Abstract
Decades have now passed since Colin Pittendrigh first proposed a model of a circadian clock composed of two coupled oscillators, individually responsive to the rising and setting sun, as a flexible solution to the challenge of behavioral and physiological adaptation to the changing seasons. The elegance and predictive power of this postulation has stimulated laboratories around the world in searches to identify and localize such hypothesized evening and morning oscillators, or sets of oscillators, in insects, rodents, and humans, with experimental designs and approaches keeping pace over the years with technological advances in biology and neuroscience. Here, we recount the conceptual origin and highlight the subsequent evolution of this dual oscillator model for the circadian clock in the mammalian suprachiasmatic nucleus; and how, despite our increasingly sophisticated view of this multicellular pacemaker, Pittendrigh’s binary conception has remained influential in our clock models and metaphors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
There is no data included in this manuscript, only schematics and representative images provided by the authors.
References
Barca-Mayo O, Pons-Espinal M, Follert P, Armirotti A, Berdondini L, De Pietri D (2017) Astrocyte deletion of Bmal1 alters daily locootor activity and cognitive functions via GABA signalling. Nat Commun 8:14336. https://doi.org/10.1038/Ncomms14336
Beersma DGM, van Bunnik BAD, Hut RA, Daan S (2008) Emergence of circadian and photoperiodic system level properties from interactions among pacemaker cells. J Biol Rhythms 23:362–373. https://doi.org/10.1177/0748730408317992
Boulos Z, Morin LP (1986) Entrainment of split circadian activity rhythms in hamsters. J Biol Rhythms 1:1–15
Boulos Z, Terman M (1979) Splitting of circadian rhythms in the rat. J Comp Physiol 134:75–83
Brancaccio M, Maywood ES, Chesham JE, Loudon AS, Hastings MH (2013) A Gq-Ca2+ axis controls circuit-level encoding of circadian time in the suprachiasmatic nucleus. Neuron 78:714–728. https://doi.org/10.1016/j.neuron.2013.03.011
Brancaccio M, Patton AP, Chesham JE, Maywood ES, Hastings MH (2017) Astrocytes control circadian timekeeping in the suprachiasmatic nucleus via glutamatergic signaling. Neuron 93:1420–1435. https://doi.org/10.1016/j.neuron.2017.02.030
Brancaccio M, Edwards MD, Patton AP, Smyllie NJ, Chesham JE, Maywood ES, Hastings MH (2019) Cell-autonomous clock of astrocytes drives circadian behavior in mammals. Science 363:187–192. https://doi.org/10.1126/science.aat4104
Brown TM, Piggins HD (2009) Spatiotemporal heterogeneity in the electrical activity of suprachiasmatic nuclei neurons and their response to photoperiod. J Biol Rhythms 24:44–54. https://doi.org/10.1177/0748730408327918
Buijink MR, Almog A, Wit CB, Roethler O, Olde Engberink AHO, Meijer JH, Garlaschelli D, Rohling JHT, Michel S (2016) Evidence for weakened intercellular coupling in the mammalian circadian clock under long photoperiod. PLoS One 11:e0168954. https://doi.org/10.1371/journal.pone.0168954
Burgoon PW, Lindberg PT, Gillette MU (2004) Different patterns of circadian oscillation in the suprachiasmatic nucleus of hamster, mouse, and rat. J Comp Physiol A 190:167–171. https://doi.org/10.1007/s00359-003-0486-z
Daan S, Berde C (1978) Two coupled oscillators: simulations of the circadian pacemaker in mammalian activity rhythms. J Theor Biol 70:297–313
de la Iglesia HO, Meyer J, Carpino A Jr, Schwartz WJ (2000) Antiphase oscillation of the left and right suprachiasmatic nuclei. Science 290:799–801. https://doi.org/10.1126/science.290.5492.799
de la Iglesia HO, Cambras T, Schwartz WJ, Díez-Noguera A (2004a) Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr Biol 14:796–800. https://doi.org/10.1016/j.cub.2004.04.034
de la Iglesia HO, Meyer J, Schwartz WJ (2004b) Using Per gene expression to search for photoperiodic oscillators in the hamster suprachiasmatic nucleus. Molec Brain Res 127:121–127. https://doi.org/10.1016/j.molbrainres.2004.05.018
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, Aizawa S, Kobayashi M, Obrietan K, Tsujimoto G, Okamura H (2011) Circadian regulation of intracellular G-protein signaling mediates intercellular synchrony and rhythmicity in the suprachiasmatic nucleus. Nat Commun 2:327. https://doi.org/10.1038/ncomms1316
Earnest DJ, Turek FW (1982) Splitting of the circadian rhythm of activity in hamsters: effects of exposure to constant darkness and subsequent re-exposure to constant light. J Comp Physiol A 145:405–411
Elliott JA, Tamarkin L (1994) Complex circadian regulation of pineal melatonin and wheel-running in Syrian hamsters. J Comp Physiol A 174:469–484
Enoki R, Kuroda S, Ono D, Hasan MT, Ueda T, Honma S, Honma K (2012) Topological specificity and hierarchical network of the circadian calcium rhythm in the suprachiasmatic nucleus. Proc Natl Acad Sci USA 109:21498–21503. https://doi.org/10.1073/pnas.1214415110
Eskin A (1979) Identification and physiology of circadian pacemakers. Fed Proc Fed Am Soc Exp Biol 38:2570–2572
Evans JA, Leise TL, Castanon-Cervantes O, Davidson AJ (2011) Intrinsic regulation of spatiotemporal organization within the suprachiasmatic nucleus. PLoS One 6:e15869. https://doi.org/10.1371/journal.pone.0015869
Evans JA, Leise TL, Castanon-Cervantes O, Davidson AJ (2013) Dynamic interactions mediated by nonredundant signaling mechanisms couple circadian clock neurons. Neuron 80:973–983. https://doi.org/10.1016/j.neuron.2013.08.022
Farajnia S, van Westering TL, Meijer JH, Michel S (2014) Seasonal induction of GABAergic excitation in the central mammalian clock. Proc Natl Acad Sci USA 111:9627–9632. https://doi.org/10.1073/pnas.1319820111
Foley NC, Tong TY, Foley D, LeSauter J, Welsh DK, Silver R (2011) Characterization of orderly spatiotemporal patterns of clock gene activation in mammalian suprachiasmatic nucleus. Eur J Neurosci 33:1851–1865. https://doi.org/10.1111/j.1460-9568.2011.07682.x
Fujiwara Y, Hermann-Luibl C, Katsura M, Sekiguchi M, Ida T, Helfrich-Förster C, Yoshii T (2018) The CCHamide1 neuropeptide expressed in the anterior dorsal neuron 1 conveys a circadian signal to the ventral lateral neurons in Drosophila melanogaster. Front Physiol 9:1276. https://doi.org/10.3389/fphys.2018.01276
Grima B, Chélot E, Xia R, Rouyer F (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431:869–873. https://doi.org/10.1038/nature02935
Hamnett R, Crosby P, Chesham JE, Hastings MH (2019) Vasoactive intestinal peptide controls the suprachiasmatic circadian clock network via ERK1/2 and DUSP4 signalling. Nat Commun 10:542. https://doi.org/10.1038/s41467-019-08427-3
Harrington ME, Eskes GA, Dickson P, Rusak B (1990) Lesions dorsal to the suprachiasmatic nuclei abolish split activity rhythms of hamsters. Brain Res Bull 24:593–597
Hastings MH, Walker AP, Herbert J (1987) Effect of asymmetrical reductions of photoperiod on pineal melatonin, locomotor activity and gonadal condition of male Syrian hamsters. J Endocrinol 114:221–229
Hastings MH, Maywood ES, Brancaccio M (2018) Generation of circadian rhythms in the suprachiasmatic nucleus. Nat Rev Neurosci 19:453–469. https://doi.org/10.1038/s41583-018-0026-z
Hazlerigg DG, Ebling FJ, Johnston JD (2005) Photoperiod differentially regulates gene expression rhythms in the rostral and caudal SCN. Curr Biol 15:R449-450. https://doi.org/10.1016/j.cub.2005.06.010
Herzog ED, Takahashi JS, Block GD (1998) Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat Neurosci 1:708–713. https://doi.org/10.1038/3708
Hoffmann K (1971) Splitting of the circadian rhythm as a function as a function of light intensity. In: Menaker M (ed) Biochronometry. National Academy of Sciences, Washington D.C., pp 134–150
Honma K, Honma S, Hiroshige T (1985) Response curve, free-running period, and activity time in circadian locomotor rhythm of rats. Jpn J Physiol 35:643–658
Honma S, Shirakawa T, Katsuno Y, Namihira M, Honma K (1998) Circadian periods of single suprachiasmatic neurons in rats. Neurosci Lett 250:157–160. https://doi.org/10.1016/s0304-3940(98)00464-9
Houben T, Deboer T, Van OF, Meijer JH (2009) Correlation with behavioral activity and rest implies circadian regulation by SCN neuronal activity levels. J Biol Rhythms 24:477–487. https://doi.org/10.1177/0748730409349895
Illnerová H, Vanĕček J (1982) Two-oscillator structure of the pacemaker controlling the circadian rhythm of N-acetyltransferase in the rat pineal gland. J Comp Physiol A 145:539–548
Inagaki N, Honma S, Ono D, Tanahashi Y, Honma K (2007) Separate oscillating cell groups in mous suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci USA 104:7664–7669. https://doi.org/10.1073/pnas.0607713104
Jagota A, de la Iglesia HO, Schwartz WJ (2000) Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro. Nat Neurosci 3:372–376. https://doi.org/10.1038/73943
Johnston JD (2005) Measuring seasonal time within the circadian system: regulation of the suprachiasmatic nuclei by photoperiod. J Neuroendocrinol 17:459–465. https://doi.org/10.1111/j.1365-2826.2005.01326.x
Joye DAM, Rohr KE, Suenkens K, Wuorinen A, Inda T, Arzbecker M, Mueller E, Huber A, Pancholi H, Blackmore MG, Carmona-Alcocer V, Evans JA (2023) Somatostatin regulates central clock function and circadian responses to light. Proc Natl Acad Sci 120(18):e2216820120. https://doi.org/10.1073/pnas.2216820120
Kim S, McMahon DG (2021) Light sets the brain’s daily clock by regional quickening and slowing of the molecular clockworks at dawn and dusk. Elife 10:e70137. https://doi.org/10.7554/eLife.70137
Koinuma S, Asakawa T, Nagano M, Furukawa K, Sujino M, Masumoto K-H, Nakajima Y, Hashimoto S, Yagita K, Shigeyoshi Y (2013) Regional circadian period difference in the suprachiasmatic nucleus of the mammalian circadian center. Eur J Neurosci 38:2832–2841. https://doi.org/10.1111/ejn.12308
Lees JG, Hallonquist JD, Mrosovsky N (1983) Differential effects of dark pulses on the two components of split circadian activity rhythms in golden hamsters. J Comp Physiol A 153:123–132
Liang X, Holy TE, Taghert PH (2016) Synchronous Drosophila circadian pacemakers display nonsynchronous Ca2+ rhythms in vivo. Science 351:976–981. https://doi.org/10.1126/science.aad3997
Liang X, Holy TE, Taghert PH (2017) A series of suppressive signals within the Drosophila circadian neural circuit generates sequential daily outputs. Neuron 94:1173–1189. https://doi.org/10.1016/j.neuron.2017.05.007
Lucassen EA, van Diepen HC, Houben T, Michel S, Colwell CS, Meijer JH (2012) Role of vasoactive intestinal peptide in seasonal encoding by the suprachiasmatic nucleus clock. Eur J Neurosci 35:1466–1474. https://doi.org/10.1111/j.1460-9568.2012.08054.x
Maywood ES, Drynan L, Chesham JE, Edwards MD, Dardente H, Fustin JM, Hazlerigg DG, O’Neill JS, Codner GF, Smyllie NJ, Brancaccio M, Hastings MH (2013) Analysis of core circadian feedback loop in suprachiasmatic nucleus of mCry1-luc transgenic reporter mouse. Proc Natl Acad Sci USA 110:9547–9552. https://doi.org/10.1073/pnas.1220894110
McManus D, Polidarova L, Smyllie NJ, Patton AP, Chesham JE, Maywood ES, Chin JW, Hastings MH (2022) Cryptochrome 1 as a state variable of the circadian clockwork of the suprachiasmatic nucleus: evidence from translational switching. Proc Natl Acad Sci USA 119:e2203563119. https://doi.org/10.1073/pnas.2203563119
Meijer JH, De Vries MJ (1995) Light-induced phase shifts in onset and offset of running-wheel activity in the Syrian hamster. J Biol Rhythms 10:4–16
Meijer JH, Daan S, Overkamp GJF, Hermann PM (1990) The two-oscillator circadian system of tree shrews (Tupaia belangeri) and its response to light and dark pulses. J Biol Rhythms 5:1–16
Mieda M, Okamoto H, Sakurai T (2016) Manipulating the cellular circadian period of arginine vasopressin neurons alters the behavioral circadian period. Curr Biol 26:2535–2542. https://doi.org/10.1016/j.cub.2016.07.022
Moore RY, Speh JC, Leak RK (2002) Suprachiasmatic nucleus organization. Cell Tissue Res 309:89–98. https://doi.org/10.1007/s00441-002-0575-2
Morin LP, Cummings LA (1982) Splitting of wheelrunning rhythms by castrated or steroid treated male and female hamsters. Physiol Behav 29:665–675
Morris EL, Patton AP, Chesham JE, Crisp A, Adamson A, Hastings MH (2021) Single-cell transcriptomics of suprachiasmatic nuclei reveal a Prokineticin-driven circadian network. Embo J 40:e108614. https://doi.org/10.15252/embj.2021108614
Mrugala M, Zlomanczuk P, Jagota A, Schwartz WJ (2000) Rhythmic multiunit neural activity in slices of hamster suprachiasmatic nucleus reflect prior photoperiod. Am J Physiol 278:R987–R994. https://doi.org/10.1152/ajpregu.2000.278.4.R987
Myung J, Hong S, DeWoskin D, De Schutter E, Forger DB, Takumi T (2015) GABA-mediated repulsive coupling between circadian clock neurons in the SCN encodes seasonal time. Proc Acad Sci USA 112:E3920–E3929. https://doi.org/10.1073/pnas.1421200112
Naito E, Watanabe T, Tei H, Yoshimura T, Ebihara S (2008) Reorganization of the suprachiasmatic nucleus coding for day length. J Biol Rhythms 23:140–149. https://doi.org/10.1177/0748730408314572
Nakamura W, Honma S, Shirakawa T, Honma K (2001) Regional pacemakers composed of multiple oscillator neurons in the rat suprachiasmatic nucleus. Eur J Neurosci 14:666–674. https://doi.org/10.1046/j.0953-816x.2001.01684.x
Nave C, Roberts L, Hwu P, Estrella JD, Vo TC, Nguyen TH, Bui TT, Rindner DJ, Pervolarakis N, Shaw PJ, Leise TL, Holmes TC (2021) Weekend light shifts evoke persistent Drosophila circadian neural network desynchrony. J Neurosci 41:5173–5189. https://doi.org/10.1523/JNEUROSCI.3074-19.2021
Ohta H, Yamazaki S, McMahon DG (2005) Constant light desynchronizes mammalian clock neurons. Nat Neurosci 8:267–269. https://doi.org/10.1203/01.pdr.0000233114.18403.66
Patton AP, Edwards MD, Smyllie NJ, Hamnett R, Chesham JE, Brancaccio M, Maywood ES, Hastings MH (2020) The VIP-VPAC2 neuropeptidergic axis is a cellular pacemaking hub of the suprachiasmatic nucleus circadian circuit. Nat Commun 11:3394. https://doi.org/10.1038/s41467-020-17110-x
Perini L (2005) Explanation in two dimensions: diagrams and biological explanation. Biol Philos 20:257–269. https://doi.org/10.1007/s10539-005-2562-y
Pickard GE, Turek FW (1982) Splitting of the circadian rhythm of activity is abolished by unilateral lesions of the suprachiasmatic nuclei. Science 215:1119–1121
Pickard GE, Kahn R, Silver R (1984) Splitting of the circadian rhythm of body temperature in the golden hamster. Physiol Behav 32:763–766
Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harbor Symp Quant Biol 25:159–184
Pittendrigh CS (1967) Circadian rhythms space research and manned space flight. Life sciences and space research V. North Holland Publishing Co, Amsterdam, pp 122–134
Pittendrigh CS (1974) Circadian oscillations in cells and the circadian organization of multicellular systems. In: Schmitt FO, Worden FG (eds) The neurosciences: third study program. MIT Press, Cambridge, pp 437–458
Pittendrigh CS, Bruce VG (1957) An oscillator model for biological clocks. In: Rudnick D (ed) Rhythmic and synthetic processes in growth. Princeton University Press, New Jersey, pp 75–109
Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: a clock for all seasons. J Comp Physiol A 106:333–355
Porcu A, Nilsson A, Booreddy S, Barnes SA, Welsh DK, Dulcis D (2022) Seasonal changes in day length induce multisynaptic neurotransmitter switching to regulate hypothalamic network activity and behavior. Sci Adv 8(35):eabn9867. https://doi.org/10.1126/sciadv.abn9867
Reinhard N, Schubert FK, Bertolini E, Hagedorn N, Manoli G, Sekiguchi M, Yoshii T, Rieger D, Helfrich-Förster C (2022) The neuronal circuit of the dorsal circadian clock neurons in Drosophila melanogaster. Front Physiol 13:886432. https://doi.org/10.3389/fphys.2022.886432
Rohr KE, Pancholi H, Haider S, Karow C, Modert D, Raddatz NJ, Evans J (2019) Seasonal plasticity in GABAA signaling is necessary for restoring phase synchrony in the master circadian clock network. Elife 8:e49578. https://doi.org/10.7554/eLife.49578
Schaap J, Albus H, VanderLeest HT, Eilers PH, Detari L, Meijer JH (2003) Heterogeneity of rhythmic suprachiasmatic nucleus neurons: implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci USA 100:15994–15999. https://doi.org/10.1073/pnas.2436298100
Shafer OT, Gutierrez GJ, Li K, Mildenhall A, Spira D, Marty J, Lazar AA, de la Paz FM (2022) Connectomic analysis of the Drosophila lateral neuron clock cells reveals the synaptic basis of functional pacemaker classes. Elife 11:e79139. https://doi.org/10.7554/eLife.79139
Shan Y, Abel JH, Li Y, Izumo M, Cox KH, Jeong B, Yoo S-H, Olson DP, Doyle FJ III, Takahashi JS (2020) Dual-color single-cell imaging of the suprachiasmatic nucleus reveals a circadian role in network synchrony. Neuron 108:164–179. https://doi.org/10.1016/j.neuron.2020.07.012
Shibuya CA, Melnyk RB, Mrosovsky N (1980) Simultaneous splitting of drinking and locomotor activity rhythms in a golden hamster. Naturwissenschaften 67:S45
Shinohara K, Honma S, Katsuno Y, Abe H, Honma K (1995) Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc Natl Acad Sci USA 92:7396–7400
Smyllie NJ, Chesham JE, Hamnett R, Maywood ES, Hastings MH (2016) Temporally chimeric mice reveal flexibility of circadian period-setting in the suprachiasmatic nucleus. Proc Natl Acad Sci USA 113:3657–3662. https://doi.org/10.1073/pnas.1511351113
Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behavior of Drosophila. Nature 431:862–868
Stoleru D, Peng Y, Nawathean P, Rosbash M (2005) A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438:238–242. https://doi.org/10.1038/nature02926
Sumová A, Trávnicková Z, Peters R, Schwartz WJ, Illnerová H (1995) The rat suprachiasmatic nucleus is a clock for all seasons. Proc Natl Acad Sci USA 92:7754–7758
Swann J, Turek FW (1982) Cycle of lordosis behavior in female hamsters whose circadian activity rhythm has split into two components. Am J Physiol 243:R112–R118
Swann J, Turek FW (1985) Multiple circadian oscillators regulate the timing of behavioral and endocrine rhythms in female golden hamsters. Science 228:898–900
Tavakoli-Nezhad M, Schwartz WJ (2005) c-Fos expression in the brains of behaviorally “split” hamsters in constant light: calling attention to a dorsolateral region of the suprachiasmatic nucleus and the medial division of the lateral habenula. J Biol Rhythms 20:419–429. https://doi.org/10.1177/0748730405278443
Todd WD, Venner A, Anaclet C, Broadhurst RY, De Luca R, Bandaru SS, Issokson L, Hablitz LM, Cravetchi O, Arrigoni E, Campbell JN, Allen CN, Olson DP, Fuller PM (2020) Suprachiasmatic VIP neurons are required for normal circadian rhythmicity and comprised of molecularly distinct subpopulations. Nat Commun 11:4410. https://doi.org/10.1038/s41467-020-17197-2
Tso CF, Simon T, Greenlaw AC, Puri T, Mieda M, Herzog ED (2017) Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behavior. Curr Biol 27:1055–1061. https://doi.org/10.1016/j.cub.2017.02.037
VanderLeest HT, Houben T, Michel S, Deboer T, Albus H, Vansteensel MJ, Block GD, Meijer JH (2007) Seasonal encoding by the circadian pacemaker of the SCN. Curr Biol 17:468–473. https://doi.org/10.1016/j.cub.2007.01.048
Vosko AM, Schroeder A, Loh DH, Colwell CS (2007) Vasoactive intestinal peptide and the mammalian circadian system. Gen Comp Endrocrinol 152:165–175. https://doi.org/10.1016/j.ygcen.2007.04.018
Vuillez P, Jacob N, Teclemariam-Mesbah T, Pévet P (1996) In Syrian and European hamsters, the duration of sensitive phase to light of the suprachiasmatic nuclei depends on the photoperiod. Neurosci Lett 208:37–40. https://doi.org/10.1016/0304-3940(96)12535-0
Welsh DK, Logothetis DE, Meister M, Reppert SM (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697–706
Wen S, Ma DM, 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 23:456–467. https://doi.org/10.1038/s41593-020-0586-x
Xie L, Xiong Y, Ma D, Shi K, Chen J, Yang Q, Yan J (2023) Cholecystokinin neurons in mouse suprachiasmatic nucleus regulate the robustness of circadian clock. Neuron. https://doi.org/10.1016/j.neuron.2023.04.016
Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, Kobayashi M, Okamura H (2003) Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302:1408–1412. https://doi.org/10.1126/science.1089287
Yan L, Silver R (2008) Day-length encoding through tonic photic effects in the retinorecipient SCN region. Eur J Neurosci 28:2108–2115. https://doi.org/10.1111/j.1460-9568.2008.06493.x
Yan L, Foley NC, Bobula JM, Kriegsfeld LJ, Silver R (2005) Two antiphase oscillations occur in each suprachiasmatic nucleus of behaviorally split hamsters. J Neurosci 25:9017–9026. https://doi.org/10.1523/JNEUROSCI.2538-05.2005
Yao Z, Shafer OT (2014) The Drosophila circadian clock is a variably coupled network of multiple peptidergic units. Science 343:1516–1520. https://doi.org/10.1126/science.1251285
Yao Z, Bennett AJ, Clem J, Shafer OT (2016) The Drosophila clock neuron network features diverse coupling modes and requires network-wide coherence for robust circadian rhythms. Cell Rep 17:2873–2881. https://doi.org/10.1016/j.celrep.2016.11.053
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 42:2678–2689. https://doi.org/10.1111/ejn.13061
Yoshikawa T, Inagaki NF, Takagi S, Kuroda S, Yamasaki M, Watanabe M, Honma S, Honma K (2017) Localization of photoperiod responsive circadian oscillators in the mouse suprachiasmatic nucleus. Sci Rep 7:8210. https://doi.org/10.1038/s41598-017-08186-5
Yoshikawa T, Pauls S, Foley N, Taub A, LeSauter J, Foley D, Honma K, Honma S, Silver R (2021) Phase gradients and anisotropy of the suprachiasmatic network: discovery of phaseoids. eNeuro 8(5):ENEURO.0078-21.2021. https://doi.org/10.1523/ENEURO.0078-21.2021
Acknowledgements
We thank Dr. Orie Shafer for helpful discussions. JAE acknowledges support from the National Institutes of Health (R01GM143545).
Author information
Authors and Affiliations
Contributions
WJS and JAE wrote the article, produced figures, and reviewed the final work together.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Dirk Rieger.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Evans, J.A., Schwartz, W.J. On the origin and evolution of the dual oscillator model underlying the photoperiodic clockwork in the suprachiasmatic nucleus. J Comp Physiol A (2023). https://doi.org/10.1007/s00359-023-01659-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00359-023-01659-1