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2 - Central Clock Dynamics

Daily Timekeeping, Photic Processing, and Photoperiodic Encoding by the Suprachiasmatic Nucleus

Published online by Cambridge University Press:  07 October 2023

By
Deborah A. M. Joye ,
Robert Wheeler  and
Jennifer A. Evans
Edited by
Laura K. Fonken  and
Randy J. Nelson
Laura K. Fonken
Affiliation:
University of Texas, Austin
Randy J. Nelson
Affiliation:
West Virginia University
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Summary

Daily and seasonal rhythms are programmed by neural circuits that anticipate predictable changes in the environment (i.e., temperature, food, predation). The time and duration of daily light exposure is a strategic cue used to predict changes in the environment that determine fitness and survival. Light is transduced by a specialized visual system that serves as an irradiance detector. These inputs are processed and encoded by the suprachiasmatic nucleus (SCN), which serves as the body’s daily clock and annual calendar. The SCN encodes time-of-day and photoperiod to regulate downstream systems via multiple routes (e.g., melatonin, cortisol, feeding, body temperature). A deeper understanding of SCN timekeeping circuits, photoperiodic encoding mechanisms, and light-driven cellular adaptations is imperative for understanding plasticity and pathology in multiple biological systems.

Keywords

circadian rhythmsseasonalitybiological clocksSCN
Type
Chapter
Information
Biological Implications of Circadian Disruption
A Modern Health Challenge
 , pp. 23 - 57
Publisher: Cambridge University Press
Print publication year: 2023

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References

Abrahamson, E. E., & Moore, R. Y. (2001). Suprachiasmatic nucleus in the mouse: Retinal innervation, intrinsic organization and efferent projections. Brain Res, 916(1–2), 172–191.Google Scholar
Adlanmerini, M., Krusen, B. M., Nguyen, H. C. B., Teng, C. W., Woodie, L. N., Tackenberg, M. C., Geisler, C. E., Gaisinsky, J., Peed, L. C., Carpenter, B. J., Hayes, M. R., & Lazar, M. A. (2021). Rev-erb nuclear receptors in the suprachiasmatic nucleus control circadian period and restrict diet-induced obesity. Sci Adv, 7(44), eabh2007.Google Scholar
Albers, H. E., Walton, J. C., Gamble, K. L., McNeill, J. K., & Hummer, D. L. (2017). The dynamics of GABA signaling: Revelations from the circadian pacemaker in the suprachiasmatic nucleus. Front Neuroendocrinol, 44, 35–82.Google Scholar
Albus, H., Vansteensel, M. J., Michel, S., Block, G. D., & Meijer, J. H. (2005). A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol, 15(10), 886–893.CrossRefGoogle ScholarPubMed
An, S., Irwin, R. P., Allen, C. N., Tsai, C. A., & Herzog, E. D. (2011). Vasoactive intestinal polypeptide requires parallel changes in adenylate cyclase and phospholipase c to entrain circadian rhythms to a predictable phase. J Neurophysiol, 105(5), 2289–2296.CrossRefGoogle ScholarPubMed
Antle, M. C., & Silver, R. (2005). Orchestrating time: Arrangements of the brain circadian clock. Trends Neurosci, 28(3), 145–151.Google Scholar
Aranda, M. L., & Schmidt, T. M. (2020). Diversity of intrinsically photosensitive retinal ganglion cells: Circuits and functions. Cell Mol Life Sci, 78(3), 889–907.Google Scholar
Ashkenazy-Frolinger, T., Einat, H., & Kronfeld-Schor, N. (2015). Diurnal rodents as an advantageous model for affective disorders: Novel data from diurnal degu (Octodon Degus). J Neural Transm, 122(Suppl 1), S35–S45.Google Scholar
Ashkenazy-Frolinger, T., Kronfeld-Schor, N., Juetten, J., & Einat, H. (2010). It is darkness and not light: Depression-like behaviors of diurnal unstriped Nile grass rats maintained under a short photoperiod schedule. J Neurosci Methods, 186(2), 165–170.Google Scholar
Aton, S. J., Colwell, C. S., Harmar, A. J., Waschek, J., & Herzog, E. D. (2005). Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci, 8(4), 476–483.Google Scholar
Aumann, T. D., Raabus, M., Tomas, D., Prijanto, A., Churilov, L., Spitzer, N. C., & Horne, M. K. (2016). Differences in number of midbrain dopamine neurons associated with summer and winter photoperiods in humans. PLoS One, 11(7), e0158847.Google Scholar
Ayers, J. W., Althouse, B. M., Allem, J. P., Rosenquist, J. N., & Ford, D. E. (2013). Seasonality in seeking mental health information on google. Am J Prev Med, 44(5), 520–525.Google Scholar
Azzi, A., Evans, J. A., Leise, T., Myung, J., Takumi, T., Davidson, A. J., & Brown, S. A. (2017). Network dynamics mediate circadian clock plasticity. Neuron, 93(2), 441–450.CrossRefGoogle ScholarPubMed
Ball, G. F., & Balthazart, J. (2015). Seasonal changes in the neuroendocrine system: Introduction to the special issue. Front Neuroendocrinol, 37, 1–2.Google Scholar
Bartness, T. J., Goldman, B. D., & Bittman, E. L. (1991). SCN lesions block responses to systemic melatonin infusions in Siberian hamsters. Am J Physiol, 260(1 Pt 2), R102–R112.Google Scholar
Bass, C. E., Jansen, H. T., & Roberts, D. C. (2010). Free-running rhythms of cocaine self-administration in rats held under constant lighting conditions. Chronobiol Int, 27(3), 535–548.Google Scholar
Bedont, J. L., Rohr, K. E., Bathini, A., Hattar, S., Blackshaw, S., Sehgal, A., & Evans, J. A. (2018). Asymmetric vasopressin signaling spatially organizes the master circadian clock. J Comp Neurol, 526(13), 2048–2067.Google Scholar
Benabid, N., Mesfioui, A., & Ouichou, A. (2008). Effects of photoperiod regimen on emotional behaviour in two tests for anxiolytic activity in Wistar rat. Brain Res Bull, 75(1), 53–59.CrossRefGoogle ScholarPubMed
Berson, D. M., Castrucci, A. M., & Provencio, I. (2010). Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Comp Neurol, 518(13), 2405–2422.CrossRefGoogle ScholarPubMed
Binkley, S., & Mosher, K. (1986). Photoperiod modifies circadian resetting responses in sparrows. Am J Physiol, 251(6 Pt 2), R1156–R1162.Google ScholarPubMed
Bittman, E. L., Bartness, T. J., Goldman, B. D., & DeVries, G. J. (1991). Suprachiasmatic and paraventricular control of photoperiodism in Siberian hamsters. Am J Physiol, 260(1 Pt 2), R90–R101.Google Scholar
Boland, M. R., Shahn, Z., Madigan, D., Hripcsak, G., & Tatonetti, N. P. (2015). Birth month affects lifetime disease risk: A phenome-wide method. J Am Med Inform Assoc, 22(5), 1042–1053.Google Scholar
Brainard, G. C., Hanifin, J. P., Greeson, J. M., Byrne, B., Glickman, G., Gerner, E., & Rollag, M. D. (2001). Action spectrum for melatonin regulation in humans: Evidence for a novel circadian photoreceptor. J Neurosci, 21(16), 6405–6412.Google Scholar
Brancaccio, M., Maywood, E. S., Chesham, J. E., Loudon, A. S., & Hastings, M. H. (2013). A Gq-Ca2+ axis controls circuit-level encoding of circadian time in the suprachiasmatic nucleus. Neuron, 78(4), 714–728.Google Scholar
Brown, T. M., Hughes, A. T., & Piggins, H. D. (2005). Gastrin-releasing peptide promotes suprachiasmatic nuclei cellular rhythmicity in the absence of vasoactive intestinal polypeptide-VPAC2 receptor signaling. J Neurosci, 25(48), 11155–11164.CrossRefGoogle ScholarPubMed
Brown, T. M., & Piggins, H. D. (2009). Spatiotemporal heterogeneity in the electrical activity of suprachiasmatic nuclei neurons and their response to photoperiod. J Biol Rhythms, 24(1), 44–54.Google Scholar
Brown, T. M., Wynne, J., Piggins, H. D., & Lucas, R. J. (2011). Multiple hypothalamic cell populations encoding distinct visual information. J Physiol, 589(Pt 5), 1173–1194.Google Scholar
Buhr, E. D., Yoo, S. H., & Takahashi, J. S. (2010). Temperature as a universal resetting cue for mammalian circadian oscillators. Science, 330(6002), 379–385.CrossRefGoogle ScholarPubMed
Buijink, M. R., Olde Engberink, A. H. O., Wit, C. B., Almog, A., Meijer, J. H., Rohling, J. H. T., & Michel, S. (2020). Aging affects the capacity of photoperiodic adaptation downstream from the central molecular clock. J Biol Rhythms, 35(2), 167–179.CrossRefGoogle ScholarPubMed
Buijs, R. M., Wortel, J., van Heerikhuize, J. J., Feenstra, M. G. P., Ter Horst, G. J., Romijn, H. J., & Kalsbeek, A. (1999). Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci, 11(5), 1535–1544.Google Scholar
Cajochen, C. (2007). Alerting effects of light. Sleep Med Rev, 11(6), 453–464.Google Scholar
Carr, A. J., Johnston, J. D., Semikhodskii, A. G., Nolan, T., Cagampang, F. R., Stirland, J. A., & Loudon, A. S. (2003). Photoperiod differentially regulates circadian oscillators in central and peripheral tissues of the Syrian hamster. Curr Biol, 13(17), 1543–1548.Google Scholar
Cassone, V. M., Chesworth, M. J., & Armstrong, S. M. (1986). Entrainment of rat circadian rhythms by daily injection of melatonin depends upon the hypothalamic suprachiasmatic nuclei. Physiol Behav, 36(6), 1111–1121.CrossRefGoogle ScholarPubMed
Castel, M., Morris, J., & Belenky, M. (1996). Non-synaptic and dendritic exocytosis from dense-cored vesicles in the suprachiasmatic nucleus. Neuroreport, 7(2), 543–547.Google Scholar
Chen, S. K., Badea, T. C., & Hattar, S. (2011). Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature, 476(7358), 92–95.Google Scholar
Collins, B., Pierre-Ferrer, S., Muheim, C., Lukacsovich, D., Cai, Y., Spinnler, A., Herrera, C. G., Wen, S., Winterer, J., Belle, M. D. C., Piggins, H. D., Hastings, M., Loudon, A., Yan, J., Foldy, C., Adamantidis, A., & Brown, S. A. (2020). Circadian VIPergic neurons of the suprachiasmatic nuclei sculpt the sleep-wake cycle. Neuron, 108(3), 486–499, e485.CrossRefGoogle ScholarPubMed
Colwell, C. S. (2001). NMDA-evoked calcium transients and currents in the suprachiasmatic nucleus: Gating by the circadian system. Eur J Neurosci, 13(7), 1420–1428.Google Scholar
Colwell, C. S. (2011). Linking neural activity and molecular oscillations in the SCN. Nat Rev Neurosci, 12(10), 553–569.Google Scholar
Colwell, C. S., Michel, S., Itri, J., Rodriguez, W., Tam, J., Lelievre, V., Hu, Z., Liu, X., & Waschek, J. A. (2003). Disrupted circadian rhythms in Vip- and Phi-deficient mice. Am J Physiol, 285(5), R939–R949.Google Scholar
Comai, S., Ochoa-Sanchez, R., Dominguez-Lopez, S., Bambico, F. R., & Gobbi, G. (2015). Melancholic-like behaviors and circadian neurobiological abnormalities in melatonin MT1 receptor knockout mice. Int J Neuropsychopharmacol, 18(3), pyu075.CrossRefGoogle ScholarPubMed
Coomans, C. P., Ramkisoensing, A., & Meijer, J. H. (2015). The suprachiasmatic nuclei as a seasonal clock. Front Neuroendocrinol, 37, 29–42.Google Scholar
Daan, S. (2000). Colin Pittendrigh, Jurgen Aschoff, and the natural entrainment of circadian systems. J Biol Rhythms, 15(3), 195–207.Google Scholar
Dardente, H., Menet, J. S., Challet, E., Tournier, B. B., Pevet, P., & Masson-Pevet, M. (2004). Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Brain Res Mol Brain Res, 124(2), 143–151.CrossRefGoogle ScholarPubMed
Dardente, H., Wood, S., Ebling, F., & Saenz de Miera, C. (2019). An integrative view of mammalian seasonal neuroendocrinology. J Neuroendocrinol, 31(5), e12729.Google Scholar
DeCoursey, P. J., & Krulas, J. R. (1998). Behavior of SCN-lesioned chipmunks in natural habitat: A pilot study. J Biol Rhythms, 13(3), 229–244.CrossRefGoogle ScholarPubMed
Dellapolla, A., Kloehn, I., Pancholi, H., Callif, B., Wertz, D., Rohr, K. E., Hurley, M. M., Baker, K. M., Hattar, S., Gilmartin, M. R., & Evans, J. A. (2017). Long days enhance recognition memory and increase insulin-like growth factor 2 in the hippocampus. Sci Rep, 7(1), 3925.Google Scholar
Dodd, A. N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J. M., Millar, A. J., & Webb, A. A. (2005). Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309(5734), 630–633.Google Scholar
Doi, M., Ishida, A., Miyake, A., Sato, M., Komatsu, R., Yamazaki, F., Kimura, I., Tsuchiya, S., Kori, H., Seo, K., Yamaguchi, Y., Matsuo, M., Fustin, J. M., Tanaka, R., Santo, Y., Yamada, H., Takahashi, Y., Araki, M., Nakao, K., … Okamura, H. (2011). Circadian regulation of intracellular g-protein signalling mediates intercellular synchrony and rhythmicity in the suprachiasmatic nucleus. Nat Commun, 2, 327.Google Scholar
Dubocovich, M. L., & Markowska, M. (2005). Functional MT1 and MT2 melatonin receptors in mammals. Endocrine, 27(2), 101–110.Google Scholar
Duffy, J. F., & Wright, K. P. Jr. (2005). Entrainment of the human circadian system by light. J Biol Rhythms, 20(4), 326–338.Google Scholar
Dulcis, D., Jamshidi, P., Leutgeb, S., & Spitzer, N. C. (2013). Neurotransmitter switching in the adult brain regulates behavior. Science, 340(6131), 449–453.CrossRefGoogle ScholarPubMed
Ebling, F. J. (2015). Hypothalamic control of seasonal changes in food intake and body weight. Front Neuroendocrinol, 37, 97–107.Google Scholar
Edwards, M. D., Brancaccio, M., Chesham, J. E., Maywood, E. S., & Hastings, M. H. (2016). Rhythmic expression of cryptochrome induces the circadian clock of arrhythmic suprachiasmatic nuclei through arginine vasopressin signaling. PNAS, 113(10), 2732–2737.Google Scholar
Eisenberg, D. P., Kohn, P. D., Baller, E. B., Bronstein, J. A., Masdeu, J. C., & Berman, K. F. (2010). Seasonal effects on human striatal presynaptic dopamine synthesis. J Neurosci, 30(44), 14691–14694.Google Scholar
Elliott, J. E. (1981). Circadian rhythms, entrainment and photoperiodism in the Syrian hamster. In Follett, B. K., & Follett, D. E. (eds.), Biological clocks in seasonal reproductive cycles (pp. 203–217). Bristol: J. Wright & Sons.Google Scholar
Enoki, R., Kuroda, S., Ono, D., Hasan, M. T., Ueda, T., Honma, S., & Honma, K. (2012). Topological specificity and hierarchical network of the circadian calcium rhythm in the suprachiasmatic nucleus. PNAS, 109(52), 21498–21503.Google Scholar
Eskes, G. A., & Rusak, B. (1985). Horizontal knife cuts in the suprachiasmatic area prevent hamster gonadal responses to photoperiod. Neurosci Lett, 61(3), 261–266.Google Scholar
Evans, J. A. (2016). Collective timekeeping among cells of the master circadian clock. J Endocrinol, 230(1), R27–R49.Google Scholar
Evans, J. A., & Davidson, A. J. (2013). Health consequences of circadian disruption in humans and animal models. Prog Mol Biol Transl Sci, 119, 283–323.CrossRefGoogle ScholarPubMed
Evans, J. A., & Gorman, M. R. (2016). In synch but not in step: Circadian clock circuits regulating plasticity in daily rhythms. Neuroscience, 320, 259–280.CrossRefGoogle Scholar
Evans, J. A., Leise, T. L., Castanon-Cervantes, O., & Davidson, A. J. (2011). Intrinsic regulation of spatiotemporal organization within the suprachiasmatic nucleus. PLoS One, 6(1), e15869.CrossRefGoogle ScholarPubMed
Evans, J. A., Leise, T. L., Castanon-Cervantes, O., & Davidson, A. J. (2013). Dynamic interactions mediated by nonredundant signaling mechanisms couple circadian clock neurons. Neuron, 80(4), 973–983.Google Scholar
Evans, J. A., & Silver, R. (2016). The suprachiasmatic nucleus and the circadian timekeeping system of the body. In Pfaff, D., & Volkow, N. (eds.), Neuroscience in the 21st century: From basic to clinical, 2241–2288. New York: Springer.CrossRefGoogle Scholar
Fagiani, F., Di Marino, D., Romagnoli, A., Travelli, C., Voltan, D., Mannelli, L. D. C., Racchi, M., Govoni, S., & Lanni, C. (2022). Molecular regulations of circadian rhythm and implications for physiology and diseases. Signal Transduct Target Ther, 7(1), 41.Google Scholar
Farajnia, S., van Westering, T. L., Meijer, J. H., & Michel, S. (2014). Seasonal induction of GABAergic excitation in the central mammalian clock. PNAS, 111(26), 9627–9632.Google Scholar
Fernandez, D. C., Chang, Y. T., Hattar, S., & Chen, S. K. (2016). Architecture of retinal projections to the central circadian pacemaker. PNAS, 113(21), 6047–6052.CrossRefGoogle Scholar
Fernandez, D. C., Fogerson, P. M., Lazzerini Ospri, L., Thomsen, M. B., Layne, R. M., Severin, D., Zhan, J., Singer, J. H., Kirkwood, A., Zhao, H., Berson, D. M., & Hattar, S. (2018). Light affects mood and learning through distinct retina-brain pathways. Cell, 175(1), 71–84 e18.Google Scholar
Flaisher-Grinberg, S., Gampetro, D. R., Kronfeld-Schor, N., & Einat, H. (2011). Inconsistent effects of photoperiod manipulations in tests for affective-like changes in mice: Implications for the selection of appropriate model animals. Behav Pharmacol, 22(1), 23–30.Google Scholar
Flourakis, M., Kula-Eversole, E., Hutchison, A. L., Han, T. H., Aranda, K., Moose, D. L., White, K. P., Dinner, A. R., Lear, B. C., Ren, D. J., Diekman, C. O., Raman, I. M., & Allada, R. (2015). A conserved bicycle model for circadian clock control of membrane excitability. Cell, 162(4), 836–848.Google Scholar
Foster, R. G., & Roenneberg, T. (2008). Human responses to the geophysical daily, annual and lunar cycles. Curr Biol, 18(17), R784–R794.CrossRefGoogle Scholar
Freeman, G. M. Jr., Krock, R. M., Aton, S. J., Thaben, P., & Herzog, E. D. (2013). GABA networks destabilize genetic oscillations in the circadian pacemaker. Neuron, 78, 799–806.Google Scholar
Gamble, K. L., Allen, G. C., Zhou, T., & McMahon, D. G. (2007). Gastrin-releasing peptide mediates light-like resetting of the suprachiasmatic nucleus circadian pacemaker through camp response element-binding protein and Per1 activation. J Neurosci, 27(44), 12078–12087.Google Scholar
Gizowski, C., Zaelzer, C., & Bourque, C. W. (2016). Clock-driven vasopressin neurotransmission mediates anticipatory thirst prior to sleep. Nature, 537(7622), 685–688.Google Scholar
Glickman, G., Byrne, B., Pineda, C., Hauck, W. W., & Brainard, G. C. (2006). Light therapy for seasonal affective disorder with blue narrow-band light-emitting diodes (LEDs). Biol Psychiatry, 59(6), 502–507.Google Scholar
Glickman, G., Webb, I. C., Elliott, J. A., Baltazar, R. M., Reale, M. E., Lehman, M. N., & Gorman, M. R. (2012). Photic sensitivity for circadian response to light varies with photoperiod. J Biol Rhythms, 27(4), 308–318.Google Scholar
Goldman, B. D. (1999). The Siberian hamster as a model for study of the mammalian photoperiodic mechanism. Adv Exp Med Biol, 460, 155–164.CrossRefGoogle Scholar
Goldman, B. D. (2001). Mammalian photoperiodic system: Formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms, 16(4), 283–301.Google Scholar
Grandner, M. A., Kripke, D. F., & Langer, R. D. (2006). Light exposure is related to social and emotional functioning and to quality of life in older women. Psychiatry Res, 143(1), 35–42.Google Scholar
Graw, P., Recker, S., Sand, L., Krauchi, K., & Wirz-Justice, A. (1999). Winter and summer outdoor light exposure in women with and without seasonal affective disorder. J Affect Disord, 56(2–3), 163–169.Google Scholar
Green, N. H., Jackson, C. R., Iwamoto, H., Tackenberg, M. C., & McMahon, D. G. (2015). Photoperiod programs dorsal raphe serotonergic neurons and affective behaviors. Curr Biol, 25(10), 1389–1394.Google Scholar
Grippo, R. M., Purohit, A. M., Zhang, Q., Zweifel, L. S., & Guler, A. D. (2017). Direct midbrain dopamine input to the suprachiasmatic nucleus accelerates circadian entrainment. Curr Biol, 27(16), 2465–2475 e2463.Google Scholar
Grosse, J., & Hastings, M. H. (1996). A role for the circadian clock of the suprachiasmatic nuclei in the interpretation of serial melatonin signals in the Syrian hamster. J Biol Rhythms, 11(4), 317–324.CrossRefGoogle ScholarPubMed
Gu, C., Li, J., Zhou, J., Yang, H., & Rohling, J. (2021). Network structure of the master clock is important for its primary function. Front Physiol, 12, 678391.CrossRefGoogle ScholarPubMed
Guillemette, J., Hebert, M., Paquet, J., & Dumont, M. (1998). Natural bright light exposure in the summer and winter in subjects with and without complaints of seasonal mood variations. Biol Psychiatry, 44(7), 622–628.Google Scholar
Guler, A. D., Ecker, J. L., Lall, G. S., Haq, S., Altimus, C. M., Liao, H. W., Barnard, A. R., Cahill, H., Badea, T. C., Zhao, H., Hankins, M. W., Berson, D. M., Lucas, R. J., Yau, K. W., & Hattar, S. (2008). Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature, 453(7191), 102–105.Google Scholar
Hamnett, R., Crosby, P., Chesham, J. E., & Hastings, M. H. (2019). Vasoactive intestinal peptide controls the suprachiasmatic circadian clock network via Erk1/2 and Dusp4 signalling. Nat Commun, 10(1), 542.Google Scholar
Han, S., Yu, F. H., Schwartz, M. D., Linton, J. D., Bosma, M. M., Hurley, J. B., Catterall, W. A., & de la Iglesia, H. O. (2012). Na(v)1.1 channels are critical for intercellular communication in the suprachiasmatic nucleus and for normal circadian rhythms. PNAS, 109(6), E368–E377.Google Scholar
Harmar, A. J. (2003). An essential role for peptidergic signalling in the control of circadian rhythms in the suprachiasmatic nuclei. J Neuroendocrinol, 15(4), 335–338.Google Scholar
Harmar, A. J., Marston, H. M., Shen, S., Spratt, C., West, K. M., Sheward, W. J., Morrison, C. F., Dorin, J. R., Piggins, H. D., Reubi, J. C., Kelly, J. S., Maywood, E. S., & Hastings, M. H. (2002). The VPAC2 receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell, 109(4), 497–508.Google Scholar
Harmatz, M. G., Well, A. D., Overtree, C. E., Kawamura, K. Y., Rosal, M., & Ockene, I. S. (2000). Seasonal variation of depression and other moods: A longitudinal approach. J Biol Rhythms, 15(4), 344–350.CrossRefGoogle ScholarPubMed
Harrison, E. M., & Gorman, M. R. (2015). Rapid adjustment of circadian clocks to simulated travel to time zones across the globe. J Biol Rhythms, 30, 557–562.Google Scholar
Harvey, J. R. M., Plante, A. E., & Meredith, A. L. (2020). Ion channels controlling circadian rhythms in suprachiasmatic nucleus excitability. Physiol Rev, 100(4), 1415–1454.Google Scholar
Hastings, M. H., Maywood, E. S., & Brancaccio, M. (2018). Generation of circadian rhythms in the suprachiasmatic nucleus. Nat Rev Neurosci, 19(8), 453–469.Google Scholar
Hazlerigg, D. G., Ebling, F. J., & Johnston, J. D. (2005). Photoperiod differentially regulates gene expression rhythms in the rostral and caudal SCN. Curr Biol, 15(12), R449–R450.Google Scholar
Herzog, E. D., Aton, S. J., Numano, R., Sakaki, Y., & Tei, H. (2004). Temporal precision in the mammalian circadian system: A reliable clock from less reliable neurons. J Biol Rhythms, 19(1), 35–46.Google Scholar
Houben, T., Deboer, T., van Oosterhout, F., & Meijer, J. H. (2009). Correlation with behavioral activity and rest implies circadian regulation by SCN neuronal activity levels. J Biol Rhythms, 24(6), 477–487.CrossRefGoogle ScholarPubMed
Hughes, A. T., Croft, C. L., Samuels, R. E., Myung, J., Takumi, T., & Piggins, H. D. (2015). Constant light enhances synchrony among circadian clock cells and promotes behavioral rhythms in VPAC2-signaling deficient mice. Sci Rep, 5, 14044.CrossRefGoogle ScholarPubMed
Hughes, A. T., Fahey, B., Cutler, D. J., Coogan, A. N., & Piggins, H. D. (2004). Aberrant gating of photic input to the suprachiasmatic circadian pacemaker of mice lacking the VPAC2 receptor. J Neurosci, 24(14), 3522–3526.Google Scholar
Hughes, A. T., Guilding, C., Lennox, L., Samuels, R. E., McMahon, D. G., & Piggins, H. D. (2008). Live imaging of altered Period1 expression in the suprachiasmatic nuclei of Vipr2-/- mice. J Neurochem, 106(4), 1646–1657.CrossRefGoogle ScholarPubMed
Humlova, M., & Illnerova, H. (1992). Resetting of the rat circadian clock after a shift in the light/dark cycle depends on the photoperiod. Neurosci Res, 13(2), 147–153.CrossRefGoogle ScholarPubMed
de la Iglesia, H. O., Cambras, T., Schwartz, W. J., & Diez-Noguera, A. (2004). Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr Biol, 14(9), 796–800.Google Scholar
de la Iglesia, H. O., Meyer, J., Carpino, A. Jr., & Schwartz, W. J. (2000). Antiphase oscillation of the left and right suprachiasmatic nuclei. Science, 290(5492), 799–801.Google Scholar
Inagaki, N., Honma, S., Ono, D., Tanahashi, Y., & Honma, K. (2007). Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. PNAS, 104(18), 7664–7669.Google Scholar
Inouye, S. T., & Turek, F. W. (1986). Horizontal knife cuts either ventral or dorsal to the hypothalamic paraventricular nucleus block testicular regression in golden hamsters maintained in short days. Brain Res, 370(1), 102–107.Google Scholar
Irwin, R. P., & Allen, C. N. (2007). Calcium response to retinohypothalamic tract synaptic transmission in suprachiasmatic nucleus neurons. J Neurosci, 27(43), 11748–11757.Google Scholar
Jagannath, A., Butler, R., Godinho, S. I., Couch, Y., Brown, L. A., Vasudevan, S. R., Flanagan, K. C., Anthony, D., Churchill, G. C., Wood, M. J., Steiner, G., Ebeling, M., Hossbach, M., Wettstein, J. G., Duffield, G. E., Gatti, S., Hankins, M. W., Foster, R. G., & Peirson, S. N. (2013). The Crtc1-Sik1 pathway regulates entrainment of the circadian clock. Cell, 154(5), 1100–1111.Google Scholar
Jagota, A., de la Iglesia, H. O., & Schwartz, W. J. (2000). Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat Neurosci, 3(4), 372–376.Google Scholar
Johnson, C. H. (1999). Forty years of PRCs: What have we learned? Chronobiol Int, 16(6), 711–743.Google Scholar
Johnston, J. D., Ebling, F. J., & Hazlerigg, D. G. (2005). Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus Sungorus). Eur J Neurosci, 21(11), 2967–2974.CrossRefGoogle ScholarPubMed
Jones, J. R., Chaturvedi, S., Granados-Fuentes, D., & Herzog, E. D. (2021). Circadian neurons in the paraventricular nucleus entrain and sustain daily rhythms in glucocorticoids. Nat Commun, 12(1), 5763.CrossRefGoogle ScholarPubMed
Jones, J. R., Simon, T., Lones, L., & Herzog, E. D. (2018). SCN VIP neurons are essential for normal light-mediated resetting of the circadian system. J Neurosci, 38(37), 7986–7995.CrossRefGoogle ScholarPubMed
Joye, D. A. M., & Evans, J. A. (2021). Sex differences in daily timekeeping and circadian clock circuits. Semin Cell Dev Biol, 126, 45–55.Google Scholar
Kalsbeek, A., Perreau-Lenz, S., & Buijs, R. M. (2006). A network of (autonomic) clock outputs. Chronobiol Int, 23(3), 521–535.Google Scholar
Kasper, S., Rogers, S. L., Yancey, A., Schulz, P. M., Skwerer, R. G., & Rosenthal, N. E. (1989). Phototherapy in individuals with and without subsyndromal seasonal affective disorder. Arch Gen Psychiatry, 46(9), 837–844.Google Scholar
Kiessling, S., Sollars, P. J., & Pickard, G. E. (2014). Light stimulates the mouse adrenal through a retinohypothalamic pathway independent of an effect on the clock in the suprachiasmatic nucleus. PLoS One, 9(3), e92959.CrossRefGoogle ScholarPubMed
Kim, S., & McMahon, D. G. (2021). Light sets the brain’s daily clock by regional quickening and slowing of the molecular clockworks at dawn and dusk. Elife, 10, e70137.Google Scholar
Krivisky, K., Ashkenazy, T., Kronfeld-Schor, N., & Einat, H. (2011). Antidepressants reverse short-photoperiod-induced, forced swim test depression-like behavior in the diurnal fat sand rat: Further support for the utilization of diurnal rodents for modeling affective disorders. Neuropsychobiology, 63(3), 191–196.Google Scholar
Leach, G., Ramanathan, C., Langel, J., & Yan, L. (2013). Responses of brain and behavior to changing day-length in the diurnal grass rat (Arvicanthis Niloticus). Neuroscience, 234, 31–39.Google Scholar
Leak, R. K., & Moore, R. Y. (2001). Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol, 433(3), 312–334.Google Scholar
Lee, B., Li, A., Hansen, K. F., Cao, R., Yoon, J. H., & Obrietan, K. (2010). CREB influences timing and entrainment of the SCN circadian clock. J Biol Rhythms, 25(6), 410–420.Google Scholar
Lee, I. T., Chang, A. S., Manandhar, M., Shan, Y., Fan, J., Izumo, M., Ikeda, Y., Motoike, T., Dixon, S., Seinfeld, J. E., Takahashi, J. S., & Yanagisawa, M. (2015). Neuromedin S-producing neurons act as essential pacemakers in the suprachiasmatic nucleus to couple clock neurons and dictate circadian rhythms. Neuron, 85(5), 1086–1102.Google Scholar
Lee, J. E., Zamdborg, L., Southey, B. R., Atkins, N. Jr., Mitchell, J. W., Li, M., Gillette, M. U., Kelleher, N. L., & Sweedler, J. V. (2013). Quantitative peptidomics for discovery of circadian-related peptides from the rat suprachiasmatic nucleus. J Proteome Res, 12(2), 585–593.Google Scholar
Lee, R., Tapia, A., Kaladchibachi, S., Grandner, M. A., & Fernandez, F. X. (2021). Meta-analysis of light and circadian timekeeping in rodents. Neurosci Biobehav Rev, 123, 215–229.CrossRefGoogle ScholarPubMed
Lee, T. M., & Zucker, I. (1991). Suprachiasmatic nucleus and photic entrainment of circannual rhythms in ground squirrels. J Biol Rhythms, 6(4), 315–330.Google Scholar
Levitan, R. D., Masellis, M., Basile, V. S., Lam, R. W., Kaplan, A. S., Davis, C., Muglia, P., Mackenzie, B., Tharmalingam, S., Kennedy, S. H., Macciardi, F., & Kennedy, J. L. (2004). The dopamine-4 receptor gene associated with binge eating and weight gain in women with seasonal affective disorder: An evolutionary perspective. Biol Psychiatry, 56(9), 665–669.Google Scholar
Levitan, R. D., Masellis, M., Lam, R. W., Kaplan, A. S., Davis, C., Tharmalingam, S., Mackenzie, B., Basile, V. S., & Kennedy, J. L. (2006). A birth-season/Drd4 gene interaction predicts weight gain and obesity in women with seasonal affective disorder: A seasonal thrifty phenotype hypothesis. Neuropsychopharmacology, 31(11), 2498–2503.Google Scholar
Lewy, A. J., Lefler, B. J., Emens, J. S., & Bauer, V. K. (2006). The circadian basis of winter depression. PNAS, 103(19), 7414–7419.CrossRefGoogle ScholarPubMed
Lim, A. S., Klein, H. U., Yu, L., Chibnik, L. B., Ali, S., Xu, J., Bennett, D. A., & De Jager, P. L. (2017). Diurnal and seasonal molecular rhythms in human neocortex and their relation to Alzheimer’s disease. Nat Commun, 8, 14931.Google Scholar
Lincoln, G. A., Johnston, J. D., Andersson, H., Wagner, G., & Hazlerigg, D. G. (2005). Photorefractoriness in mammals: Dissociating a seasonal timer from the circadian-based photoperiod response. Endocrinology, 146(9), 3782–3790.Google Scholar
Liu, A. C., Tran, H. G., Zhang, E. E., Priest, A. A., Welsh, D. K., & Kay, S. A. (2008). Redundant function of Rev-erbalpha and beta and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet, 4(2), e1000023.Google Scholar
Liu, A. C., Welsh, D. K., Ko, C. H., Tran, H. G., Zhang, E. E., Priest, A. A., Buhr, E. D., Singer, O., Meeker, K., Verma, I. M., Doyle, F. J., 3rd, Takahashi, J. S., & Kay, S. A. (2007). Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell, 129(3), 605–616.Google Scholar
Liu, C., & Reppert, S. M. (2000). GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron, 25(1), 123–128.Google Scholar
Loudon, A. S., Meng, Q. J., Maywood, E. S., Bechtold, D. A., Boot-Handford, R. P., & Hastings, M. H. (2007). The biology of the circadian Ck1epsilon tau mutation in mice and Syrian hamsters: A tale of two species. Cold Spring Harb Symp Quant Biol, 72, 261–271.Google Scholar
Low-Zeddies, S. S., & Takahashi, J. S. (2001). Chimera analysis of the Clock mutation in mice shows that complex cellular integration determines circadian behavior. Cell, 105(1), 25–42.Google Scholar
Lucassen, E. A., van Diepen, H. C., Houben, T., Michel, S., Colwell, C. S., & Meijer, J. H. (2012). Role of vasoactive intestinal peptide in seasonal encoding by the suprachiasmatic nucleus clock. Eur J Neurosci, 35(9), 1466–1474.Google Scholar
Lyall, L. M., Wyse, C. A., Celis-Morales, C. A., Lyall, D. M., Cullen, B., Mackay, D., Ward, J., Graham, N., Strawbridge, R. J., Gill, J. M. R., Ferguson, A., Bailey, M. E. S., Pell, J. P., Curtis, A. M., & Smith, D. J. (2018). Seasonality of depressive symptoms in women but not in men: A cross-sectional study in the UK biobank cohort. J Affect Disord, 229, 296–305.Google Scholar
Maejima, T., Tsuno, Y., Miyazaki, S., Tsuneoka, Y., Hasegawa, E., Islam, M. T., Enoki, R., Nakamura, T. J., & Mieda, M. (2021). GABA from vasopressin neurons regulates the time at which suprachiasmatic nucleus molecular clocks enable circadian behavior. PNAS, 118(6), e20101681.Google Scholar
Magnusson, A. (2000). An overview of epidemiological studies on seasonal affective disorder. Acta Psychiatr Scand, 101(3), 176–184.Google Scholar
Majrashi, N. A., Alyami, A. S., Shubayr, N. A., Alenezi, M. M., & Waiter, G. D. (2022). Amygdala and subregion volumes are associated with photoperiod and seasonal depressive symptoms: A cross-sectional study in the UK biobank cohort. Eur J Neurosci, 55(5), 1388–1404.Google Scholar
Martinez, M. E. (2018). The calendar of epidemics: Seasonal cycles of infectious diseases. PLoS Pathog, 14(11), e1007327.Google Scholar
Masson-Pevet, M., Naimi, F., Canguilhem, B., Saboureau, M., Bonn, D., & Pevet, P. (1994). Are the annual reproductive and body weight rhythms in the male European hamster (Cricetus Cricetus) dependent upon a photoperiodically entrained circannual clock? J Pineal Res, 17(4), 151–163.Google Scholar
Mathes, A., Engel, L., Holthues, H., Wolloscheck, T., & Spessert, R. (2007). Daily profile in melanopsin transcripts depends on seasonal lighting conditions in the rat retina. J Neuroendocrinol, 19(12), 952–957.Google Scholar
Maywood, E. S., Chesham, J. E., O’Brien, J. A., & Hastings, M. H. (2011). A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. PNAS, 108(34), 14306–14311.Google Scholar
Maywood, E. S., Reddy, A. B., Wong, G. K., O’Neill, J. S., O’Brien, J. A., McMahon, D. G., Harmar, A. J., Okamura, H., & Hastings, M. H. (2006). Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr Biol, 16(6), 599–605.Google Scholar
Mazuski, C., Abel, J. H., Chen, S. P., Hermanstyne, T. O., Jones, J. R., Simon, T., Doyle, F. J., 3rd, & Herzog, E. D. (2018). Entrainment of circadian rhythms depends on firing rates and neuropeptide release of VIP SCN neurons. Neuron, 99(3), 555–563 e555.Google Scholar
Mazuski, C., Chen, S. P., & Herzog, E. D. (2020). Different roles for VIP neurons in the neonatal and adult suprachiasmatic nucleus. J Biol Rhythms, 35(5), 465–475.Google Scholar
McArthur, A. J., Coogan, A. N., Ajpru, S., Sugden, D., Biello, S. M., & Piggins, H. D. (2000). Gastrin-releasing peptide phase-shifts suprachiasmatic nuclei neuronal rhythms in vitro. J Neurosci, 20(14), 5496–5502.Google Scholar
Meijer, J. H., & Schwartz, W. J. (2003). In search of the pathways for light-induced pacemaker resetting in the suprachiasmatic nucleus. J Biol Rhythms, 18(3), 235–249.Google Scholar
Melrose, S. (2015). Seasonal affective disorder: An overview of assessment and treatment approaches. Depress Res Treat, 2015, 178564.Google ScholarPubMed
Mendoza-Viveros, L., Chiang, C. K., Ong, J. L. K., Hegazi, S., Cheng, A. H., Bouchard-Cannon, P., Fana, M., Lowden, C., Zhang, P., Bothorel, B., Michniewicz, M. G., Magill, S. T., Holmes, M. M., Goodman, R. H., Simonneaux, V., Figeys, D., & Cheng, H. M. (2017). Mir-132/212 modulates seasonal adaptation and dendritic morphology of the central circadian clock. Cell Rep, 19(3), 505–520.Google Scholar
Meredith, A. L., Wiler, S. W., Miller, B. H., Takahashi, J. S., Fodor, A. A., Ruby, N. F., & Aldrich, R. W. (2006). Bk calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat Neurosci, 9(8), 1041–1049.Google Scholar
Mieda, M., Okamoto, H., & Sakurai, T. (2016). Manipulating the cellular circadian period of arginine vasopressin neurons alters the behavioral circadian period. Curr Biol, 26(18), 2535–2542.Google Scholar
Mieda, M., Ono, D., Hasegawa, E., Okamoto, H., Honma, K., Honma, S., & Sakurai, T. (2015). Cellular clocks in AVP neurons of the SCN are critical for interneuronal coupling regulating circadian behavior rhythm. Neuron, 85(5), 1103–1116.Google Scholar
Miller, M. A., Leckie, R. L., Donofry, S. D., Gianaros, P. J., Erickson, K. I., Manuck, S. B., & Roecklein, K. A. (2015). Photoperiod is associated with hippocampal volume in a large community sample. Hippocampus, 25(4), 534–543.Google Scholar
Modai, I., Kikinzon, L., & Valevski, A. (1994). Environmental factors and admission rates in patients with major psychiatric disorders. Chronobiol Int, 11(3), 196–199.Google Scholar
Mohawk, J. A., Green, C. B., & Takahashi, J. S. (2012). Central and peripheral circadian clocks in mammals. Annu Rev Neurosci, 35, 445–462.Google Scholar
Molina-Hernandez, M., & Tellez-Alcantara, P. (2000). Long photoperiod regimen may produce antidepressant actions in the male rat. Prog Neuropsychopharmacol Biol Psychiatry, 24(1), 105–116.Google Scholar
Monecke, S., Sage-Ciocca, D., Wollnik, F., & Pevet, P. (2013). Photoperiod can entrain circannual rhythms in pinealectomized European hamsters. J Biol Rhythms, 28(4), 278–290.Google Scholar
Moore, R. Y., Speh, J. C., & Leak, R. K. (2002). Suprachiasmatic nucleus organization. Cell Tissue Res, 309(1), 89–98.Google Scholar
Morris, E. L., Patton, A. P., Chesham, J. E., Crisp, A., Adamson, A., & Hastings, M. H. (2021). Single-cell transcriptomics of suprachiasmatic nuclei reveal a Prokineticin-driven circadian network. EMBO J, 40(20), e108614.Google Scholar
Mrugala, M., Zlomanczuk, P., Jagota, A., & Schwartz, W. J. (2000). Rhythmic multiunit neural activity in slices of hamster suprachiasmatic nucleus reflect prior photoperiod. Am J Physiol, 278(4), R987–R994.Google Scholar
Myung, J., Hong, S., DeWoskin, D., De Schutter, E., Forger, D. B., & Takumi, T. (2015). GABA-mediated repulsive coupling between circadian clock neurons in the SCN encodes seasonal time. PNAS, 112(29), E3920–E3929.Google Scholar
Naito, E., Watanabe, T., Tei, H., Yoshimura, T., & Ebihara, S. (2008). Reorganization of the suprachiasmatic nucleus coding for day length. J Biol Rhythms, 23(2), 140–149.Google Scholar
Noya, S. B., Colameo, D., Bruning, F., Spinnler, A., Mircsof, D., Opitz, L., Mann, M., Tyagarajan, S. K., Robles, M. S., & Brown, S. A. (2019). The forebrain synaptic transcriptome is organized by clocks but its proteome is driven by sleep. Science, 366(6462), eaav2642.Google Scholar
O’Neill, J. S., & Reddy, A. B. (2011). Circadian clocks in human red blood cells. Nature, 469(7331), 498–503.Google Scholar
Obrietan, K., Impey, S., & Storm, D. R. (1998). Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat Neurosci, 1(8), 693–700.Google Scholar
Oda, G. A., Menaker, M., & Friesen, W. O. (2000). Modeling the dual pacemaker system of the tau mutant hamster. J Biol Rhythms, 15(3), 246–264.Google Scholar
Ohta, H., Yamazaki, S., & McMahon, D. G. (2005). Constant light desynchronizes mammalian clock neurons. Nat Neurosci, 8(3), 267–269.Google Scholar
Okimura, K., Nakane, Y., Nishiwaki-Ohkawa, T., & Yoshimura, T. (2021). Photoperiodic regulation of dopamine signaling regulates seasonal changes in retinal photosensitivity in mice. Sci Rep, 11(1), 1843.Google Scholar
Ono, D., Honma, K. I., & Honma, S. (2021). Roles of neuropeptides, VIP and AVP, in the mammalian central circadian clock. Front Neurosci, 15, 650154.Google Scholar
Ono, D., Mukai, Y., Hung, C. J., Chowdhury, S., Sugiyama, T., & Yamanaka, A. (2020). The mammalian circadian pacemaker regulates wakefulness via CRF neurons in the paraventricular nucleus of the hypothalamus. Sci Adv, 6(45), eabd0384.Google Scholar
Ono, H., Hoshino, Y., Yasuo, S., Watanabe, M., Nakane, Y., Murai, A., Ebihara, S., Korf, H. W., & Yoshimura, T. (2008). Involvement of thyrotropin in photoperiodic signal transduction in mice. PNAS, 105(47), 18238–18242.Google Scholar
Otsuka, T., Goto, M., Kawai, M., Togo, Y., Sato, K., Katoh, K., Furuse, M., & Yasuo, S. (2012). Photoperiod regulates corticosterone rhythms by altered adrenal sensitivity via melatonin-independent mechanisms in Fischer 344 rats and C57Bl/6J mice. PLoS One, 7(6), e39090.Google Scholar
Otsuka, T., Kawai, M., Togo, Y., Goda, R., Kawase, T., Matsuo, H., Iwamoto, A., Nagasawa, M., Furuse, M., & Yasuo, S. (2014). Photoperiodic responses of depression-like behavior, the brain serotonergic system, and peripheral metabolism in laboratory mice. Psychoneuroendocrinology, 40, 37–47.Google Scholar
Ouyang, Y., Andersson, C. R., Kondo, T., Golden, S. S., & Johnson, C. H. (1998). Resonating circadian clocks enhance fitness in Cyanobacteria. PNAS, 95(15), 8660–8664.Google Scholar
Patke, A., Young, M. W., & Axelrod, S. (2020). Molecular mechanisms and physiological importance of circadian rhythms. Nat Rev Mol Cell Biol, 21(2), 67–84.Google Scholar
Patton, A. P., Edwards, M. D., Smyllie, N. J., Hamnett, R., Chesham, J. E., Brancaccio, M., Maywood, E. S., & Hastings, M. H. (2020). The VIP-VPAC2 neuropeptidergic axis is a cellular pacemaking hub of the suprachiasmatic nucleus circadian circuit. Nat Commun, 11(1), 3394.Google Scholar
Paul, S., & Brown, T. (2019). Direct effects of the light environment on daily neuroendocrine control. J Endocrinol, 243(1), R1–R18.Google Scholar
Paul, S., Hanna, L., Harding, C., Hayter, E. A., Walmsley, L., Bechtold, D. A., & Brown, T. M. (2020). Output from VIP cells of the mammalian central clock regulates daily physiological rhythms. Nat Commun, 11(1), 1453.Google Scholar
Perreau-Lenz, S., Kalsbeek, A., Garidou, M. L., Wortel, J., van der Vliet, J., van Heijningen, C., Simonneaux, V., Pevet, P., & Buijs, R. M. (2003). Suprachiasmatic control of melatonin synthesis in rats: Inhibitory and stimulatory mechanisms. Eur J Neurosci, 17(2), 221–228.CrossRefGoogle ScholarPubMed
Pfeffer, M., von Gall, C., Wicht, H., & Korf, H. W. (2022). The role of the melatoninergic system in circadian and seasonal rhythms-insights from different mouse strains. Front Physiol, 13, 883637.Google Scholar
Pfeffer, M., Korf, H. W., & Wicht, H. (2017). The role of the melatoninergic system in light-entrained behavior of mice. Int J Mol Sci, 18(3), 530.CrossRefGoogle ScholarPubMed
Pfeffer, M., Rauch, A., Korf, H. W., & von Gall, C. (2012). The endogenous melatonin (MT) signal facilitates reentrainment of the circadian system to light-induced phase advances by acting upon MT2 receptors. Chronobiol Int, 29(4), 415–429.Google Scholar
Piggins, H. D., Antle, M. C., & Rusak, B. (1995). Neuropeptides phase shift the mammalian circadian pacemaker. J Neurosci, 15(8), 5612–5622.Google Scholar
Pittendrigh, C. S., Elliott, J. A., & Takamura, T. (1984). The circadian component in photoperiodic induction. Ciba Found Symp, 104, 26–47.Google Scholar
Pittendrigh, C. S., & Minis, D. H. (1972). Circadian systems: Longevity as a function of circadian resonance in Drosophila melanogaster. PNAS, 69(6), 1537–1539.Google Scholar
Pohl, H. (1984). Differences in responses of the circadian system to light in the Syrian hamster. Physiol Zool, 57(5), 509–520.Google Scholar
van den Pol, A. N., & Tsujimoto, K. L. (1985). Neurotransmitters of the hypothalamic suprachiasmatic nucleus: Immunocytochemical analysis of 25 neuronal antigens. Neuroscience, 15(4), 1049–1086.Google Scholar
Power, A., Hughes, A. T., Samuels, R. E., & Piggins, H. D. (2010). Rhythm-promoting actions of exercise in mice with deficient neuropeptide signaling. J Biol Rhythms, 25(4), 235–246.Google Scholar
Prendergast, B. J., & Nelson, R. J. (2005). Affective responses to changes in day length in Siberian hamsters (Phodopus sungorus). Psychoneuroendocrinology, 30(5), 438–452.Google Scholar
Pyter, L. M., & Nelson, R. J. (2006). Enduring effects of photoperiod on affective behaviors in Siberian hamsters (Phodopus sungorus). Behav Neurosci, 120(1), 125–134.Google Scholar
Ralph, M. R., & Menaker, M. (1988). A mutation of the circadian system in golden hamsters. Science, 241(4870), 1225–1227.Google Scholar
Reed, H. E., Cutler, D. J., Brown, T. M., Brown, J., Coen, C. W., & Piggins, H. D. (2002). Effects of vasoactive intestinal polypeptide on neurones of the rat suprachiasmatic nuclei in vitro. J Neuroendocrinol, 14(8), 639–646.Google Scholar
Refinetti, R. (2003). Effects of prolonged exposure to darkness on circadian photic responsiveness in the mouse. Chronobiol Int, 20(3), 417–440.Google Scholar
Riemersma-van der Lek, R. F., Swaab, D. F., Twisk, J., Hol, E. M., Hoogendijk, W. J., & Van Someren, E. J. (2008). Effect of bright light and melatonin on cognitive and noncognitive function in elderly residents of group care facilities: A randomized controlled trial. JAMA, 299(22), 2642–2655.Google Scholar
Roberts, D. C., Brebner, K., Vincler, M., & Lynch, W. J. (2002). Patterns of cocaine self-administration in rats produced by various access conditions under a discrete trials procedure. Drug Alcohol Depend, 67(3), 291–299.Google Scholar
Roecklein, K. A., Rohan, K. J., Duncan, W. C., Rollag, M. D., Rosenthal, N. E., Lipsky, R. H., & Provencio, I. (2009). A missense variant (P10l) of the melanopsin (Opn4) gene in seasonal affective disorder. J Affect Disord, 114(1–3), 279–285.Google Scholar
Roecklein, K. A., Wong, P. M., Franzen, P. L., Hasler, B. P., Wood-Vasey, W. M., Nimgaonkar, V. L., Miller, M. A., Kepreos, K. M., Ferrell, R. E., & Manuck, S. B. (2012). Melanopsin gene variations interact with season to predict sleep onset and chronotype. Chronobiol Int, 29(8), 1036–1047.Google Scholar
Rohling, J., Meijer, J. H., VanderLeest, H. T., & Admiraal, J. (2006). Phase differences between SCN neurons and their role in photoperiodic encoding; a simulation of ensemble patterns using recorded single unit electrical activity patterns. J Physiol Paris, 100(5–6), 261–270.Google Scholar
Rohling, J. H., Vanderleest, H. T., Michel, S., Vansteensel, M. J., & Meijer, J. H. (2011). Phase resetting of the mammalian circadian clock relies on a rapid shift of a small population of pacemaker neurons. PLoS One, 6(9), e25437.Google Scholar
Rohr, K. E., Pancholi, H., Haider, S., Karow, C., Modert, D., Raddatz, N. J., & Evans, J. (2019). Seasonal plasticity in GABAa signaling is necessary for restoring phase synchrony in the master circadian clock network. Elife, 8, e49578.Google Scholar
Rosen, L. N., Targum, S. D., Terman, M., Bryant, M. J., Hoffman, H., Kasper, S. F., Hamovit, J. R., Docherty, J. P., Welch, B., & Rosenthal, N. E. (1990). Prevalence of seasonal affective disorder at four latitudes. Psychiatry Res, 31(2), 131–144.Google Scholar
Rosenthal, N. E., Sack, D. A., Carpenter, C. J., Parry, B. L., Mendelson, W. B., & Wehr, T. A. (1985). Antidepressant effects of light in seasonal affective disorder. Am J Psychiatry, 142(2), 163–170.Google Scholar
Rosenthal, N. E., Sack, D. A., Gillin, J. C., Lewy, A. J., Goodwin, F. K., Davenport, Y., Mueller, P. S., Newsome, D. A., & Wehr, T. A. (1984). Seasonal affective disorder. A description of the syndrome and preliminary findings with light therapy. Arch Gen Psychiatry, 41(1), 72–80.Google Scholar
Ruby, N. F., Ibuka, N., Barnes, B. M., & Zucker, I. (1989). Suprachiasmatic nuclei influence torpor and circadian temperature rhythms in hamsters. Am J Physiol, 257(1 Pt 2), R210–R215.Google Scholar
Rupp, A. C., Ren, M., Altimus, C. M., Fernandez, D. C., Richardson, M., Turek, F., Hattar, S., & Schmidt, T. M. (2019). Distinct ipRGC subpopulations mediate light’s acute and circadian effects on body temperature and sleep. Elife, 8, e44358.Google Scholar
Saenz de Miera, C., Sage-Ciocca, D., Simonneaux, V., Pevet, P., & Monecke, S. (2018). Melatonin-independent photoperiodic entrainment of the circannual TSH rhythm in the pars tuberalis of the European hamster. J Biol Rhythms, 33(3), 302–317.Google Scholar
Schaap, J., Albus, H., VanderLeest, H. T., Eilers, P. H., Detari, L., & Meijer, J. H. (2003). Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding. PNAS, 100(26), 15994–15999.Google Scholar
Schwartz, M. D., Congdon, S., & de la Iglesia, H. O. (2010). Phase misalignment between suprachiasmatic neuronal oscillators impairs photic behavioral phase shifts but not photic induction of gene expression. J Neurosci, 30(39), 13150–13156.Google Scholar
Scott, C. J., Jansen, H. T., Kao, C. C., Kuehl, D. E., & Jackson, G. L. (1995). Disruption of reproductive rhythms and patterns of melatonin and prolactin secretion following bilateral lesions of the suprachiasmatic nuclei in the ewe. J Neuroendocrinol, 7(6), 429–443.Google Scholar
Sellix, M. T., Evans, J. A., Leise, T. L., Castanon-Cervantes, O., Hill, D. D., DeLisser, P., Block, G. D., Menaker, M., & Davidson, A. J. (2012). Aging differentially affects the re-entrainment response of central and peripheral circadian oscillators. J Neurosci, 32(46), 16193–16202.Google Scholar
Shan, Y., Abel, J. H., Li, Y., Izumo, M., Cox, K. H., Jeong, B., Yoo, S. H., Olson, D. P., Doyle, F. J., 3rd, & Takahashi, J. S. (2020). Dual-color single-cell imaging of the suprachiasmatic nucleus reveals a circadian role in network synchrony. Neuron, 108(1), 164–179 e167.Google Scholar
Shibata, S., Watanabe, A., Hamada, T., Ono, M., & Watanabe, S. (1994). N-methyl-d-aspartate induces phase shifts in circadian rhythm of neuronal activity of rat SCN in vitro. Am J Physiol, 267(2 Pt 2), R360–R364.Google Scholar
Shirakawa, T., Honma, S., Katsuno, Y., Oguchi, H., & Honma, K. I. (2000). Synchronization of circadian firing rhythms in cultured rat suprachiasmatic neurons. Eur J Neurosci, 12(8), 2833–2838.Google Scholar
Siemann, J. K., Grueter, B. A., & McMahon, D. G. (2021). Rhythms, reward, and blues: Consequences of circadian photoperiod on affective and reward circuit function. Neuroscience, 457, 220–234.Google Scholar
Smyllie, N. J., Chesham, J. E., Hamnett, R., Maywood, E. S., & Hastings, M. H. (2016). Temporally chimeric mice reveal flexibility of circadian period-setting in the suprachiasmatic nucleus. PNAS, 113(13), 3657–3662.Google Scholar
Sonoda, T., Lee, S. K., Birnbaumer, L., & Schmidt, T. M. (2018). Melanopsin phototransduction is repurposed by IPRGC subtypes to shape the function of distinct visual circuits. Neuron, 99(4), 754–767 e754.Google Scholar
Sonoda, T., Li, J. Y., Hayes, N. W., Chan, J. C., Okabe, Y., Belin, S., Nawabi, H., & Schmidt, T. M. (2020). A noncanonical inhibitory circuit dampens behavioral sensitivity to light. Science, 368(6490), 527–531.Google Scholar
Spitschan, M., Santhi, N., Ahluwalia, A., Fischer, D., Hunt, L., Karp, N. A., Levi, F., Pineda-Torra, I., Vidafar, P., & White, R. (2022). Sex differences and sex bias in human circadian and sleep physiology research. Elife, 11, e65419.Google Scholar
Stevenson, T. J., & Prendergast, B. J. (2015). Photoperiodic time measurement and seasonal immunological plasticity. Front Neuroendocrinol, 37, 76–88.CrossRefGoogle ScholarPubMed
Stirland, J. A., Hastings, M. H., Loudon, A. S., & Maywood, E. S. (1996). The tau mutation in the Syrian hamster alters the photoperiodic responsiveness of the gonadal axis to melatonin signal frequency. Endocrinology, 137(5), 2183–2186.Google Scholar
Sumova, A., & Illnerova, H. (1996). Endogenous melatonin signal does not mediate the effect of photoperiod on the rat suprachiasmatic nucleus. Brain Res, 725(2), 281–283.Google Scholar
Sumova, A., Travnickova, Z., Peters, R., Schwartz, W. J., & Illnerova, H. (1995). The rat suprachiasmatic nucleus is a clock for all seasons. PNAS, 92(17), 7754–7758.Google Scholar
Tackenberg, M. C., Hughey, J. J., & McMahon, D. G. (2021). Optogenetic stimulation of VIPergic SCN neurons induces photoperiodic-like changes in the mammalian circadian clock. Eur J Neurosci, 54(9), 7063–7071.Google Scholar
Tahkamo, L., Partonen, T., & Pesonen, A. K. (2019). Systematic review of light exposure impact on human circadian rhythm. Chronobiol Int, 36(2), 151–170.Google Scholar
Terman, M., & Terman, J. S. (1975). Control of the rat’s circadian self-stimulation rhythm by light-dark cycles. Physiol Behav, 14(6), 781–789.Google Scholar
Todd, W. D., Fenselau, H., Wang, J. L., Zhang, R., Machado, N. L., Venner, A., Broadhurst, R. Y., Kaur, S., Lynagh, T., Olson, D. P., Lowell, B. B., Fuller, P. M., & Saper, C. B. (2018). A hypothalamic circuit for the circadian control of aggression. Nat Neurosci, 21(5), 717–724.Google Scholar
Todd, W. D., Venner, A., Anaclet, C., Broadhurst, R. Y., De Luca, R., Bandaru, S. S., Issokson, L., Hablitz, L. M., Cravetchi, O., Arrigoni, E., Campbell, J. N., Allen, C. N., Olson, D. P., & Fuller, P. M. (2020). Suprachiasmatic VIP neurons are required for normal circadian rhythmicity and comprised of molecularly distinct subpopulations. Nat Commun, 11(1), 4410.Google Scholar
Tognini, P., Samad, M., Kinouchi, K., Liu, Y., Helbling, J. C., Moisan, M. P., Eckel-Mahan, K. L., Baldi, P., & Sassone-Corsi, P. (2020). Reshaping circadian metabolism in the suprachiasmatic nucleus and prefrontal cortex by nutritional challenge. PNAS, 117(47), 29904–29913.Google Scholar
Tournier, B. B., Dardente, H., Simonneaux, V., Vivien-Roels, B., Pevet, P., Masson-Pevet, M., & Vuillez, P. (2007). Seasonal variations of clock gene expression in the suprachiasmatic nuclei and pars tuberalis of the European hamster (Cricetus Cricetus). Eur J Neurosci, 25(5), 1529–1536.Google Scholar
Travnickova, Z., Sumova, A., Peters, R., Schwartz, W. J., & Illnerova, H. (1996a). Photoperiod-dependent correlation between light-induced SCN c-Fos expression and resetting of circadian phase. Am J Physiol, 271(4 Pt 2), R825–R831.Google Scholar
Travnickova, Z., Sumova, A., Peters, R., Schwartz, W. J., & Illnerova, H. (1996b). Photoperiod-dependent correlation between light-induced SCN c-Fos expression and resetting of circadian phase. Am J Physiol, 271(4 Pt 2), R825–R831.Google Scholar
Underwood, H., & Goldman, B. D. (1987). Vertebrate circadian and photoperiodic systems: Role of the pineal gland and melatonin. J Biol Rhythms, 2(4), 279–315.Google Scholar
VanderLeest, H. T., Houben, T., Michel, S., Deboer, T., Albus, H., Vansteensel, M. J., Block, G. D., & Meijer, J. H. (2007). Seasonal encoding by the circadian pacemaker of the SCN. Curr Biol, 17(5), 468–473.Google Scholar
VanderLeest, H. T., Rohling, J. H., Michel, S., & Meijer, J. H. (2009). Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization. PLoS One, 4(3), e4976.Google Scholar
Varadarajan, S., Tajiri, M., Jain, R., Holt, R., Ahmed, Q., LeSauter, J., & Silver, R. (2018). Connectome of the suprachiasmatic nucleus: New evidence of the core-shell relationship. eNeuro, 5(5), eneuro.0205-18.Google Scholar
Vosko, A. M., Schroeder, A., Loh, D. H., & Colwell, C. S. (2007). Vasoactive intestinal peptide and the mammalian circadian system. Gen Comp Endocrinol, 152(2–3), 165–175.Google Scholar
Vuillez, P., Jacob, N., Teclemariam-Mesbah, R., & Pevet, P. (1996). In Syrian and European hamsters, the duration of sensitive phase to light of the suprachiasmatic nuclei depends on the photoperiod. Neurosci Lett, 208(1), 37–40.Google Scholar
Wang, T. A., Yu, Y. V., Govindaiah, G., Ye, X., Artinian, L., Coleman, T. P., Sweedler, J. V., Cox, C. L., & Gillette, M. U. (2012). Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science, 337(6096), 839–842.Google Scholar
Weaver, D. R. (1998). The suprachiasmatic nucleus: A 25-year retrospective. J Biol Rhythms, 13(2), 100–112.Google Scholar
Webb, A. B., Angelo, N., Huettner, J. E., & Herzog, E. D. (2009). Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. PNAS, 106(38), 16493–16498.Google Scholar
Wehr, T. (2001). Seasonal photoperiodic responses of the human circadian system. In Takahashi, J., Turek, F., & Moore, R. (eds.), Handbook of behavioral neurobiology: Circadian clocks (Vol. 12, pp. 715–744). New York: Kluwer Academic.Google Scholar
Wehr, T. A., Duncan, W. C. Jr., Sher, L., Aeschbach, D., Schwartz, P. J., Turner, E. H., Postolache, T. T., & Rosenthal, N. E. (2001). A circadian signal of change of season in patients with seasonal affective disorder. Arch Gen Psychiatry, 58(12), 1108–1114.Google Scholar
Weil, Z. M., Borniger, J. C., Cisse, Y. M., Abi Salloum, B. A., & Nelson, R. J. (2015). Neuroendocrine control of photoperiodic changes in immune function. Front Neuroendocrinol, 37, 108–118.Google Scholar
Welsh, D. K., Logothetis, D. E., Meister, M., & Reppert, S. M. (1995). Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron, 14(4), 697–706.Google Scholar
Wen, S., Ma, D., Zhao, M., Xie, L., Wu, Q., Gou, L., Zhu, C., Fan, Y., Wang, H., & Yan, J. (2020). Spatiotemporal single-cell analysis of gene expression in the mouse suprachiasmatic nucleus. Nat Neurosci, 23(3), 456–467.Google Scholar
Wirz-Justice, A. (2018). Seasonality in affective disorders. Gen Comp Endocrinol, 258, 244–249.Google Scholar
Workman, J. L., Manny, N., Walton, J. C., & Nelson, R. J. (2011). Short day lengths alter stress and depressive-like responses, and hippocampal morphology in Siberian hamsters. Horm Behav, 60(5), 520–528.Google Scholar
Xu, L. Z., Liu, L. J., Yuan, M., Li, S. X., Yue, X. D., Lai, J. L., & Lu, L. (2016). Short photoperiod condition increases susceptibility to stress in adolescent male rats. Behav Brain Res, 300, 38–44.Google Scholar
Yamaguchi, S., Isejima, H., Matsuo, T., Okura, R., Yagita, K., Kobayashi, M., & Okamura, H. (2003). Synchronization of cellular clocks in the suprachiasmatic nucleus. Science, 302(5649), 1408–1412.Google Scholar
Yamaguchi, Y., Suzuki, T., Mizoro, Y., Kori, H., Okada, K., Chen, Y., Fustin, J. M., Yamazaki, F., Mizuguchi, N., Zhang, J., Dong, X., Tsujimoto, G., Okuno, Y., Doi, M., & Okamura, H. (2013). Mice genetically deficient in vasopressin V1a and V1b receptors are resistant to jet lag. Science, 342(6154), 85–90.Google Scholar
Yan, L., & Silver, R. (2004). Resetting the brain clock: Time course and localization of mPER1 and mPER2 protein expression in suprachiasmatic nuclei during phase shifts. Eur J Neurosci, 19(4), 1105–1109.Google Scholar
Yan, L., & Silver, R. (2008). Day-length encoding through tonic photic effects in the retinorecipient SCN region. Eur J Neurosci, 28(10), 2108–2115.Google Scholar
Yoshikawa, T., Inagaki, N. F., Takagi, S., Kuroda, S., Yamasaki, M., Watanabe, M., Honma, S., & Honma, K. I. (2017). Localization of photoperiod responsive circadian oscillators in the mouse suprachiasmatic nucleus. Sci Rep, 7(1), 8210.Google Scholar
Yoshikawa, T., Nakajima, Y., Yamada, Y., Enoki, R., Watanabe, K., Yamazaki, M., Sakimura, K., Honma, S., & Honma, K. (2015). Spatiotemporal profiles of arginine vasopressin transcription in cultured suprachiasmatic nucleus. Eur J Neurosci, 42(9), 2678–2689.Google Scholar
Yoshikawa, T., Pauls, S., Foley, N., Taub, A., LeSauter, J., Foley, D., Honma, K. I., Honma, S., & Silver, R. (2021). Phase gradients and anisotropy of the suprachiasmatic network: Discovery of phaseoids. eNeuro, 8(5), eneuro.0078-21.Google Scholar
Young, J. W., Cope, Z. A., Romoli, B., Schrurs, E., Aniek, J., van Enkhuizen, J., Sharp, R. F., & Dulcis, D. (2018). Mice with reduced DAT levels recreate seasonal-induced switching between states in bipolar disorder. Neuropsychopharmacology, 43(8), 1721–1731.Google Scholar
Zhang, C., Clough, S. J., Adamah-Biassi, E. B., Sveinsson, M. H., Hutchinson, A. J., Miura, I., Furuse, T., Wakana, S., Matsumoto, Y. K., Okanoya, K., Hudson, R. L., Kato, T., Dubocovich, M. L., & Kasahara, T. (2021). Impact of endogenous melatonin on rhythmic behaviors, reproduction, and survival revealed in melatonin-proficient C57Bl/6J congenic mice. J Pineal Res, 71(2), e12748.Google Scholar
Zhang, R., Lahens, N. F., Ballance, H. I., Hughes, M. E., & Hogenesch, J. B. (2014). A circadian gene expression atlas in mammals: Implications for biology and medicine. PNAS, 111(45), 16219–16224.Google Scholar
Zhao, X., Hirota, T., Han, X., Cho, H., Chong, L. W., Lamia, K., Liu, S., Atkins, A. R., Banayo, E., Liddle, C., Yu, R. T., Yates, J. R., 3rd, Kay, S. A., Downes, M., & Evans, R. M. (2016). Circadian amplitude regulation via Fbxw7-targeted Rev-erbalpha degradation. Cell, 165(7), 1644–1657.Google Scholar

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