Regulation of dopaminergic transmission and cocaine reward by the Clock gene
Open accessAbstract
Although there are clear interactions between circadian rhythms and drug addiction, mechanisms for such interactions remain unknown. Here we establish a role for the Clock gene in regulating the brain's reward circuit. Mice lacking a functional Clock gene display an increase in cocaine reward and in the excitability of dopamine neurons in the midbrain ventral tegmental area, a key brain reward region. These phenotypes are associated with increased expression and phosphorylation of tyrosine hydroxylase (the rate-limiting enzyme in dopamine synthesis), as well as changes in several genes known to regulate dopamine activity in the ventral tegmental area. These findings demonstrate the involvement of a circadian-associated gene, Clock , in regulating dopamine function and cocaine reward.
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Circadian genes in brain regions outside the SCN contribute locally to the control of neuronal metabolism, neurotransmitter synthesis and activity, and disruption of these functions might contribute to brain disorders.
“circadian genes in other brain regions outside of this central pace-maker also contribute locally to the control of neuronal metabolism, neurotransmitter synthesis and activity, and the disruption of these functions might contribute to brain disorders264,304–315”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [308]
Clock mutants display increased dopaminergic cell firing and bursting in the VTA.
“it was verified that Clock mutants display increased dopaminergic cell firing and bursting in the VTA (McClung et al., 2005).”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as McClung et al., 2005
The manic-like profile of Clock mutant mice includes hyperactivity, lowered depression-like behavior, greater risk taking behavior, an increase in the preference for sucrose and cocaine, and an increase in goal-directed behavior resulting in intracranial self-stimulation.
“This includes hyperactivity, lowered depression-like behavior, greater risk taking behavior, an increase in the preference for sucrose and cocaine, and an increase in goal-directed behavior resulting in intracranial self-stimulation.”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as McClung et al., 2005
Mice with a mutation in the Clock gene have a behavioral profile that is strikingly similar to human mania.
“Mice with a mutation in the Clock gene have a behavioral profile that is strikingly similar to human mania (McClung et al., 2005; Roybal et al., 2007).”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as McClung et al., 2005
A microarray analysis identified a number of potential target genes of CLOCK in the VTA which are important regulators of dopaminergic activity.
“a microarray analysis identified a number of potential target genes of CLOCK in the VTA which are important regulators of dopaminergic activity (McClung et al., 2005).”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as McClung et al., 2005
Circadian gene mutants often demonstrate altered reward behavior, such as increased preference for alcohol or hypersensitization to cocaine.
“Furthermore, circadian gene mutants often demonstrate altered reward behavior, such as increased preference for alcohol or hypersensitization to cocaine (McClung et al., 2005; Spanagel et al., 2005).”
From Sleep and circadian contributions to adolescent alcohol use disorder (2015) · cites this paper as McClung et al., 2005
Circadian genes are expressed widely throughout the brain, notably in components of the mesocorticolimbic reward system such as the ventral tegmental area and striatum.
“Circadian genes are expressed widely throughout the brain, notably in components of the mesocorticolimbic reward system such as the ventral tegmental area (VTA) and striatum (e.g., Lynch, Girgenti, Breslin, Newton, & Taylor, 2008; McClung et al., 2005; Uz, Akhisaroglu, Ahmed, & Manev, 2003).”
From Sleep and circadian contributions to adolescent alcohol use disorder (2015) · cites this paper as McClung et al., 2005
Expression of circadian genes in the striatum may be important in controlling the hedonic state.
“which suggest that expression of these genes in the striatum may be important in controlling the hedonic state”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
Additional microarray studies have found expression changes in circadian genes in striatal regions with psychostimulants such as cocaine.
“Additional microarray studies have found expression changes in circadian genes in striatal regions with psychostimulants such as cocaine”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
Alterations in the midbrain dopaminergic system have been implicated in mania.
“alterations in the midbrain dopaminergic system have been implicated in mania”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
CLOCK mutant mice display reduced anxiety or increased risk taking behavior in several measures.
“reduced anxiety or increased risk taking behavior in several measures”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
CLOCK is expressed in the ventral tegmental area.
“CLOCK is expressed in the VTA”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
CLOCK mutant mice have an increase in dopamine cell firing and bursting in the ventral tegmental area.
“we found an increase in dopamine cell firing and bursting in the ventral tegmental area (VTA) (McClung et al., 2005; Nestler, 2005; Nestler and Carlezon, 2006).”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
CLOCK mutant mice display hyperactivity in response to novelty and over the light/dark cycle.
“Their behavioral profile includes hyperactivity in response to novelty and over the light/dark cycle”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
CLOCK appears to regulate a number of genes that are important in dopaminergic transmission.
“it appears to regulate a number of genes that are important in dopaminergic transmission (McClung et al., 2005).”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
CLOCK mutant mice display reduced depression-like behavior in the forced swim test and learned helplessness tests.
“reduced depression-like behavior in the forced swim test and learned helplessness tests”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
CLOCK mutant mice display an increase in the reward value of cocaine, sucrose and intracranial self-stimulation.
“an increase in the reward value of cocaine, sucrose and intracranial self-stimulation (McClung et al., 2005; Roybal et al, in press).”
From Circadian genes, rhythms and the biology of mood disorders (2007) · cites this paper as McClung et al., 2005
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Self-citationCLOCK is suggested to associate with comorbid alcohol use and depressive disorders
Sjoholm, L. K., Kovanen, L., Saarikoski, S. T., Schalling, M., & Lavebratt, C. (2010) · Journal of Circadian Rhythms · doi:10.1186/1740-3391-8-1 · Cited by 97 · see citing works
Lithium Ameliorates Nucleus Accumbens Phase-Signaling Dysfunction in a Genetic Mouse Model of Mania
Dzirasa, K., Coque, L., Sidor, M. M., Kumar, S., Dancy, E. A., Takahashi, J. S., McClung, C. A., & Nicolelis, M. A. L. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4289-10.2010 · Cited by 85 · see citing works
Self-citationMinutes, days and years: molecular interactions among different scales of biological timing
Golombek, D. A., Bussi, I. L., & Agostino, P. V. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0465 · Cited by 80 · see citing works
Cocaine self-administration behaviors in ClockΔ19 mice
Ozburn, A. R., Larson, E. B., Self, D. W., & McClung, C. A. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2704-2 · Cited by 85 · see citing works
Self-citationPER2 rs2304672 polymorphism moderates circadian-relevant reward circuitry activity in adolescents
Forbes, E. E., Dahl, R. E., Almeida, J. R. C., Ferrell, R. E., Nimgaonkar, V. L., Mansour, H., Sciarrillo, S. R., Holm, S. M., Rodriguez, E. E., & Phillips, M. L. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.012 · Cited by 83 · see citing works
Mice with reduced DAT levels recreate seasonal-induced switching between states in bipolar disorder
Young, J. W., Cope, Z. A., Romoli, B., Schrurs, E., Joosen, A., van Enkhuizen, J., Sharp, R. F., & Dulcis, D. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0031-y · Cited by 81 · see citing works
Ashkenazy, T., Einat, H., & Kronfeld-Schor, N. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009115 · Cited by 81 · see citing works
Loss of dopamine disrupts circadian rhythms in a mouse model of Parkinson's disease
Fifel, K., & Cooper, H. M. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.08.024 · Cited by 80 · see citing works
Investigating the mechanism(s) underlying switching between states in bipolar disorder
Young, J. W., & Dulcis, D. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.03.019 · Cited by 68 · see citing works
Association of PER2 genotype and stressful life events with alcohol drinking in young adults
Blomeyer, D., Buchmann, A. F., Lascorz, J., Zimmermann, U. S., Esser, G., Desrivieres, S., Schmidt, M. H., Banaschewski, T., Schumann, G., & Laucht, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059136 · Cited by 65 · see citing works
Arey, R. N., Enwright, J. F., Spencer, S. M., Falcon, E., Ozburn, A. R., Ghose, S., Tamminga, C., & McClung, C. A. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.12 · Cited by 62 · see citing works
Self-citationRole for the<i>Clock</i>Gene in Bipolar Disorder
McClung, C. A. (2007) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2007.72.031 · Cited by 57 · see citing works
Self-citationKrishnan, V., Graham, A., Mazei-Robison, M. S., Lagace, D. C., Kim, K.-S., Birnbaum, S., Eisch, A. J., Han, P.-L., Storm, D. R., Zachariou, V., et al. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.03.026 · Cited by 56 · see citing works
Self-citationLee, H.-J., Son, G.-H., & Geum, D. (2013) · Psychiatry Investigation · doi:10.4306/pi.2013.10.3.225 · Cited by 48 · see citing works
Logan, R. W., Parekh, P. K., Kaplan, G. N., Becker-Krail, D. D., Williams, W. P., Yamaguchi, S., Yoshino, J., Shelton, M. A., Zhu, X., Zhang, H., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0061-1 · Cited by 48 · see citing works
Self-citationParekh, P. K., Becker-Krail, D., Sundaravelu, P., Ishigaki, S., Okado, H., Sobue, G., Huang, Y., & McClung, C. A. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.06.022 · Cited by 48 · see citing works
Self-citationBaird, A. L., Coogan, A. N., Kaufling, J., Barrot, M., & Thome, J. (2013) · Brain Research · doi:10.1016/j.brainres.2013.03.038 · Cited by 46 · see citing works
McCarthy, M. J., Fernandes, M., Kranzler, H. R., Covault, J. M., & Welsh, D. K. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12106 · Cited by 32 · see citing works
Doura, M. B., Luu, T. V., Lee, N. H., & Perry, D. C. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.06.071 · Cited by 24 · see citing works
Photoperiodic suppression of drug reinstatement
Sorg, B. A., Stark, G., Sergeeva, A., & Jansen, H. T. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2010.12.022 · Cited by 25 · see citing works
Güleç, A., Güler, H. A., & Türkoğlu, S. (2024) · Chronobiology International · doi:10.1080/07420528.2024.2319218 · Cited by 3 · see citing works
- Authors
- McClung, C. A., Sidiropoulou, K., Vitaterna, M., Takahashi, J. S., White, F. J., Cooper, D. C., & Nestler, E. J.
- Affiliations
- Northwestern University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2005-06-20
- Volume
- 102
- Issue
- 26
- Pages
- 9377-9381
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1166621
- OpenAlex
- W1998352623
- Cited by
- 493
- References
- 37
- Citations by year
- 2026: 15 · 2025: 10 · 2024: 17 · 2023: 17 · 2022: 24 · 2021: 28 · 2020: 19 · 2019: 21 · 2018: 30 · 2017: 25 · 2016: 24 · 2015: 23 · 2014: 32 · 2013: 25 · 2012: 27
- FWCI
- 9.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health
- National Institute on Drug Abuse (K01DA017750)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- clock genes, circadian rhythm, cocaine reward, dopaminergic neurons, ventral tegmental area, tyrosine hydroxylase, dopamine synthesis, drug addiction, knockout mice
- MeSH terms
- Animals, Brain, Circadian Rhythm, Cocaine, Dopamine, Dose-Response Relationship, Drug, Electrophysiology, Homozygote, Immunohistochemistry, Male, Mice, Transgenic, Models, Neurological, Mutation, Neurons, Phenotype, Phosphorylation, Reward, Time Factors, Tyrosine 3-Monooxygenase, Blotting, Western, Trans-Activators, Point Mutation, Ventral Tegmental Area, Substance-Related Disorders, Oligonucleotide Array Sequence Analysis, Mice, CLOCK Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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