrhythmicity with extent of supra-chiasmatic nucleus deletion. Survival was documented in the field by daily radio tracking and by regular trapping censuses except during winter hibernation. A significantly higher proportion of supra-chiasmatic nucleus-lesioned than surgical control chipmunks or intact controls were killed by weasel predation during the first 80 days after repatriation. A 28-h continuous census found no surface activity of any chipmunks during hours of darkness. However, episodes of nocturnal movement were detected within the permanent dens by radio telemetric data logging, especially in supra-chiasmatic nucleus-lesioned animals. Excavation and mapping of six chipmunk burrow systems aided in the interpretation of the telemetric activity data. Nighttime restlessness of supra-chiasmatic nucleus-lesioned animals may have acted as a clue to the predator for locating its prey.

Behavior of SCN-lesioned chipmunks in natural habitat: a pilot study.

The necessity of a circadian pacemaker, the suprachiasmatic nuclei (SCN), for survival was evaluated in a population of approximately 65 wild eastern chipmunks, Tamias striatus. The research involved over 3000 h of field-work between May 1995 and October 1997 on a study site at Mountain Lake Biological Station, Virginia. The 28 chipmunks randomly designated as project animals included 10 SCN-lesioned chipmunks, 5 surgical controls (sham-lesioned), and 13 intact controls. Visual observation, live trapping, and radio telemetric tracking were used to assess 6 aspects of survival and reproduction. Upon release after surgery, every animal returned to its den site and was able to maintain its home territory. In warm months from May through October, all chipmunks were active above ground with a strictly day-active pattern. During the remaining cold months, they were normothermic but relatively torpid in their underground dens for extended periods of time. Short-term mortality for the initial 3 months included only a single intact control chipmunk; loss for the extended period from August 1995 to October 1996 was 40% for the SCN-lesioned animals, 0% for surgical controls, and 15.4% for the intact controls. Survival differences were not significant between surgical control and intact control groups but were significant (alpha = .10) between SCN-lesioned and pooled control groups. Annual body weight patterns were similar for both groups. Most individuals in both SCN-lesioned and control groups were reproductively active in the spring and fall breeding periods. Lack of major differences may be attributable to the exceptionally favorable conditions for survival such as a very abundant fall acorn crop, medium population size, and absence of heavy predation.

Relationship of circadian temperature and activity rhythms in two rodent species.

Despite the large number of publications concerning circadian body temperature in rodents, relatively little is known about phase relationships of the body temperature cycle relative to daily locomotor rhythms. Phase angle differences between core body temperature and locomotor activity were determined by a group of overlapping methods for 14 hamsters and 11 chipmunks under constant light (LL) and entrained (LD) photo schedules. The study compared the onset of the body temperature cycle with three separate components of daily locomotor activity: the onset of wheel running, the onset of total activity in a standard wheel cage, and the onset of total activity in a restricted cage, respectively. The temperature cycle showed a pronounced phase lead over onset of wheel-running activity in all hamsters and in the majority of chipmunks, but the phase lead was reduced when total activity was considered. With activity restriction, the onset of temperature rise and activity onset concurred. The body temperature onset in some species may serve as a valid phase point for indirect measurement of circadian timing, but the potential artifact of masking by heat generated from muscular activity should be kept clearly in mind.

Circadian performance of suprachiasmatic nuclei (SCN)-lesioned antelope ground squirrels in a desert enclosure.

Circadian activity parameters of 53 white-tailed antelope ground squirrels, Ammospermophilus leucurus, were measured to determine the role of the suprachiasmatic nuclei (SCN) pacemaker in their health and survival. Wheel-running activity was monitored in the laboratory with 44 individuals to document the presence of free-running circadian rhythms and ability to entrain to light-dark cycles. Twenty-two individuals were returned to the desert site of origin, including 12 intact control animals and 10 animals whose circadian timing had been disrupted by SCN-lesioning. Time of activity was recorded continuously for 15 days in a large outdoor enclosure by a motion detector, a microchip transponder detector, and video surveillance. An unplanned nighttime attack by a feral cat resulted in the death of 60% of the SCN-lesioned animals and 29% of the control animals in the enclosure. Surface activity of SCN-lesioned animals at the food cache occurred both in daytime and at night, ranging from 16.0% nighttime activity for one partially lesioned individual to 52.1% for one completely lesioned animal. Controls were strongly day-active, with nighttime surface trips constituting only 0-1.3% of all excursions to the cache. Nine wild free-ranging individuals, including one with a radiotransmitter collar, were exclusively day-active. One of the functions of the SCN in mammals may be to reduce activity of animals during times that are unfavorable for activity.

Circadian rhythmicity after neural transplant to hamster third ventricle: specificity of suprachiasmatic nuclei.

Neural transplants into the third ventricle utilized to quantitatively assess the effectiveness of fetal tissue from selected brain sites in restoring circadian locomotor rhythmicity of adult hamsters rendered arrhythmic by lesions of the suprachiasmatic nuclei (SCN). Circadian function was continuously monitored in recording wheel cages under controlled environmental conditions. Animals which remained arrhythmic for 3-4 weeks after SCN lesions received transplants of neural tissue from 13-14-day-old fetuses: either SCN tissue or non-SCN tissue (cerebral cortex or hypothalamus excluding SCN). Quantitative evaluation of the data indicated partial restoration of circadian rhythmicity in 37% of 19 animals with SCN transplants, but in 0% of the 9 animals with non-SCN neural transplants. The mean time for reappearance of rhythmicity was 20 days after SCN transplantation. Animals were sacrificed 8-10 weeks after transplantation for histological analysis in order to visualize lesion placement and to characterize transplants. The cytoarchitecture and neuropeptide organization of the transplants were consistent with the brain region. Only SCN transplants were characterized by aggregates of small neurons with codistributed immunoreactivity for SCN-characteristic neuropeptides.

Light-sampling behavior in photoentrainment of a rodent circadian rhythm.

Behavioral aspects of photoentrainment of circadian locomotor activity rhythms were recorded for a nocturnal den-dwelling rodent, the flying squirrel, Glaucomys volans. Methods included both telemetric monitoring and infrared observations of animals under constant dark (DD) or light-dark (LD) schedules in either standard wheel cages or in newly developed simulated den cages. By means of the den cages, several aspects of a circadian activity cycle could be simultaneously measured emphasizing the arousal from rest, the light-sampling behavior by which a squirrel assessed the environmental photoregimen, and the phase-shifting by which photoentrainment was achieved. Each animal in a den cage remained for 12 or more hours of its rest period almost exclusively in the darkened nest box, then at an abrupt arousal time moved to the light-sampling porthole. In darkness each animal initiated wheel activity immediately after arousal; light at arousal time, however, induced a return to the nest box for a nap and a delay phase-shift in onset of activity of approximately 40 min. On subsequent days, each animal appeared to be free-running (tau FR less than 24 h) until onset again advanced into the light period. A squirrel usually viewed only a few minutes light per day, and on free-running days occasionally saw none of the 12-h light period. The significance of these data for theories of circadian photoentrainment is discussed.

Circadian photoentrainment: parameters of phase delaying.

Experiments were carried out using simulated den cages to delineate specific characteristics of phase delaying in circadian photoentrainment of a nocturnal rodent, the flying squirrel. The principal experiments entailed presentation of one to five consecutive 15-min white-light pulses per activity cycle at activity onset to animals free-running in darkness, in order to determine the immediate and final phase-shifting effect. Auxiliary experiments recorded entrainment patterns on light-dark (LD) schedules in the den cages. Phase response curves (PRCs) based on 15-min white-light pulses in standard wheel cages were also constructed for these animals as background information for interpreting the phase-delaying experiments. Exposure of a den animal to light by light sampling at the time of initial arousal from the rest state at circadian time (CT) 12, either by an LD schedule or by a 15-min light pulse, resulted in a return to the nest box for a short rest period. The phase delay occurring after a single light exposure at activity onset was equal to the induced rest, thus suggesting an immediate phase shift. The maximum delay was about 1 1/2 hr/cycle, with the amount of delay related to the number of light exposures. During the photoentrained state on an LD schedule, the activity rhythm of a den-housed animal was essentially free-running on the days following a phase delay. The data are used to expand current models for photoentrainment of circadian activity rhythms in nocturnal rodents.

Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms.

Environmental light cycles are the dominant synchronizers of circadian rhythms in the field, and artificial light cycles and pulses are the major tools used in the laboratory to analyse properties of circadian systems. It is therefore surprising that few studies have analysed the physical parameters of light stimuli that affect circadian rhythms. There have previously been no spectral sensitivity measurements for phase shifting the circadian rhythms of mammals and only two preliminary reports on the wavelength dependence of this response exist. Using the magnitude of phase shift caused by a single 15-min pulse of monochromatic light given 6 h after activity onset, we have now characterized the spectral sensitivity of the photoreceptors responsible for phase shifting the locomotor rhythm of the hamster (Mesocricetus auratus). The sensitivity curve for this response has a maximum near 500 nm and is similar to the absorption spectrum for rhodopsin. Although the spectral sensitivity is consistent with a rhodopsin-based photopigment, two features of the photoreceptive system that mediates entrainment are unusual: the threshold of the response is high, especially for a predominantly rod retina like that of the hamster, and the reciprocal relationship between intensity and duration holds for extremely long durations (up to 45 min). These results suggest that the photoreceptive system mediating entrainment is markedly different from that involved in visual image formation.