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The Journal of Neuroscience, January 1, 2002, 22(1):357-364
The Suprachiasmatic Nucleus Is Essential for Circadian Body Temperature Rhythms in Hibernating Ground Squirrels
Norman F. Ruby1, John Dark2, D. Erik Burns1, H. Craig Heller1, and Irving Zucker2, 3 1 Department of Biological Sciences, Stanford University, Stanford, California 94305, and Departments of 2 Psychology and 3 Integrative Biology, University of California, Berkeley, California 94720
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Body temperature (Tb) was recorded at 10 min intervals over 2.5 years in female golden-mantled ground squirrels that sustained complete ablation of the suprachiasmatic nucleus (SCNx). Animals housed at an ambient temperature (Ta) of 6.5°C were housed in a 12 hr light/dark cycle for 19 months followed by 11 months in constant light. The circadian rhythm of Tb was permanently eliminated in euthermic and torpid SCNx squirrels, but not in those with partial destruction of the SCN or in neurologically intact control animals. Among control animals, some low-amplitude Tb rhythms during torpor were driven by small (<0.1°C) diurnal changes in Ta. During torpor bouts in which Tb rhythms were unaffected by Ta, Tb rhythm period ranged from 23.7 to 28.5 hr. Both SCNx and control squirrels were more likely to enter torpor at night and to arouse during the day in the presence of the light/dark cycle, whereas entry into and arousal from torpor occurred at random clock times in both SCNx and control animals housed in constant light. Absence of circadian rhythms 2.5 years after SCN ablation indicates that extra-SCN pacemakers are unable to mediate circadian organization in euthermic or torpid ground squirrels. The presence of diurnal rhythms of entry into and arousal from torpor in SCNx animals held under a light/dark cycle, and their absence in constant light, suggest that light can reach the retina of hibernating ground squirrels maintained in the laboratory and affect hibernation via an SCN-independent mechanism.
Key words: suprachiasmatic nucleus; hibernation; circadian; torpor; body temperature; golden-mantled ground squirrel
INTRODUCTION
Mammals from several orders engage in seasonal heterothermy. Survival during times of food shortages and low winter temperatures is facilitated by marked reductions in metabolic rate and body temperature (Tb). In heterothermic mammals, individual bouts of torpor range in duration from several hours to several days. A hibernation season typically consists of multiday torpor bouts that alternate with brief (<20 hr) intervals of euthermia (Lyman et al., 1982
). By contrast, other rodent species engage in daily torpor bouts that are relatively brief (i.e., 2-10 hr) and restricted to the inactive phase of the rest-activity cycle (Lindberg and Hayden, 1974
The role of the circadian system in timing multiday torpor bouts during hibernation is less clear. Rodent hibernators typically remain in their underground burrows continuously throughout the winter where they are not exposed to daily changes in illumination. Nevertheless, circadian control of entry into and arousal from individual torpor bouts remains a distinct possibility. Tb rhythms persist with a mean circadian period of 22 hr during deep torpor (Tb ~ 12°C) in golden-mantled ground squirrels (Spermophilus lateralis) (Grahn et al., 1994
The SCN is a likely candidate for circadian control of torpor bout duration during hibernation. Not only is the SCN the primary circadian pacemaker in mammals (Rusak and Zucker, 1979
Two previous reports documented that ablation of the SCN is associated with marked changes in the duration of individual torpor bouts and also affects the duration of the hibernation season (Ruby et al., 1996
MATERIALS AND METHODS
Animals
The female golden-mantled ground squirrels used in this study were born in the Berkeley laboratory to pregnant females that were trapped near Truckee, CA at an elevation of1800 m. Squirrels were housed individually in a 14:10 light/dark (LD) cycle [lights on from 7:00 A.M. to 9:00 P.M., Pacific standard time (PST)] at Ta = 23 ± 2°C. Food (Purina Chow #5012) and water were available ad libitum, and animals were weighed weekly (± 0.1 gm) throughout the study. Squirrels were provided cotton batting for nesting material.
Brain lesions
When animals were 2-3 years of age and at or near their annual body mass nadir they were deeply anesthetized with pentobarbital sodium (12.5 mg/100 gm body mass + 0.1 mg/each additional 10 gm body mass, administered intraperitoneally) supplemented with methoxyflurane vapors (Metofane) as necessary to maintain deep anesthesia. Squirrels were positioned in a stereotaxic instrument (David Kopf Instruments, Tujunga, CA) with the incisor bar 1.0 mm above the interaural line, and a single midline incision was made. Bilateral radiofrequency lesions were made at 8.2 and 8.4 mm anterior to ear bar zero, ±0.3 mm lateral to the midsagittal sinus, and 9.7 mm ventral to dura by passing current (Body temperature and locomotor activity
All squirrels had radiofrequency transmitters (model VM-FH disc; Minimitter Co.) implanted in their abdominal cavities for telemetric recording of Tb 1-2 years after brain surgery. Calibration and implantation of transmitters were as described previously (Dark et al., 1992Autopsy procedures
At the end of the study squirrels were administered a lethal dose of pentobarbital sodium (intraperitoneally) and perfused with 0.9% saline followed by buffered formalin. Brains were immediately removed, and frozen coronal sections (50 µm) were cut through an area beginning rostral to the optic chiasm and ending caudal to the retrochiasmatic area. Tissue was stained with a Nissl-type stain (cresyl violet), and damage was assessed independently by two investigators without knowledge of the corresponding behavioral or body mass data. Densely stained tissue that had apparently viable neurons along the borders of the damaged area, but within boundaries of the SCN, was considered evidence of possible residual SCN tissue. Complete SCN ablation was strictly defined as the unambiguous absence of any SCN tissue. The extent of damage to non-SCN nuclei was estimated by comparing tissue sections of control animals and those with brain lesions. When interinvestigator assessment of tissue damage to non-SCN nuclei differed by >15%, sections were reexamined until a consensus was reached; re-examination was necessary in <10% of all sections.Data analysis
Circadian rhythms during euthermia. SCNx squirrels were categorized as either "continuous hibernators" (SCNx-CH) that expressed torpor bouts throughout the year or "noncontinuous hibernators" (SCNx-NCH) that had typical seasonal cycles of hibernation; these designations are retained from earlier studies of these animals (Ruby et al., 1996
RESULTS
Histological analysis of brain lesions
A detailed histological analysis of brain lesions for animals in this study has been reported (Ruby et al., 1998
Circadian Tb rhythms in euthermic squirrels between hibernation seasons
Circadian Tb rhythms were observed in all control animals in the months between hibernation seasons. During housing in the LD cycle, rhythms were always entrained (mean period = 24.05 ± 0.04 hr). At the beginning, middle, and end of each euthermic season in LL, tau ranged from 23.67 to 24.33 hr and was always >24.17 or <23.83 hr in individual animals. Tau never changed by >10 min (i.e., one sampling interval) in individual squirrels within each euthermic season or across successive ones (Fig. 1); mean (±SE) Q value = 0.82 ± 0.01.
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Figure 1. Representative Tb plots from control (A), SCNx-CH (B), SCNx-NCH (C), and PSCNx (D) squirrels. Periodogram results [Q(p)] for each animal are adjacent to their respective plots; tau is given for significant peaks (p < 0.001). Data in A, C, and D were obtained during the middle phase of each squirrel's annual nonhibernation season during housing in constant light. Because annual patterns of hibernation were eliminated in SCNx-CH animals, Tb data (B) were obtained for these squirrels during the single longest euthermic period during housing in constant light.
In contrast to control animals, no significant circadian rhythms in Tb were detected in SCNx-NCH animals at any time in either the LD cycle or LL (p > 0.05) (Fig. 1). Euthermic intervals between individual torpor bouts never exceeded 10 d in SCNx-CH squirrels, consequently, periodogram analyses were conducted on data spans of 5-7 d for each of these animals. No significant circadian periodicity was detected in any of these squirrels (p > 0.05) (Fig. 1). Tb rhythms of PSCNx squirrels entrained to the LD cycle and then free-ran during LL with tau values ranging from 23.83 to 24.50 hr (Q value = 0.74) in LL (Fig. 1).
Circadian Tb rhythms before onset and after termination of the hibernation season
Circadian organization for squirrels housed in LD and LL conditions was evaluated during the 5 d periods before the first torpor bout, and after the final torpor bout, of each hibernation season. Normal integrity of Tb rhythms was maintained before the onset of the first hibernation bout in control and PSCNx squirrels, whereas Tb rhythms were absent in all SCNx-NCH animals (Fig. 2). In two of six control animals, some loss in rhythm coherence was observed during the first 2-3 d after the terminal arousal from hibernation seasons in the LD cycle and in LL (Fig. 2). Arrhythmia was not observed in the remaining four control animals or in any of the PSCNx squirrels, but all SCNx-NCH and SCNx-CH animals were arrhythmic before and after each hibernation season.
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Figure 2. Representative Tb plots from different control (A, B) and SCNx-NCH (C, D) squirrels before (left panels) and after (right panels) a hibernation season in LL. Circadian Tb rhythms were robust in all control animals in the days immediately preceding the onset of hibernation. Post-hibernation arrhythmicity was observed in two of six control animals and lasted for no more than 3 d (A, right panel). Tb rhythms were undetectable in SCNx-NCH squirrels before and after hibernation.
Circadian Tb rhythms during deep torpor
Periodogram analysis confirmed the absence of circadian Tb rhythms in 45 of 80 torpor bouts expressed by control animals in LL. No further analyses were performed on those bouts. In the remaining 35 bouts, changes in Tb frequently paralleled small changes in Ta. In most cases, the timing and amplitude of these rhythms were similar (Fig. 3).
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Figure 3. Representative plots of relative Tb and Ta values from control (left panels) and SCNx-NCH (right panels) squirrels during deep torpor bouts in which changes in Tb closely parallel changes in Ta. Tb is the top, and Ta is the bottom line in each plot. Vertical reference lines indicate Tb nadirs. Data are plotted as relative values because the large difference between Tb and Ta (2-3°C) and the very small rhythm amplitudes (<0.05°C in many cases) made rhythm synchrony difficult to visualize in the raw data. To facilitate visualization of phase relations between Tb and Ta rhythms, the interval between Tb and Ta was reduced by subtracting a different constant from raw Tb and Ta values for each torpor bout. This normalization procedure preserves the rhythm phases and amplitudes observed in the raw data. Note that rises in Ta after the nadir always precede rises in Tb.
Phase relations between simultaneously recorded Tb and Ta records were evaluated by visual inspection; they were judged as synchronous if they unambiguously oscillated in unison and as asynchronous if concurrent Tb and Ta changes were in opposite directions. Records in which Tb and Ta rhythms were synchronized for only part of a torpor bout were excluded from the analysis that was performed by an independent investigator not otherwise involved in this study. Pearson's correlation coefficient between Tb and Ta was calculated for each torpor bout to quantify the magnitude of synchronization between Tb and Ta. Correlation coefficients from every bout were statistically significant (p < 0.001) and used to generate mean coefficients for synchronous or asynchronous torpor bouts.
There was a robust correlation for both control and SCNx-NCH animals (r > 0.60) between Tb and Ta for bouts in which these rhythms were categorized as synchronous (p < 0.001) (Fig. 4). Mean correlation coefficients for both groups of animals in which the rhythms were judged as asynchronous were weak (r < 0.11) and significantly lower than values obtained for synchronous bouts (p < 0.001) (Fig. 4). In the synchronous bouts, the nadir of the Ta oscillation always preceded the nadir of the Tb oscillation in both control and SCNx-NCH squirrels (Fig. 3). The time lag between the nadirs of these two oscillations was over four times greater for SCNx-NCH animals than for control squirrels (p < 0.001) (Table 1). In the asynchronous bouts, the nadirs of Tb and Ta rhythms were ~180° out of phase (Fig. 5), and the interval between the nadirs of the Ta oscillation and the subsequent Tb oscillation did not differ between control and SCNx-NCH groups (p > 0.05) (Table 1).
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Figure 4. Mean (±SE) r values for correlations between Tb and Ta for torpor bouts that were judged as synchronous or asynchronous based on visual inspection of the data. *p < 0.001 compared with synchronous bouts.
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Table 1. Period and phase of Tb and Ta rhythms during deep torpor in LL
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Figure 5. Representative Tb and Ta plots from control (left panels) and SCNx-NCH (right panels) squirrels during deep torpor bouts in which Tb rhythms appear to be independent of changes in Ta. Conventions as in Figure 3. Note that rises in Tb occur when Ta is declining or stable (indicated by arrows). Absolute values were normalized as in Figure 3.
Significant periodicity (p < 0.001) in the circadian range was evident in the rhythms of control animals in which Tb and Ta rhythms were synchronous or asynchronous (Table 1). Rhythm periods ranged from 23.7 to 28.5 hr for Tb and 22.4 to 26.9 hr for Ta and did not differ between synchronous and asynchronous bouts. The difference between Tb and Ta periods within individual torpor bouts was negligible when these two rhythms were synchronized, but exceeded 90 min when the two rhythms were asynchronous. In the latter case, the mean periods of the Tb and Ta rhythms were >24 hr and <23 hr, respectively (Table 1). Significant circadian Tb rhythms were detected in SCNx-NCH animals during torpor bouts in which Tb and Ta were synchronized (p < 0.001) but not when these two measures were asynchronous (p > 0.05) (Table 1).
Timing of torpor entry and arousal
Entries into and arousals from torpor were categorized into four 6 hr time bins. Because only two PSCNx animals survived until the end of the study, data for this group were excluded from the statistical analysis. The time bin during which squirrels entered and aroused from torpor did not differ among the SCNx-NCH, SCNx-CH, and control squirrels (p > 0.05). Data from SCNx-NCH and SCNx-CH were combined to form a single SCNx group for subsequent analyses. Entry into torpor occurred more frequently during the first 6 hr of the dark phase (ZT 12-18) for squirrels maintained in the LD cycle (p < 0.05) (Fig. 6) but was distributed equally in each 6 hr time bin for animals housed in LL (p > 0.05) (Fig. 6). Arousals from torpor were more likely during the daytime in both control and SCNx animals in LD conditions (p < 0.05) (Fig. 6) but occurred with equal frequency in each time bin for squirrels housed in LL (p > 0.05) (Fig. 6).
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Figure 6. Time of day of entries in an LD cycle (A) and in LL (B) and of arousals from torpor in an LD cycle (C) and in LL (D) for control and SCNx squirrels. Bars with different letters differ significantly from each other (p < 0.05). There were no differences among control and SCNx animals in either lighting condition. Statistical comparisons were not made between LD and LL values. Zeitgeber time 0 = light onset (8:00 A.M. PST) in the 12 hr LD cycle.
Duration of torpor entry and arousal
Entry into deep torpor (Tb < 8.0°C) was completed in 9.4 ± 0.5 hr by control animals but required an extra 2 hr for SCNx-CH, SCNx-NCH, and PSCNx squirrels (p < 0.05) (Fig. 7); there were no significant differences among the latter three groups (p > 0.05). In contrast, the four groups did not differ in the time needed to arouse from torpor (p > 0.05) (Fig. 7), which was 64.9 ± 11.3 min.
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Figure 7. Torpor entry and arousal durations for all animals. Entries and arousals are defined as the time required for Tb to change between 14 and 34°C. *p < 0.05 compared with control value.
DISCUSSION
Circadian Tb rhythms during the nonhibernation season were eliminated in animals that sustained complete ablation of the SCN but persisted in ground squirrels with as little as 10% of the SCN intact. Tb rhythms were robust in control animals during 11 months of exposure to constant light, as previously documented for locomotor activity rhythms in this species (Zucker et al., 1983
The persistence of Tb rhythms in all control and some SCNx squirrels during some bouts of deep torpor may reflect passive heating and cooling in response to changes in Ta or, alternatively, the expression of a weak endogenous Tb rhythm synchronized to Ta oscillations. The sensitivity of Tb to small fluctuations in Ta emphasizes the importance of continuous monitoring of Ta during torpor as a means of distinguishing endogenous from exogenously driven Tb rhythms. The period of the Ta rhythm must be assessed separately for each bout, because the Ta rhythm often was not stable but varied by >4 hr. Small-amplitude Ta rhythms were sometimes the result of cyclic activity of the machinery used to cool the animal room and likely are present in the majority of laboratory investigations, although not usually reported. Ground squirrels housed in an environmental chamber in which cyclic Ta fluctuations are absent at 9°C, nevertheless continue to express circadian Tb rhythms during torpor (J. E. Larkin, P. Franken, and H. C. Heller, unpublished observations). The dependence of Tb on diurnal rhythms in Ta has also been reported for European hamsters and marmots housed in a laboratory (Wollnik and Schmidt, 1995
The positive masking effects of Ta on Tb are temperature-dependent and may explain why circadian rhythms were not observed in many of the torpor bouts in control animals. In a different study of this species, circadian Tb rhythms during deep torpor were uniformly present in all ground squirrels housed at various Ta values between 10 and 27°C, but were only detectable in a minority of animals housed at 5°C (Grahn et al., 1992
2 to 7°C).
Several features of Tb-Ta relations during asynchronous torpor bouts suggest that Tb rhythms were endogenously generated and not driven by Ta. Tb rhythms free ran with periods >24 hr in LL, whereas Ta rhythms simultaneously oscillated with periods that were <24 hr. The time lag between Tb and Ta nadirs was also over 10 times greater for these bouts than for synchronous ones. In many cases, a rise in Tb was coincident with a decline in Ta. These phenomena are characteristic of two independently oscillating rhythms. In addition, SCNx animals never expressed Tb rhythms in the absence of Ta rhythms. In golden-mantled ground squirrels, circadian Tb rhythms evidently persist during deep torpor at Ta = 10°C. The periods of these rhythms, although more variable than euthermic Tb rhythms, are temperature-compensated (Grahn et al., 1994
European and Arctic ground squirrels undergo seasonal circadian arrhythmia under seminatural and field conditions, respectively (Wollnik and Schmidt, 1995
Timing of entry into and arousal from torpor in intact and SCNx animals was influenced by the LD cycle. Both groups of squirrels were more likely to enter torpor during the night and to arouse during the day. This is unlikely to be an artifact of extraneous noise and human disturbances during the daylight hours because the apparent rhythms were absent in animals housed in LL, although laboratory procedures were similar to those in place during the LD cycle. The similarities among control and SCNx squirrels suggests that the LD cycle may have exerted its effects through noncircadian (i.e., masking) mechanisms. Because hibernators enter torpor during slow-wave sleep (Heller et al., 1978
The effects of SCN ablation on individual components of hibernation may be unrelated to the attendant loss of circadian organization. Rate of entry into torpor, duration of torpor bouts, intervals between bouts, and duration of hibernation seasons (Ruby et al., 1996
FOOTNOTES Received Aug. 22, 2001; revised Oct. 19, 2001; accepted Oct. 22, 2001.
This work was supported by National Institutes of Health Grants HD-14595, HD-07471, NS30816, and AG-11084. We thank Tom Kang, Kimberly Pelz, Atul Saran, and Christiana Tuthill for their excellent technical assistance.
Correspondence should be addressed to Norman F. Ruby, Department of Biological Sciences, Stanford University, Stanford, CA 94305-5020. E-mail: ruby{at}stanford.edu.
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