Dual regulation of clock gene Per2 expression in discrete brain areas by the circadian pacemaker and methamphetamine‐induced oscillator in rats
Abstract
Behavioral rhythms induced by methamphetamine (MAP) treatment in rats are independent of the circadian pacemaker in the suprachiasmatic nucleus (SCN). To know the site and mechanism of an underlying oscillation (MAP-induced oscillator; MAO), extra-SCN circadian rhythms in the discrete brain areas were examined in rats with and without the SCN. To fix the phase of MAO, MAP was supplied in drinking water at a restricted time of day for 14 days (R-MAP) and subsequently given ad libitum (ad-MAP). Plain water was given to the controls at the same restricted time (R-Water). Clock gene Per2 expression was measured by a bioluminescence reporter in cultured brain tissues. In SCN-intact rats, MAO was induced by R-MAP and behavioral rhythms were phase-delayed from the restricted time under ad-MAP with relative coordination. Circadian Per2 rhythms in R-MAP rats were not affected in the SCN but were slightly phase-advanced in the olfactory bulb (OB), caudate-putamen (CPU) and substantia nigra (SN) as compared with R-Water rats. Following SCN lesion, R-MAP-induced MAO phase-shifted more slowly and did not show a sign of relative coordination. In these rats, circadian Per2 rhythms were significantly phase-shifted in the OB and SN as compared with SCN-intact rats. These findings indicate that MAO was induced by MAP given at a restricted time of day in association with phase-shifts of the extra-SCN circadian oscillators in the brain dopaminergic areas. The findings also suggest that these extra-SCN oscillators are the components of MAO and receive dual regulation by MAO and the SCN circadian pacemaker.
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Clock genes exhibit periodic variations in striatal structures and could be related to rhythms in the expression of dopamine-related genes.
“Clock genes also exhibit periodic variations in striatal structures (Bussi et al., 2014, Li et al., 2009, Natsubori et al., 2014), and could be related to rhythms in the expression of dopamine-related genes (Shumay et al., 2012).”
From Circadian dysregulation in Parkinson's disease (2017) · cites this paper as Natsubori et al., 2014
Cites
Coordination of circadian timing in mammals
Reppert, S. M., & Weaver, D. R. (2002) · Nature · doi:10.1038/nature00965 · Cited by 4,379 · see citing works
Central and Peripheral Circadian Clocks in Mammals
Mohawk, J. A., Green, C. B., & Takahashi, J. S. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153128 · Cited by 2,265 · see citing works
Circadian rhythms in isolated brain regions
Abe, M., Herzog, E. D., Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M., & Block, G. D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00350.2002 · Cited by 681 · see citing works
Anticipation of 24-hr feeding schedules in rats with lesions of the suprachiasmatic nucleus
Stephan, F. K., Swann, J. M., & Sisk, C. L. (1979) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(79)90415-1 · Cited by 310 · see citing works
Masubuchi, S., Honma, S., Abe, H., Ishizaki, K., Namihira, M., Ikeda, M., & Honma, K. (2000) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2000.01313.x · Cited by 177 · see citing works
Self-citationIndependent Circadian Oscillations ofPeriod1in Specific Brain AreasIn VivoandIn Vitro
Abraham, U., Prior, J. L., Granados‐Fuentes, D., Piwnica-Worms, D. R., & Herzog, E. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2225-05.2005 · Cited by 124 · see citing works
The Methamphetamine-Sensitive Circadian Oscillator (MASCO) in Mice
Tataroğlu, Ö., Davidson, A. J., Benvenuto, L. J., & Menaker, M. (2006) · Journal of Biological Rhythms · doi:10.1177/0748730406287529 · Cited by 109 · see citing works
Influence of Water Deprivation on Adrenocortical Rhythms
Johnson, J. T., & Levine, S. Z. (2008) · Neuroendocrinology · doi:10.1159/000122139 · Cited by 100 · see citing works
The SCN‐independent clocks, methamphetamine and food restriction
Honma, K., & Honma, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06976.x · Cited by 94 · see citing works
Self-citationDisorganization of the rat activity rhythm by chronic treatment with methamphetamine
Honma, K., Honma, S., & Hiroshige, T. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90265-9 · Cited by 93 · see citing works
Self-citationYamanaka, Y., Honma, S., & Honma, K.-I. (2008) · Genes to Cells · doi:10.1111/j.1365-2443.2008.01183.x · Cited by 82 · see citing works
Self-citationRoles of paraventricular catecholamines in feeding-associated corticosterone rhythm in rats
Honma, K., Noe, Y., Honma, S., Katsuno, Y., & Hiroshige, T. (1992) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1992.262.6.e948 · Cited by 51 · see citing works
Self-citationHonma, S., & Honma, K.-I. (1995) · Brain Research · doi:10.1016/0006-8993(95)00027-n · Cited by 30 · see citing works
Self-citationMistlberger, R. E., & Rechtschaffen, A. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90070-8 · Cited by 28 · see citing works
Natsubori, A., Honma, K., & Honma, S. (2012) · European Journal of Neuroscience · doi:10.1111/ejn.12034 · Cited by 22 · see citing works
Self-citationHonma, K., Honma, S., Hirai, T., Katsuno, Y., & Hiroshige, T. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90186-1 · Cited by 22 · see citing works
Self-citationYoshihara, T., Honma, S., Mitome, M., & Honma, K. (1996) · Brain Research · doi:10.1016/0006-8993(95)01343-1 · Cited by 20 · see citing works
Self-citationNatsubori, A., Honma, K., & Honma, S. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12265 · Cited by 19 · see citing works
Self-citationYoshihara, T., Honma, S., Mitome, M., & Honma, K.-I. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)13353-5 · Cited by 18 · see citing works
Self-citationWater as entrainer of circadian running activity in rat
Dhume, R. A., & Mg, G. (1982) · Physiology & Behavior · doi:10.1016/0031-9384(82)90136-6 · Cited by 12 · see citing works
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Honma, S. (2018) · The Journal of Physiological Sciences · doi:10.1007/s12576-018-0597-5 · Cited by 233 · see citing works
Self-citationRegulation and function of extra‐SCN circadian oscillators in the brain
Begemann, K., Neumann, A., & Oster, H. (2020) · Acta Physiologica · doi:10.1111/apha.13446 · Cited by 102 · see citing works
Gallardo, C. M., Darvas, M., Oviatt, M., Chang, C. H., Michalik, M. J., Huddy, T. F., Meyer, E. E., Shuster, S. A., Aguayo, A., Hill, E. M., et al. (2014) · eLife · doi:10.7554/elife.03781 · Cited by 98 · see citing works
Circadian regulation of membrane physiology in neural oscillators throughout the brain
Paul, J. R., Davis, J. A., Goode, L. K., Becker, B., Fusilier, A. R., Meador-Woodruff, A., & Gamble, K. L. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14343 · Cited by 80 · see citing works
Circadian dysregulation in Parkinson's disease
Videnovic, A., & Golombek, D. (2017) · Neurobiology of Sleep and Circadian Rhythms · doi:10.1016/j.nbscr.2016.11.001 · Cited by 63 · see citing works
Involvement of dopamine signaling in the circadian modulation of interval timing
Bussi, I. L., Levín, G., Golombek, D. A., & Agostino, P. V. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12569 · Cited by 62 · see citing works
Yamanaka, Y., Hashimoto, S., Masubuchi, S., Natsubori, A., Nishide, S., Honma, S., & Honma, K. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00087.2014 · Cited by 62 · see citing works
Self-citationVerwey, M., Dhir, S. K., & Amir, S. (2016) · F1000Research · doi:10.12688/f1000research.9180.1 · Cited by 62 · see citing works
Racing the clock: The role of circadian rhythmicity in addiction across the lifespan
Gulick, D., & Gamsby, J. J. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.03.003 · Cited by 50 · see citing works
Becker‐Krail, D. D., Walker, W. H., & Nelson, R. J. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.886704 · Cited by 45 · see citing works
The role of circadian rhythm in choroid plexus functions
Quintela, T., Furtado, A., Duarte, A. C., Gonçalves, I., Myung, J., & Santos, C. R. A. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102129 · Cited by 43 · see citing works
Basic concepts and unique features of human circadian rhythms: implications for human health
Yamanaka, Y. (2020) · Nutrition Reviews · doi:10.1093/nutrit/nuaa072 · Cited by 32 · see citing works
Chronobiology of Parkinson's disease: Past, present and future
Asadpoordezaki, Z., Coogan, A. N., & Henley, B. M. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15859 · Cited by 31 · see citing works
Dopamine systems and biological rhythms: Let’s get a move on
Tang, Q., Assali, D. R., Güler, A. D., & Steele, A. D. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.957193 · Cited by 25 · see citing works
Ono, D., Honma, S., & Honma, K. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13111 · Cited by 23 · see citing works
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Pradel, K., Drwiȩga, G., Chrobok, Ł., & Błasiak, T. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.932378 · Cited by 15 · see citing works
Social defeat stress affects resident’s clock gene and bdnf expression in the brain
Moravcová, S., Červená, K., Míková, H., Pačesová, D., Pallag, G., Novotný, J., & Bendová, Z. (2020) · Stress · doi:10.1080/10253890.2020.1759548 · Cited by 12 · see citing works
The circadian neurobiology of reward
Olejniczak, I., Begemann, K., Wilhelm, I., & Oster, H. (2023) · Acta Physiologica · doi:10.1111/apha.13928 · Cited by 11 · see citing works
Sleep Disturbance in Tourette’s Disorder: Potential Underlying Mechanisms
Ricketts, E. J., Swisher, V. S., Greene, D. J., Silverman, D. H. S., Nofzinger, E. A., & Colwell, C. S. (2023) · Current Sleep Medicine Reports · doi:10.1007/s40675-022-00242-5 · Cited by 10 · see citing works
Maternal morphine intake during pregnancy and lactation affects the circadian clock of rat pups
Pačesová, D., Spišská, V., Novotný, J., & Bendová, Z. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.09.016 · Cited by 10 · see citing works
A Complex Relationship Among the Circadian Rhythm, Reward Circuit and Substance Use Disorder (SUD)
Samanta, S., Bagchi, D., Gold, M. S., Badgaiyan, R. D., Barh, D., & Blum, K. (2024) · Psychology Research and Behavior Management · doi:10.2147/prbm.s473310 · Cited by 9 · see citing works
Yamanaka, Y., Honma, S., & Honma, K. (2018) · Journal of Biological Rhythms · doi:10.1177/0748730418796300 · Cited by 8 · see citing works
Self-citationNishide, S., Suzuki, Y., Ono, D., Honma, S., & Honma, K. (2021) · Journal of Biological Rhythms · doi:10.1177/07487304211047937 · Cited by 7 · see citing works
Self-citationSeeing the forest and trees: whole‐body and whole‐brain imaging for circadian biology
Ode, K. L., & Ueda, H. R. (2015) · Diabetes Obesity and Metabolism · doi:10.1111/dom.12511 · Cited by 6 · see citing works
Taufique, S. K. T., Ehichioya, D. E., Pendergast, J. S., & Yamazaki, S. (2022) · F1000Research · doi:10.12688/f1000research.125432.1 · Cited by 6 · see citing works
Pačesová, D., Spišská, V., Novotný, J., & Bendová, Z. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25236 · Cited by 6 · see citing works
Spišská, V., Pačesová, D., Míková, H., Pohanová, P., Telenský, P., Novotný, J., & Bendová, Z. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146952 · Cited by 5 · see citing works
Swaroop, A., Paul, J. R., McMeekin, L. J., Barnett, A. M., Colafrancesco, A. M., Russell, D. L., Smith, C. M., Simmons, M. S., Volpicelli‐Daley, L. A., Cowell, R. M., et al. (2025) · npj Biological Timing and Sleep · doi:10.1038/s44323-025-00044-2 · Cited by 3 · see citing works
Chronobiology: Human circadian pacemaker and circadian rhythms
Yamanaka, Y. (2020) · 体力科學 · doi:10.7600/jspfsm.69.343 · Cited by 2 · see citing works
Yoshikawa, T., Honma, K., Shigeyoshi, Y., Yamagata, Y., & Honma, S. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16316 · Cited by 2 · see citing works
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Liu, P., Li, H., Zhu, Y., Song, S., Kang, L., & Hu, Y. (2026) · Journal of Integrative Neuroscience · doi:10.31083/jin48501 · Cited by 1 · see citing works
The Impact of Methylphenidate on Circadian Rhythms and Clock Gene Expression
Coogan, A. N., Thome, J., & Baird, A. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800634-4.00066-4
Aldekeeva, A. S., Reznik, S. Y., Kraynova, Y. S., & Klyueva, N. Z. (2021) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-021-01065-7
Sato, R., Kanai, M., Yoshida, Y., Fukushima, S., Nogami, M., Yamaguchi, T., Iijima, N., Sutherland, K. L., Haga, S., Ozaki, M., et al. (2023) · Cells · doi:10.3390/cells12040654
Honma, S. (2024) · Royal Society of Chemistry eBooks · doi:10.1039/bk9781839167553-00107
Self-citationCircadian Clocks in Mammals: General Aspects of Oscillating Systems and Roles in Medicine
Honma, K. (2024) · Royal Society of Chemistry eBooks · doi:10.1039/bk9781839167553-00013
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- Authors
- Natsubori, A., Honma, K., & Honma, S.
- Affiliations
- Hokkaido University (JP)
- Corresponding author
- Honma, Ken‐ichi
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2013-10-25
- Volume
- 39
- Issue
- 2
- Pages
- 229-240
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2077280656
- Cited by
- 36
- References
- 20
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 4 · 2023: 4 · 2022: 5 · 2021: 4 · 2020: 5 · 2019: 1 · 2018: 3 · 2016: 3 · 2015: 2 · 2014: 3
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- methamphetamine, circadian pacemaker, suprachiasmatic nucleus, clock genes, olfactory bulb, substantia nigra, caudate-putamen, phase shift, feed restriction, behavioral rhythms, dual regulation
- MeSH terms
- Animals, Brain, Circadian Rhythm, Drinking, Eating, Gene Expression Regulation, Locomotion, Methamphetamine, Suprachiasmatic Nucleus, Time Factors, Wakefulness, Dopamine Agents, Rats, Wistar, Rats, Period Circadian Proteins, Circadian Clocks, In Vitro Techniques
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