Circadian activity precedes daily methamphetamine injections in the rat

doi:10.1016/S0304-3940(98)00439-X

Neuroscience Letters

Volume 250, Issue 2, 19 June 1998, Pages 99-102

https://doi.org/10.1016/S0304-3940(98)00439-X Get rights and content

Abstract

Scheduled daily injections of methamphetamine (MA) produced locomotor activity that preceded and followed the usual time of injection in rats housed under conditions of constant, moderately dim light and temporally distributed feeding. A circadian basis for pre-injection time activity was supported by its anticipatory timing in the apparent absence of reliable preceding external cues and by its persistence on a test day on which the rats remained undisturbed. Post-injection time locomotor activity also persisted on the test day, occurring from 24 to 29 h after the final MA injection. These results indicate that MA injections engage circadian processes underlying locomotor activity, and they raise the possibility that intake of drugs of abuse by humans may facilitate drug taking or relapse at times of day related to previous drug use.

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Acknowledgements

This work was supported by grants from NIDA (DA11092 and DA02451) and NIMH (37892).

References (14)

J.R. Blackburn et al.
Increased dopamine metabolism in the nucleus accumbens and striatum following consumption of a nutritive meal but not a palatable non-nutritive saccharin solution
Pharmacol. Biochem. Behav.
(1986)
Z. Boulos et al.
Food availability and daily biological rhythms
Neurosci. Biobehav. Rev.
(1980)
S. Honma et al.
Phase-dependent phase shift of methamphetamine-induced circadian rhythm by haloperidol in SCN-lesioned rats
Brain Res.
(1995)
K.I. Honma et al.
Activity rhythms in the circadian domain appear in suprachiasmatic nuclei lesioned rats given methamphetamine
Physiol. Behav.
(1987)
S. Honma et al.
Methamphetamine induced locomotor rhythm entrains to restricted daily feeding in SCN lesioned rats
Physiol. Behav.
(1989)
S. Honma et al.
Rhythms in behaviors, body temperature, and plasma corticosterone in SCN lesioned rats given methamphetamine
Physiol. Behav.
(1988)
R.E. Mistlberger et al.
Palatable daily meals entrain anticipatory activity in free feeding rats: dependence on meal size and nutrient content
Physiol. Behav.
(1987)

There are more references available in the full text version of this article.

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Circadian activity precedes daily methamphetamine injections in the rat

Abstract

Section snippets

Acknowledgements

Pharmacol. Biochem. Behav.

Neurosci. Biobehav. Rev.

Brain Res.

Physiol. Behav.

Physiol. Behav.

Physiol. Behav.

Physiol. Behav.