 |
 Previous Article | Next Article 
The Journal of Neuroscience, January 1, 1999, 19(1):328-333
A Nonphotic Stimulus Inverts the Diurnal-Nocturnal Phase
Preference in Octodon degus
Martien J. H.
Kas and
Dale M.
Edgar
Sleep and Circadian Neurobiology Laboratory, Sleep Research Center,
Department of Psychiatry and Behavioral Sciences, Stanford University
School of Medicine, Stanford, California 94305
 |
ABSTRACT |
Mechanisms differentiating diurnal from nocturnal species are
thought to be innate components of the circadian timekeeping system and
may be located downstream from the circadian pacemaker within the
suprachiasmatic nucleus (SCN) of the hypothalamus. In the present
study, we found that the dominant phase of behavioral activity and body
temperature (Tb) is susceptible to modification by a specific modality
of behavioral activity (wheel-running activity) in Octodon
degus, a mammal that exhibits multiple chronotypes. Seven
Octodon degus exhibited diurnal Tb and locomotor
activity (LMA) circadian rhythms while entrained to a 24 h light/dark
cycle (LD 12:12). When the diurnal animals were provided
unrestricted access to a running wheel, the overt daily rhythms in
these animals inverted to nocturnal. This nocturnal pattern was
sustained in constant darkness and returned to diurnal after removal of
the running wheel. Six additional animals exhibited nocturnal
chronotypes in LD 12:12 regardless of access to running wheels.
Wheel-running activity inverted the phase preference in the diurnal
animals without changing the 24 hr mean LMA or Tb levels. Because wheel running did not increase the amplitude of the pre-existing diurnal pattern, simple masking effects on LMA and Tb cannot explain the rhythm
inversion. The diurnal-nocturnal inversion occurred without reversing
crepuscular-timed episodes of activity, suggesting that diurnal or
nocturnal phase preference is controlled separately from the intrinsic
timing mechanisms within the SCN and can be dependent on behavioral or
environmental factors.
Key words:
Octodon degus; circadian rhythms; wheel
running; diurnal-nocturnal; nonphotic; body temperature; locomotor
activity
| |
INTRODUCTION |
The innate properties of the
circadian pacemaker in the suprachiasmatic nuclei (SCN) are necessary
and sufficient for the generation of mammalian circadian rhythms (Moore
and Eichler, 1972 ; Stephan and Zucker, 1972; Ralph et al., 1990), but
the mechanisms that determine the distinct temporal niches in diurnal,
nocturnal, and crepuscular species are not known. Similar neuronal and
metabolic activity patterns within the SCN of nocturnal and diurnal
species (Inouye and Kawamura, 1979; Schwartz et al., 1983; Sato and
Kawamura, 1984) and similar photic phase response characteristics in
many diurnal and nocturnal mammals (Johnson, 1990) suggest that the manifest temporal niche may be determined primarily by factors that are
downstream from the intrinsic pacemaker mechanism.
In some species, such as the Octodon degus, intraspecific
variation in chronotype is reported. This hystricomorph rodent has been
characterized as diurnal with major episodes of activity at dawn and
dusk (Fulk, 1976; Labyak et al., 1997), but diurnal, nocturnal, and
crepuscular chronotypes have been observed in the laboratory (Labyak et
al., 1997). The factors accounting for differences in chronotype are
not known, but expression of specific modalities of activity behavior
may be important. For example, unrestricted wheel-running activity
differentially elevates nocturnal activity and body temperature levels
in degus when they are entrained to a light/dark cycle (Kas
and Edgar, 1998), raising the possibility that wheel-running activity
influences the overall timing of behavioral activity and other
biological rhythms in this species.
Activity-dependent modifications in the expression of circadian rhythms
are currently thought to result from nonphotic zeitgeber effects on the
phase control system within the SCN, from passive effects that mask the
expression of the endogenous circadian rhythm independently from the
pacemaker itself, or from some combination thereof. For example,
vigorous activity systematically phase shifts circadian rhythms in
nocturnal rodents [hamsters (Reebs and Mrosovsky, 1989); rats
(Mistlberger, 1991)] and in humans (Van Reeth et al., 1994; Klerman et
al., 1998) and can entrain circadian rhythms in nocturnal mice (Edgar
and Dement, 1991). Wheel running can also influence entrainment by
attenuating photic phase shifts in nocturnal species (Ralph and
Mrosovsky, 1992), an effect thought to be mediated via serotonergic
projections from the raphe nuclei to the SCN (Morin and Blanchard,
1991; Rea et al., 1994; Bradbury et al., 1997). Finally, wheel running
can exert potent exogenous effects on physiological variables that mask
their underlying endogenous circadian oscillation. In mice, wheel
running potently increases the duration of wakefulness episodes during
the usual nocturnal activity phase but does not otherwise change the
fundamental nocturnal timing of the circadian system (Welsh et al.,
1988; Edgar et al., 1991a).
Whether these active and/or passive components of activity behavior
account for variation in chronotype or otherwise alter the manifest
phase preference in Octodon degus is unknown. To address
this question, we investigated the timing and overt expression of
behavioral activity and body temperature (Tb) circadian rhythms in degus housed with and without running wheels. We found
that wheel-running activity inverted circadian rhythms in diurnal
animals without altering entrainment of the underlying circadian pacemaker.
| |
MATERIALS AND METHODS |
Animals. Thirteen adult (age 10-15 months) male
Octodon degus were used in this study. The animals were
individually housed in Nalgene cages (46 cm long × 24 cm
wide × 20 cm deep) and maintained in a 24 hr light/dark cycle (LD
12:12; 4 W fluorescent bulbs; lights-on intensity, 30-35 lux). Food
and water were available ad libitum. Ambient temperature was
23 ± 1°C.
Animal surgery. Animals were sedated with diazepam (1.6 mg/kg, i.m.), anesthetized (2% isofluorane in medical grade oxygen), and surgically prepared with a miniature biotelemetry transmitter (Barrows, Palo Alto, CA) placed in the abdomen. This transmitter allowed continuous Tb and locomotor activity (LMA) recordings throughout the study. Prophylactic antibiotics were administered preoperatively (chloramphenicol; 30 mg/kg, s.c.) and postoperatively (gentamycin; 40 mg/ml, s.c.). Postoperative pain was managed with buprenorphine (0.03 mg/kg, s.c.). At least 3 weeks of recovery from surgery were permitted before initiation of data collection.
Protocol. Animals were individually isolated from
environmental cues in a ventilated, light-proof, and sound-attenuating
stainless steel recording chamber. Body temperature and LMA were
monitored continuously while animals were subjected to four different
experimental conditions implemented in succession. First, animals were
monitored for at least 15 consecutive days while entrained to LD
12:12 without access to a running wheel. Second, a beveled
running wheel (20 cm in diameter and 7 cm wide) was placed in each
cage, and data were collected for at least 15 additional days in LD
12:12. Third, the lighting schedule was switched from LD 12:12 to
constant darkness (DD; by disconnecting the power source to the
lights at the beginning of the subjective night), and free-running
circadian rhythms were monitored from animals with running wheels for
at least 15 d. Fourth, running wheels were removed from the cages
in DD, and data were collected for at least 15 d. In some animals,
the order of these protocols was altered to confirm the lack of
running-activity order effects on manifest circadian rhythms.
Data collection and analysis. Body temperature and LMA
biotelemetry signals were detected by a telemetry receiver (Data
Sciences, St. Paul, MN) beneath the cage. A microcomputer-based data
collection system (Edgar et al., 1991b) sampled LMA as discrete events
every 10 sec and Tb (°C) each minute. Mean waveforms for LMA and Tb were computed in hourly bins for each animal as described previously (Edgar et al., 1991a). Mean waveforms were based on 15 consecutive days
of data per animal. For each animal, the amount of LMA during the light
phase [the sum of LMA counts from zeitgeber time 0 (ZT0) to ZT12] was
expressed as a percentage of its total daily amount of LMA (the sum of
LMA counts from ZT0 to ZT24). Day-night differences and changes in
total daily behavioral activity levels between conditions (with and
without running wheels in LD 12:12) were accessed using a Student's
t test (SigmaStat 1.0; Jandel Scientific, San Rafael, CA).
The effects of wheel-running activity on the manifest phase of Tb in LD
12:12 and DD were examined using digital raster plots. The vertical
tick marks in the raster plots were plotted in a density proportional
to body temperature values exceeding a 72 hr running mean (72 hr mean
calculations moved stepwise in daily increments).
| |
RESULTS |
Wheel-running effects in LD 12:12
In LD 12:12, the group mean body temperature for the 13 animals
studied exhibited crepuscular circadian waveforms (Fig.
1A). Consistent with
previous observations in this species (Labyak et al., 1997), however,
there were distinct individual day-night differences in average Tb and
LMA rhythms. On the basis of the 24 hr distribution of LMA, the animals
could be objectively classified into two groups: animals with a diurnal
phase preference [>50% of the total LMA during the subjective day
(n = 7)] and animals with a nocturnal phase preference
[<50% of the total LMA during the subjective day (n = 6)]. The mean circadian waveforms for the Tb of animals with either
a diurnal (56 ± 2% of the total LMA during the subjective day)
or nocturnal (45 ± 1% of the total LMA during the subjective
day) phase preference are shown in Figure 1, B and
C, respectively.
View larger version (31K):
[in this window]
[in a new window]
|
Figure 1.
Mean Tb waveforms of animals without
(A-C) or with (D-F)
running wheels. On the basis of the individual day-night differences
in LMA, the population of animals (A) was
classified into two groups exhibiting either >50%
(B) or <50% (C) of total
LMA during the light phase [average percentages (± SEM of 1-4%) are
indicated in the upper right corner of each graph].
Light/dark horizontal bars indicate the
light/dark cycle.
|
|
During unrestricted access to a running wheel, all animals showed
nocturnal phase preference while entrained to a light/dark cycle.
Voluntary wheel-running activity resulted in a significant decrease of
LMA during the subjective day in all animals (Fig. 1D-F). In animals with a diurnal phase
preference (Fig. 1B), wheel-running activity inverted
the phase preference from day to night (from 56 ± 2 to 38 ± 3% of total LMA during the subjective day; p = 0.0002)
and significantly increased the mean absolute Tb at night (Fig.
1E; p = 0.03). Wheel-running activity
inverted the diurnal-nocturnal phase preference in these animals
without changing the overall behavioral activity levels [1792 ± 179 counts/24 hr (without running wheel) vs 1790 ± 258 counts/24 hr (with running wheel); p > 0.9] or the 24 hr mean Tb levels [36.8 ± 0.1°C (without running wheel) vs
36.9 ± 0.1°C (with running wheel)]. In animals that expressed <50% of the total LMA during the subjective day (Fig. 1C),
nocturnal phase preference was sustained during unrestricted access to
a running wheel (Fig. 1F). Also in these animals,
wheel-running activity did not affect the total daily levels of
behavioral activity [1837 ± 221 counts/24 hr (without running
wheel) vs 2136 ± 377 counts/24 hr (with running wheel);
p > 0.5]. Furthermore, the amount of LMA during the
subjective day decreased significantly from 45 ± 1 to 35 ± 4% (p = 0.01).
Entrained versus free-running
To test whether the wheel-running-related inversion of phase
preference depended on influences of the light/dark cycle, we also
studied Tb and LMA circadian rhythms in DD. Animals that exhibited diurnal preference without running wheels (in LD 12:12) showed no changes in phase preference when lighting was switched to DD.
The mean and above mean Tb levels were observed during the subjective
day in both LD 12:12 and DD (Fig.
2).
View larger version (62K):
[in this window]
[in a new window]
|
Figure 2.
A double raster plot of Tb data obtained from a
representative animal exhibiting a diurnal phase preference when housed
without a running wheel in its cage. In LD 12:12
(LD; days 1-27), an entrained, diurnal rhythm of
Tb was observed. In DD (days 28-73), the
animal exhibited a circadian rhythm that free-ran (period length = 23.80 hr) from the phase of previous entrainment to the light/dark
cycle. Vertical tick marks in the plot indicate when the
Tb was equal to or above the mean Tb (see Materials and Methods).
Light/dark horizontal bars on the
TIME OF DAY-axis indicate the light/dark cycle. Lights
were on from 08:00 to 20:00 (8 P.M.).
|
|
In LD 12:12, animals with running wheels in the cage showed nocturnal
phase preference for both Tb and LMA circadian rhythms. Mean and above
mean Tb levels were observed at night (Figs.
3, 4,
days 1-22). Removal of the running wheel (in LD 12:12)
inverted the phase preference from day to night within two circadian
cycles (Fig. 3, day 23); however, no reversal of the
crepuscular-timed episodes of activity [seen at circadian time 12 (CT12) and CT23] was observed. Reintroduction of a running
wheel (Fig. 3, day 65) switched the temporal domain of
activity back to nighttime (CT12-CT24), demonstrating that
wheel-running-dependent inversion of phase preference is a reversible
phenomenon. After release into DD the animals maintained the phase
preference that was previously nocturnal (in LD 12:12) (Figs. 3,
day 86, 4, day 23), demonstrating that this
preference was not attributable to darkness but to the circadian phase
of subjective night. Removal of the running wheel in constant darkness
(Figs. 3, day 107, 4, day 72) inverted the phase
preference, suggesting that the inversion of the temporal domain of
activity behavior was caused by wheel-running activity.
View larger version (75K):
[in this window]
[in a new window]
|
Figure 3.
The inversion of phase preference as a function of
wheel-running activity in Octodon degus. The timing of
mean and above mean Tb is indicated by vertical tick
marks (see Materials and Methods). In this representative
animal, wheel-running activity inverted the phase preference in both LD
12:12 and in DD.
|
|
View larger version (61K):
[in this window]
[in a new window]
|
Figure 4.
An example of another animal exhibiting
a phase preference inversion as a function of wheel-running activity.
For this animal the order of the wheel-locking protocol differed from
that shown in Figure 3. Note that at the end of the study this animal
is distinctly diurnal when entrained to LD 12:12 without a running
wheel, in contrast to the situation at the beginning of the study. Tb
is double plotted as vertical tick marks indicating mean
and above mean Tb values (left). Simultaneously recorded
wheel-running activity (vertical tick marks) is shown on
the right. Dotted lines indicate missing
data.
|
|
Crepuscular-timed activity
Although wheel-running activity inverted the temporal domain of
activity from day to night, the episodes of activity at dawn and dusk
remained entrained to LD 12:12. Wheel-running activity did not
reverse the crepuscular-timed episodes of activity within a circadian
cycle (Fig. 3, days 1-85). In DD, the endogenous period length of the dusk circadian component was initially shorter than the
dawn component, causing a small transient change in their phase
relationship. A stable phase relationship between the dawn and the dusk
circadian component was established 24 ± 2 d after the light
source was disconnected. Consistent with observations in LD 12:12, the
inversion of phase preference in DD occurred without reversing the
crepuscular-timed episodes of behavioral activity within a circadian
cycle (Figs. 3, 4).
| |
DISCUSSION |
This study showed that unrestricted wheel-running activity can
invert the diurnal Tb and LMA rhythms to nocturnal in
Octodon degus. Because the diurnal-nocturnal inversion was
observed in both a light/dark cycle and constant darkness, the effect
seems to be solely dependent on wheel-running activity. Comparable
inversions in behavioral timing have been observed previously as a
consequence of seasonal changes in photoperiod in salmon (Eriksson,
1973), "spontaneously" in the cotton rat (Johnston and Zucker,
1983), or as a function of wheel-running activity in voles that are
exposed to a light/dark cycle (Gerkema et al., 1990). To our knowledge, however, diurnal-nocturnal inversions as a function of volitional wheel-running activity have not been observed in constant darkness within a species. Wheel running inverted the Tb and LMA phase preference to nocturnal in 100% of the animals classified diurnal under baseline conditions (without running wheels in LD 12:12; n = 7). The other half of the population studied
exhibited a nocturnal phase preference under baseline conditions
(n = 6), and wheel running increased the amplitude of
the existing nocturnal Tb and LMA patterns.
The individual differences in the timing and expression of behavioral
activity and Tb observed in degus without access to a
running wheel are comparable with those previously reported for this
species (Labyak et al., 1997). On the basis of variables derived from
the behavioral activity and Tb rhythms, Labyak et al. (1997) classified
Octodon degus into three chronotypes: morning, intermediate
(crepuscular), and evening types. Morning and evening types also have
been observed in humans (Foret et al., 1982). Our data suggest that
wheel running may be a factor that contributes to variation in rhythm
chronotypes within this species. Furthermore, even though the diurnal
or nocturnal modality of a species is generally thought to be innate,
the present data suggest that environmental and/or behavioral factors
can dramatically alter the apparent modality of entrainment. Thus,
activity-dependent diurnal-nocturnal inversion raises critically
important issues regarding the criteria that define the circadian
phenotype of a species.
The diurnal-nocturnal inversion observed in this study cannot be
explained by simple masking effects of wheel-running activity on the Tb
and LMA rhythms. Masking effects are influences of environmental or
behavioral factors on the overt rhythm that are independent from the
process of entrainment (Aschoff et al., 1982). For example, in mice,
volitional wheel-running activity increases the amplitude of the
circadian sleep/wake rhythm by increasing the amounts of wakefulness
during the activity phase (Welsh et al., 1988; Edgar et al., 1991a). In
the present study, wheel-running activity inverted the diurnal dominant
phase of animals housed without running wheels rather than simply
increasing the amplitude of the existing overt diurnal pattern.
Therefore, classical masking effects of wheel running on Tb and LMA do
not account for the inversion of the existing overt diurnal pattern
observed in this study.
Wheel-running activity does not appear to invert the overt diurnal
patterns to nocturnal by changing the fundamental mechanisms of
circadian rhythm entrainment. Comparable with previous findings (Labyak
et al., 1997; Kas and Edgar, 1998), our findings show that
degus exhibited prominent crepuscular episodes of behavioral activity and Tb while entrained to a light/dark cycle. The crepuscular timing of behavioral activity is thought to reflect a circadian rhythm
generated by at least two oscillators that are coupled within the SCN
(Pittendrigh and Daan, 1976). When entrained to a light/dark cycle, one
oscillator synchronizes to dawn (morning oscillator), and the other
synchronizes to dusk (evening oscillator). Wheel running inverted the
temporal domain of LMA and Tb without reversing the crepuscular
episodes of behavioral activity within a circadian cycle. Furthermore,
inversion of the phase preference occurred almost instantaneously
(within two circadian cycles) without evidence of phase transients
(progressive changes in rhythm phase during the course of a phase
shift), after the presentation or removal of the running wheel.
Therefore, our data suggest that mechanisms determining the overt
diurnal or nocturnal rhythm in this species are separate from phase
control mechanisms within the circadian pacemaker.
The inversion of the overt rhythms may also be explained by circadian
inhibition of some but not all of the behaviors at particular times of
day. For example, in the present study, the circadian pacemaker
potentially could inhibit wheel-running activity during the subjective
day without inhibiting the expression of LMA during the subjective day
in animals housed without running wheels. Circadian inhibition of
wheel-running activity during the subjective day is evident in
nocturnal mice (Edgar et al., 1997) and hamsters (Vogelbaum and
Menaker, 1992). For example, when mice are subjected to a daily
schedule of voluntary wheel running (e.g., 2 hr/d, starting at a fixed
time every day), the wheel-running levels during the subjective day are
suppressed when compared with that during the subjective night. In
contrast to these reports, however, circadian inhibition of
wheel-running activity during the subjective day is not observed in
Octodon degus when given daily schedules of volitional wheel
running similar to those used in mice (Edgar et al., 1997;
M. J. H. Kas and D. M. Edgar, unpublished observations). On the basis of these observations and the evidence that diurnal wheel-running activity has been observed in degus (Labyak
and Lee, 1995), it seems unlikely that strict nocturnal circadian control of wheel-running activity in Octodon degus accounts
for the diurnal-nocturnal inversion observed in this study.
Because the diurnal-nocturnal inversion in Octodon degus is
independent from interactions with the light/dark cycle, from simple
masking effects of wheel running on the LMA and Tb rhythms, from
pacemaker phase control, or from circadian inhibition of wheel running
during the subjective day, the present study suggests that a nonphotic
stimulus can modulate mechanisms that determine the phase preference in
this species. On the basis of the present data, we hypothesize that
these mechanisms are located peripheral to the intrinsic timing system
within the circadian pacemaker (Fig.
5).
View larger version (10K):
[in this window]
[in a new window]
|
Figure 5.
Activity-dependent influences on the mammalian
circadian timekeeping system. The SCN generates
circadian rhythms, such as wheel-running activity, via effector
mechanisms. Wheel-running activity can influence photic transduction at
the circadian pacemaker (arrow 1), can directly
phase-shift the circadian pacemaker (arrow 2), and can
impose exogenous influences on the overt rhythm by action on effector
mechanisms (arrow 4). The present study suggests
that wheel-running activity can also influence the circadian
timekeeping system by inverting the phase preference (arrow
3) independent from the pathways noted above (arrows
1, 2, 4; see Discussion for
further explanation).
|
|
The biological advantages of the diurnal-nocturnal inversion of phase
preference observed in this species are not known; however, the rapid
change in phase preference (within two circadian cycles) suggests that
it may serve as an adaptation mechanism to sudden changes in the
species's natural environment. A field study reported that
Octodon degus has both diurnal and nocturnal predators
(Fulk, 1976). Although an inversion of the phase preference may
increase survival of a species in response to a change in the temporal aspects of predation (e.g., seasonal effects on predator activity), the
nature of the ecological changes in predator prevalence is not expected
to be as sudden as the observed phase preference inversion. In addition
to biotic factors (such as predator risk), abiotic factors (e.g., food
intake, ambient temperature) may influence the timing of behavioral
activity in a species. For example, wheel-running activity in
degus could be anticipatory to other motivated behaviors [e.g., food intake (Mistlberger, 1994)] that somehow influence the
manifest phase preference without altering the underlying circadian
timing of activity at dawn and dusk. Alternatively, behavioral
thermoregulation may contribute to activity-dependent phase preference.
For example, ambient temperature affects the spatial distribution of
degus in its natural environment, independent of predator
pressure (Lagos et al., 1995). At high ambient temperatures (warm
season, mean of 27.2 ± 1.5°C with a maximum of 39.3 ± 2.9°C), degus selects covered rather than open
microhabitats, indicating that this species compensates for external
heat exposure by choosing sheltered areas (e.g., under shrubs) (Lagos
et al., 1995). A laboratory study showed that this species selects
cooler ambient temperatures when Tb increases, suggesting that
behavioral thermoregulation may influence activity levels in this
species (Refinetti, 1996). In the present study, wheel-running activity
(in LD 12:12) occurred at a time of day that is normally associated
with cooler ambient temperatures, namely, the dark phase. This suggests
that the animals selected the dark phase to compensate for the heat
production during wheel running. However, our data provided evidence
that this was not a passive response to changes in ambient temperature. For example, the day-night fluctuations of ambient temperature (in LD
12:12) in the recording environment were minimal (± 1°C). In
addition, the nocturnal phase preference in animals with running wheels
was sustained in the absence of the light/dark cycle, showing that
degus selected to be active during the subjective night in situations in which the ambient temperature did not change over the
circadian day. Thus, degus may be preprogrammed to change the timing of behavioral activity to reduce the risk of hyperthermy via
a nonphotic feedback pathway that acts downstream from the intrinsic
timing mechanism within the circadian pacemaker.
| |
FOOTNOTES |
Received July 24, 1998; revised Oct. 2, 1998; accepted Oct. 9, 1998.
This research was supported by Air Force Office of Scientific Research
Program for Research Excellence and Transition Grant F49620-95-1-0388 and by National Institutes of Health Grants AG06490 and AG11084. We thank Dr. Barbara Tate and Dr. Theresa Lee for providing the animals; Humberto Garcia, Laura Alexandre, and Ronny Tjon
for technical assistance; and Prof. Dr. Serge Daan for his helpful
feedback and comments on this manuscript.
Correspondence should be addressed to Dr. Dale M. Edgar, Sleep Research
Center, Stanford University School of Medicine, 701 Welch Road, Suite
#2226, Palo Alto, CA 94304.
| |
REFERENCES |
-
Aschoff J,
Daan S,
Honma KI
(1982)
Zeitgebers, entrainment and masking: some unsettled questions.
In: Vertebrate circadian systems, structure and physiology (Aschoff J,
Daan S,
Groos GA,
eds), pp 13-24. Berlin: Springer.
-
Bradbury MJ,
Dement WC,
Edgar DM
(1997)
Serotonin-containing fibers in the suprachiasmatic hypothalamus attenuate light-induced phase delays in mice.
Brain Res
768:125-134[Web of Science][Medline].
-
Edgar DM,
Dement WC
(1991)
Regularly scheduled voluntary exercise synchronizes the mouse circadian clock.
Am J Physiol
261:R928-R933[Abstract/Free Full Text].
-
Edgar DM,
Kilduff TS,
Martin CE,
Dement WC
(1991a)
Influence of running wheel activity on free-running sleep/wake and drinking circadian rhythms in mice.
Physiol Behav
50:373-378[Medline].
-
Edgar DM,
Seidel WF,
Dement WC
(1991b)
Triazolam-induced sleep in the rat: influence of prior sleep, circadian time, and light/dark cycles.
Psychopharmacology (Berl)
105:374-380[Medline].
-
Edgar DM,
Reid M,
Dement WC
(1997)
Serotonergic afferents mediate activity-dependent entrainment of the mouse circadian clock.
Am J Physiol
273:R265-R269[Abstract/Free Full Text].
-
Eriksson LO
(1973)
Spring inversion of the diel rhythm of locomotor activity in young sea-going trout (Salmo trutta trutta L.) and Atlantic salmon (Salmo salar L.).
Aquilo Ser Zool
14:68-79.
-
Foret JO,
Benoit O,
Royant-Parola S
(1982)
Sleep schedules and peak times of oral temperature and alertness in morning and evening types.
Ergonomics
25:821-827[Medline].
-
Fulk GW
(1976)
Notes on the activity, reproduction, and social behavior of Octodon degus.
J Mammal
57:495-505.
-
Gerkema GP,
Groos GA,
Daan S
(1990)
Differential elimination of circadian and ultradian rhythmicity by hypothalamic lesions in the common vole, Microtus arvalis.
J Biol Rhythms
5:81-95[Abstract/Free Full Text].
-
Inouye ST,
Kawamura H
(1979)
Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus.
Proc Natl Acad Sci USA
76:5962-5966[Abstract/Free Full Text].
-
Johnson CH
(1990)
In: An atlas of phase response curves for circadian and circatidal rhythms. Nashville, TN: Vanderbilt University.
-
Johnston PG,
Zucker I
(1983)
Lability and diversity of circadian rhythms of cotton rats Sigmodon hispidus.
Am J Physiol
244:R338-R346.
-
Kas MJH,
Edgar DM
(1998)
Crepuscular rhythms of EEG sleep-wake in a hystricomorph rodent, Octodon degus.
J Biol Rhythms
13:9-17[Abstract/Free Full Text].
-
Klerman EB,
Rimmer DW,
Dijk D-J,
Kronauer RE,
Rizzo III JF,
Czeisler CA
(1998)
Nonphotic entrainment of the human circadian pacemaker.
Am J Physiol
274:R991-R996.
-
Labyak SE,
Lee TM
(1995)
Estrus- and steroid-induced changes in circadian rhythms in a diurnal rodent, Octodon degus.
Physiol Behav
58:573-585[Medline].
-
Labyak SE,
Lee TM,
Goel N
(1997)
Rhythm chronotypes in a diurnal rodent, Octodon degus.
Am J Physiol
273:R1058-R1066[Abstract/Free Full Text].
-
Lagos VO,
Bozinovic F,
Contreras LC
(1995)
Microhabitat use by a small diurnal rodent (Octodon degus) in a semiarid environment: thermoregulatory constraints or predation risk?
J Mammal
76:900-905.
-
Mistlberger RE
(1991)
Effects of daily schedules of forced activity on free-running rhythms in the rat.
J Biol Rhythms
6:71-80[Abstract/Free Full Text].
-
Mistlberger RE
(1994)
Circadian food-anticipatory activity: formal models and physiological mechanisms.
Neurosci Biobehav Rev
18:171-195[Web of Science][Medline].
-
Moore RY,
Eichler VB
(1972)
Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat.
Brain Res
42:201-206[Web of Science][Medline].
-
Morin LP,
Blanchard J
(1991)
Depletion of brain serotonin by 5,7-DHT modifies hamster circadian rhythm response to light.
Brain Res
566:173-185[Web of Science][Medline].
-
Pittendrigh CS,
Daan S
(1976)
A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure-a clock for all seasons.
J Comp Physiol [A]
106:333-355.
-
Ralph MR,
Mrosovsky N
(1992)
Behavioral inhibition of circadian responses to light.
J Biol Rhythms
7:353-359[Abstract/Free Full Text].
-
Ralph MR,
Foster RG,
Davis FC,
Menaker M
(1990)
Transplanted suprachiasmatic nucleus determines circadian period.
Science
247:975-978[Abstract/Free Full Text].
-
Rea MA,
Glass JD,
Colwell CS
(1994)
Serotonin modulates photic responses in the hamster suprachiasmatic nuclei.
J Neurosci
14:3635-3642[Abstract].
-
Reebs SG,
Mrosovsky N
(1989)
Effects of induced wheel running on the circadian activity rhythms of Syrian hamsters: entrainment and phase response curve.
J Biol Rhythms
4:39-48[Abstract/Free Full Text].
-
Refinetti R
(1996)
Rhythms of body temperature and temperature selection are out of phase in a diurnal rodent, Octodon degus.
Physiol Behav
60:959-961[Medline].
-
Sato T,
Kawamura H
(1984)
Circadian rhythms in multiple unit activity inside and outside the suprachiasmatic nucleus in the diurnal chipmunk Eutamias sibiricus.
Neurosci Res
1:45-52[Medline].
-
Schwartz WJ,
Reppert SM,
Eagan SM,
Moore-Ede MC
(1983)
In vivo metabolic activity of the suprachiasmatic nuclei: a comparative study.
Brain Res
274:184-187[Web of Science][Medline].
-
Stephan FK,
Zucker I
(1972)
Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions.
Proc Natl Acad Sci USA
69:1583-1586[Abstract/Free Full Text].
-
Van Reeth O,
Sturis J,
Byrne MM,
Blackman JD,
L'Hermite-Baleriaux M,
Leproult R,
Oliner C,
Refetoff S,
Turek FW,
Van Cauter E
(1994)
Nocturnal exercise phase delays circadian rhythms of melatonin and thyrotropin secretion in normal men.
Am J Physiol
266:E964-E974[Abstract/Free Full Text].
-
Vogelbaum MA,
Menaker M
(1992)
Temporal chimeras produced by hypothalamic transplants.
J Neurosci
12:3619-3627[Abstract].
-
Welsh D,
Richardson GS,
Dement WC
(1988)
Effect of running wheel availability on circadian patterns of sleep and wakefulness in mice.
Physiol Behav
43:771-777[Medline].
Copyright © 1999 Society for Neuroscience 0270-6474/99/191328-06$05.00/0
This article has been cited by other articles:
|
|
|
|
 
E. Challet
Minireview: Entrainment of the Suprachiasmatic Clockwork in Diurnal and Nocturnal Mammals
Endocrinology,
December 1, 2007;
148(12):
5648 - 5655.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
U. Redlin and N. Mrosovsky
Nocturnal Activity in a Diurnal Rodent (Arvicanthis Niloticus): The Importance of Masking
J Biol Rhythms,
February 1, 2004;
19(1):
58 - 67.
[Abstract]
[PDF]
|
|
|
|
|
|
|
J. F. Duffy and D.-J. Dijk
Getting Through to Circadian Oscillators: Why Use Constant Routines?
J Biol Rhythms,
February 1, 2002;
17(1):
4 - 13.
[Abstract]
[PDF]
|
|
|
|
|
|
|
E. Challet, B. Pitrosky, B. Sicard, A. Malan, and P. Pevet
Circadian Organization in a Diurnal Rodent, Arvicanthis ansorgei Thomas 1910: Chronotypes, Responses to Constant Lighting Conditions, and Photoperiodic Changes
J Biol Rhythms,
February 1, 2002;
17(1):
52 - 64.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M. J. H. Kas and D. M. Edgar
Scheduled Voluntary Wheel Running Activity Modulates Free-Running Circadian Body Temperature Rhythms in Octodon degus
J Biol Rhythms,
February 1, 2001;
16(1):
66 - 75.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R. E. Mistlberger and M. M. Holmes
Behavioral feedback regulation of circadian rhythm phase angle in light-dark entrained mice
Am J Physiol Regulatory Integrative Comp Physiol,
September 1, 2000;
279(3):
R813 - R821.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. H. Kas and D. M. Edgar
Photic phase response curve in Octodon degus: assessment as a function of activity phase preference
Am J Physiol Regulatory Integrative Comp Physiol,
May 1, 2000;
278(5):
R1385 - R1389.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Blanchong, T. L. McElhinny, M. M. Mahoney, and L. Smale
Nocturnal and Diurnal Rhythms in the Unstriped Nile Rat, Arvicanthis niloticus
J Biol Rhythms,
October 1, 1999;
14(5):
364 - 377.
[Abstract]
[PDF]
|
|
|
|
Top
Abstract
Introduction
