Entrainment of methamphetamine-induced locomotor activity rhythm to feeding cycles in SCN-lesioned rats

Honma, Sato; Kanematsu, Nobue; Honma, Ken‐ichi

doi:10.1016/0031-9384(92)90360-e

Cited by 23 publications

(15 citation statements)

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“…Previous studies have suggested that the MASCO and FEO may be the same circadian oscillator (2,4,(22)(23)(24). The current study provides additional evidence supporting this hypothesis.…”

Section: Discussionsupporting

confidence: 84%

Perioddetermination in the food-entrainable and methamphetamine-sensitive circadian oscillator(s)

Pendergast

Oda

Niswender

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Daily rhythmic processes are coordinated by circadian clocks, which are present in numerous central and peripheral tissues. In mammals, two circadian clocks, the food-entrainable oscillator (FEO) and methamphetamine-sensitive circadian oscillator (MASCO), are "black box" mysteries because their anatomical loci are unknown and their outputs are not expressed under normal physiological conditions. In the current study, the investigation of the timekeeping mechanisms of the FEO and MASCO in mice with disruption of all three paralogs of the canonical clock gene, Period, revealed unique and convergent findings. We found that both the MASCO and FEO in Per1 −/− /Per2 −/− /Per3 −/− mice are circadian oscillators with unusually short (∼21 h) periods. These data demonstrate that the canonical Period genes are involved in period determination in the FEO and MASCO, and computational modeling supports the hypothesis that the FEO and MASCO use the same timekeeping mechanism or are the same circadian oscillator. Finally, these studies identify Per1 −/− /Per2 −/− /Per3 −/− mice as a unique tool critical to the search for the elusive anatomical location(s) of the FEO and MASCO. food anticipatory activity | restricted feeding | suprachiasmatic nuclei | knockout | C57BL/6J

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“…Previous studies have suggested that the MASCO and FEO may be the same circadian oscillator (2,4,(22)(23)(24). The current study provides additional evidence supporting this hypothesis.…”

Section: Discussionsupporting

confidence: 84%

Perioddetermination in the food-entrainable and methamphetamine-sensitive circadian oscillator(s)

Pendergast

Oda

Niswender

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…These signals might include hormonal and metabolic changes related to feeding (7,23) or feedback from the arousal or behavior systems (10,14,25). The catecholaminergic system is one of the candidates for mediating the input signal of feeding time (15). The signal associated with RF might be a change in the metabolic system or the arousal state, which in turn changes the clock gene expressions in the brain areas outside the SCN or in the peripheral tissues and reorganizes the oscillators outside the SCN and affects the SCN circadian pacemaker to entrain.…”

Section: Discussionmentioning

confidence: 99%

Daily restricted feeding resets the circadian clock in the suprachiasmatic nucleus of CS mice

Abe

Honma

2007

American Journal of Physiology-Regulatory, Integrative and Comp

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Abe H, Honma S, Honma K-i. Daily restricted feeding resets the circadian clock in the suprachiasmatic nucleus of CS mice. Am J Physiol Regul Integr Comp Physiol 292: R607-R615, 2007. First published September 21, 2006; doi:10.1152/ajpregu.00331.2006.-Circadian rhythms in clock gene expressions in the suprachiasmatic nucleus (SCN) of CS mice and C57BL/6J mice were measured under a daily restricted feeding (RF) schedule in continuous darkness (DD), and entrainment of the SCN circadian pacemaker to RF was examined. After 2-3 wk under a light-dark cycle with free access to food, animals were released into DD and fed for 3 h at a fixed time of day for 3-4 wk. Subsequently, they returned to having free access to food for 2-3 wk. In CS mice, wheel-running rhythms entrained to RF with a stable phase relationship between the activity onset and feeding time, and the rhythms started to free run from the feeding time after the termination of RF. mPer1, mPer2, and mBMAL1 mRNA rhythms in the SCN showed a fixed phase relationship with feeding time, indicating that the circadian pacemaker in the SCN entrained to RF. On the other hand, in C57BL/6J mice, wheel-running rhythms free ran under RF, and clock gene expression rhythms in the SCN showed a stable phase relation not to feeding time but to the behavioral rhythms, indicating that the circadian pacemaker in the SCN did not entrain. These results indicate that the SCN circadian pacemaker of CS mice is entrainable to RF under DD and suggest that CS mice have a circadian clock system that can be reset by a signal associated with feeding time.biological rhythm; food entrainment; clock gene; behavior; brain CIRCADIAN RHYTHMS UNDER A RESTRICTED feeding (RF) schedule, in which the food available time is restricted for several hours in a day, have been well studied in rats and mice (for a review, see Refs. 24 and 31). RF induces prefeeding increases in locomotor activity and adrenal corticosterone secretion 2-3 h prior to the feeding time (food-anticipatory activity). The food-anticipatory activity has been suggested to be regulated by the circadian clock because the food-anticipatory activity appears only under RF in which the feeding interval is near 24 h (circadian range). However, RF had no entraining (synchronizing) effect on oscillation components of activity rhythm driven by the circadian pacemaker located in the hypothalamic suprachiasmatic nucleus (SCN). The food-anticipatory activity was not affected by SCN bilateral lesions, which disrupted the free-running component of circadian behavioral rhythms (29,30). Moreover, the circadian expression rhythms of clock genes, such as mPer1 and mPer2 in the SCN were unchanged by RF (8,13,32,34). These findings suggested that RF cannot reset the SCN central pacemaker, and food-anticipatory activity is regulated by another oscillator(s) that entrains to the RF (food-entrainable oscillator) located outside the SCN.On the other hand, one recent study reported that the SCNdriven behavioral rhythm and mPER2 protein rhythm in the SCN of sev...

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“…Threefourths of rats held in a 12/12 light/dark (LD) cycle and given chronic MAP show a second rhythmic component of locomotor behavior, the period length of which is longer than 24 h and which exhibits relative coordination with the main component which is entrained to the LD cycle (Honma, Honma et al 1986). In addition, MAP induces robust activity rhythms in SCN-lesioned (SCNX) arrhythmic rats that occasionally persists for several cycles after withdrawal of MAP (Honma, Honma et al 1987;Honma, Honma et al 1988;Honma, Kanematsu et al 1992). Similar rhythms can also be induced in SCNX rats when MAP is administered via osmotic pumps instead of drinking water (Honma, Honma et al 1987).…”

Section: Effects Of Map On Circadian Behavior (And Other) Rhythmsmentioning

confidence: 98%

“…suggests that MASCO and FEO may share components or even be the same clock (Hiroshige, Honma et al 1991;Honma, Kanematsu et al 1992). FEO was suggested to be localized in the nervous system and if this is true then MASCO (or at least its entraining pathways) might also be in the brain.…”

Section: Localization Of Mascomentioning

confidence: 99%

“…Although there is presently no evidence either way, it has been suggested that the two rhythmic behaviors are driven by the same physical oscillator (Honma, Honma et al 1988;Honma, Honma et al 1989;Hiroshige, Honma et al 1991;Honma, Kanematsu et al 1992;Davidson, Tataroglu et al 2005). Because MAP is an addictive drug which acts primarily on dopaminergic cells in the brain, it is tempting to speculate that by exposing animals to chronic MAP we have somehow tapped into a connection between the circadian and the reward systems (for discussion see (Davidson, Tataroglu et al 2005).…”

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Effects of Methamphetamine on Circadian Rhythms of Mice

Tataroglu

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The circadian system allows an organism to anticipate rhythmic changes in the external conditions and thereby increases its fitness. In rodents, the circadian clock resides in a pair of nuclei called the suprachiasmatic nuclei (SCN) which regulates rhythms of locomotor behavior, body temperature and some other physiological variables. However, this hierarchical organization of the circadian system is challenged by the discovery of two SCN-independent major oscillators; a feeding-entrainable oscillator (FEO) and a methamphetamine-sensitive circadian oscillator (MASCO). The presence of SCN, FEO and MASCO suggests a central multi-oscillatory organization of the circadian system in rodents, similar to the organization found in non-mammal vertebrates. At present, we know very little about how this complex multi-oscillator system is integrated.Although there is substantial information available about the SCN, the molecular components, localization and natural role of MASCO in the body are unknown. In fact, it is still debated whether MASCO is a bona fide circadian oscillator rather than a simple hourglass mechanism. This is largely due to the lack of a robust circadian model to study the effects of methamphetamine (MAP) on circadian rhythms. This thesis aims to fill some of these gaps in our understanding of this fascinating major oscillator 3 Using mice, we successfully replicated the published effects of chronic MAP on the circadian rhythms of rats. In fact, the differences such as more robust and clear activity rhythms, more pronounced MAP-induced second components of the rhythm and obvious sex and strain differences make the mice a better model.The results also indicated that MASCO interacts with the SCN in a manner that is strain, sex and dose dependent. Our experiments testing the hourglass explanation showed that the effects of MAP can not be explained by such a mechanism. This suggests that MASCO has circadian properties and is indeed a bona fide circadian clock. We also tried to elucidate the similarities between the molecular components of SCN and MASCO using several circadian mutant mice that were available to us. Although, the results of these experiments are not adequate to propose a list of known circadian genes that are involved in MASCO function, they provide the background for future studies that will determine the differences between the molecular components of SCN and MASCO.Utilization of the mouse strains presented in this thesis will provide an easy to obtain standard model where MASCO can be studied using latest developments in genetics and molecular biology. Identification of the natural role of MASCO in the body and its interactions with other oscillators in the body is of both scientific and clinical significance and will greatly improve our understanding of the circadian system in mammals.4 Acknowledgements I would like to thank Dr.Menaker for his continuous support and outstanding mentoring. I owe whatever I accomplished during my time at UVA to him and could never repay my debt. I a...

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Entrainment of methamphetamine-induced locomotor activity rhythm to feeding cycles in SCN-lesioned rats

Cited by 23 publications

References 25 publications

Perioddetermination in the food-entrainable and methamphetamine-sensitive circadian oscillator(s)

Perioddetermination in the food-entrainable and methamphetamine-sensitive circadian oscillator(s)

Daily restricted feeding resets the circadian clock in the suprachiasmatic nucleus of CS mice

Effects of Methamphetamine on Circadian Rhythms of Mice

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