PII S0031-9384(97)00202-3
Phase Response Curves to Ambient Temperature
Pulses in Rats
ANDREW J. P. FRANCIS*
1
AND GRAHAME J. COLEMAN²
*Department of Psychology and IDS, Faculty of Applied Science, Royal Melbourne Institute of Technology,
Bundoora, VIC 3083, Australia and ²Department of Psychology, Faculty of Science,
Monash University, Caulfield, VIC 3145, Australia
Received 18 December 1996; Accepted 1 April 1997
FRANCIS, A. J. P. AND G. J. COLEMAN. Phase response curves to ambient temperature pulses in rats. PHYSIOL BEHAV 62(6)
1211–1217, 1997.—The effect of pulses of warm ambient temperature on the phase of activity onset in Long–Evans hooded rats, Rattus
norvegicus, free-running in constant light was examined. In two experiments, rats were exposed to pulses reaching a maximum of 34°C
or 32°C. Phase response curves were obtained with advances occurring mainly in the subjective day, and delays mainly, but not
entirely, in the subjective night. Significant negative correlations between rhythm period and phase-shifts were found. There were no
consistent relationships between changes in activity levels due to the temperature pulses and phase-shifts. Cycles of higher and lower
ambient temperature may entrain circadian activity rhythms in mammals by daily advance or delay phase-shifts. © 1997 Elsevier
Science Inc.
Rattus norvegicus Circadian rhythms Ambient temperature Phase-response curve
PROBABLY because of its reliability and precision, the alterna-
tion of light and darkness (LD) has become the primary and most
potent zeitgeber (‘time-giver’) entraining biological rhythms, there
being no circadian rhythm unresponsive to light (6). Exposure of
an animal free-running in constant darkness (DD) or dim constant
light (LL) to bright light pulses results in phase-shifts of the
rhythm—the magnitude and direction (advance or delay) of these
phase-shifts often being dependent upon the circadian time (CT) at
which the stimulus is presented, resulting in a phase-response
curve (PRC). PRCs for photic stimuli have been obtained for many
mammalian species including Glaucomys volans, Dipodomys
merriami, Mesocricetus auratus, Peromyscus leucopus, Mus
musculus, Peromyscus maniculatus and Dasyuroides byrnei (8–
10,23,30), and daily advance or delay phase-shifts produced by
discrete light exposure are thought to be the main functional
mechanism by which LD cycles entrain circadian rhythms (31,32).
Another significant geophysical cycle is the daily alternation of
warmer and cooler ambient temperatures, and the effectiveness of
cycles of higher and lower ambient temperature (TaHLs) for the
entrainment of circadian rhythms in poikilothermic and heterother-
mic species is well established (16,41,42). TaHLs have also been
shown to entrain the circadian rhythms of a variety of homeother-
mic species (as reviewed below), although (a) entrainment rates
are usually lower than where light is the zeitgeber, (b) there is a
degree of variability in the entrained phase-relation to TaHLs not
generally seen to LD cycles and, (c) the functional and physiolog-
ical mechanisms mediating entrainment to TaHLs are unknown.
To review the literature briefly, activity rhythms of both diurnal
and nocturnal species have been shown to entrain to TaHLs.
Activity rhythms of diurnal house sparrows, Passer domesticus,
free-running in constant dark (DD) entrained to a 12:12 TaHL
regime (38°C:6°C); some birds restricting activity to the cool
fraction, while others restricted activity mainly to the warm frac-
tion of the TaHLs (17). In a total of 14 tests on 7 diurnal pig-tailed
macaques, Macaca nemistrina, four cases of clear entrainment to
a 12:12 TaHL regime (32°C:17°C) under constant light (LL) were
observed, with activity restricted mainly to the warm fraction of
the TaHLs (40). The entrained animals were females, and those not
entrained were males (personal communication). In a total of 20
tests on 8 diurnal squirrel monkeys, Saimiri sciureus, free-running
in LL, 7 instances of entrainment to the 12:12 TaHLs (32°C:16°C)
were obtained from 3 monkeys (with activity restricted to the cool
fraction; 3). In nocturnal Long–Evans hooded rats, Rattus norve-
gicus, free-running in DD and exposed to a 12:12 TaHL regime
(34°C:21°C), three of 12 male rats and one of 12 female rats
entrained—restricting drinking and locomotor activity mainly to
the cool part of the TaHLs (19). Similarly, in nocturnal marsupial
Stripe-faced Dunnarts, Sminthopsis macroura, 2 of 6 animals
entrained to 12:12 TaHLs (35°C:21°C) under DD and 3 of 12
animals entrained under LL (all with activity mainly in the cool
fraction of the TaHLs; 20).
So far as the functional mechanisms mediating entrainment to
TaHLs is concerned, studies examining the discrete phase-shifting
effect of ambient temperature on mammalian circadian systems are
scant, and there is a lack of recent research in the area. In two
house sparrows it was reported that step-wise entry into a lower
1
To whom correspondence should be addressed.
Physiology & Behavior, Vol. 62, No. 6, pp. 1211–1217, 1997
© 1997 Elsevier Science Inc. All rights reserved.
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