Daily and seasonal adaptation of the circadian clock requires plasticity of the SCN neuronal network
Abstract
Circadian rhythms are an essential property of many living organisms, and arise from an internal pacemaker, or clock. In mammals, this clock resides in the suprachiasmatic nucleus (SCN) of the hypothalamus, and generates an intrinsic circadian rhythm that is transmitted to other parts of the CNS. We will review the evidence that basic adaptive functions of the circadian system rely on functional plasticity in the neuronal network organization, and involve a change in phase relation among oscillatory neurons. We will illustrate this for: (i) photic entrainment of the circadian clock to the light–dark cycle; and (ii) seasonal adaptation of the clock to changes in day length. Molecular studies have shown plasticity in the phase relation between the ventral and dorsal SCN during adjustment to a shifted environmental cycle. Seasonal adaptation relies predominantly on plasticity in the phase relation between the rostral and caudal SCN. Electrical activity is integrated in the SCN, and appears to reflect the sum of the differently phased molecular expression patterns. While both photic entrainment and seasonal adaptation arise from a redistribution of SCN oscillatory activity patterns, different neuronal coupling mechanisms are employed, which are reviewed in the present paper.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Pacemaker cells in the suprachiasmatic nucleus of the hypothalamus are organized in separate networks.
“Pacemaker cells, which individually generate circadian rhythms in the suprachiasmatic nucleus of the hypothalamus, are organized in separate networks16.”
From Bipolar mood cycles associated with lunar entrainment of a circadian rhythm (2018) · cites this paper as [16]
Cites
Geometrical Methods in the Theory of Ordinary Differential Equations
Arnold, V. I. (1988) · Grundlehren der mathematischen Wissenschaften · doi:10.1007/978-1-4612-1037-5 · Cited by 2,571 · see citing works
The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation
Rivera, C., Voipio, J., Payne, J. A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., Pirvola, U., Saarma, M., & Kaila, K. (1999) · Nature · doi:10.1038/16697 · Cited by 2,152 · see citing works
Resetting central and peripheral circadian oscillators in transgenic rats
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R.-I., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M., & Tei, H. (2000) · Science · doi:10.1126/science.288.5466.682 · Cited by 1,907 · see citing works
The genetics of mammalian circadian order and disorder: implications for physiology and disease
Takahashi, J. S., Hong, H.-K., Ko, C. H., & McDearmon, E. L. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2430 · Cited by 1,611 · see citing works
Welsh, D. K., Logothetis, D., Meister, M., & Reppert, S. (1995) · Neuron · doi:10.1016/0896-6273(95)90214-7 · Cited by 1,535 · see citing works
The Geometry of Biological Time
Winfree, A. T. (2001) · Interdisciplinary applied mathematics · doi:10.1007/978-1-4757-3484-3 · Cited by 1,242 · see citing works
Suprachiasmatic Nucleus: Cell Autonomy and Network Properties
Welsh, D. K., Takahashi, J. S., & Kay, S. A. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135919 · Cited by 1,216 · see citing works
GABA: an excitatory transmitter in early postnatal life
Cherubini, E., Gaïarsa, J., & Ben‐Ari, Y. (1991) · Trends in Neurosciences · doi:10.1016/0166-2236(91)90003-d · Cited by 1,108 · see citing works
Synchronization of Cellular Clocks in the Suprachiasmatic Nucleus
Yamaguchi, S., Isejima, H., Matsuo, T., Okura, R., Yagita, K., Kobayashi, M., & Okamura, H. (2003) · Science · doi:10.1126/science.1089287 · Cited by 934 · see citing works
Abrahamson, E. E., & Moore, R. Y. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02890-6 · Cited by 788 · see citing works
The circadian visual system, 2005
Morin, L. P., & Allen, C. N. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2005.08.003 · Cited by 786 · see citing works
When inhibition not excitation synchronizes neural firing
van Vreeswijk, C., Abbott, L. F., & Ermentrout, G. B. (1994) · Journal of Computational Neuroscience · doi:10.1007/bf00961879 · Cited by 780 · see citing works
Goldman, B. D. (2001) · Journal of Biological Rhythms · doi:10.1177/074873001129001980 · Cited by 771 · see citing works
Aton, S. J., Colwell, C. S., Harmar, A. J., Waschek, J. A., & Herzog, E. D. (2005) · Nature Neuroscience · doi:10.1038/nn1419 · Cited by 764 · see citing works
Intercellular Coupling Confers Robustness against Mutations in the SCN Circadian Clock Network
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., et al. (2007) · Cell · doi:10.1016/j.cell.2007.02.047 · Cited by 694 · see citing works
Ionic basis of GABAA receptor channel function in the nervous system
Kaila, K. (1994) · Progress in Neurobiology · doi:10.1016/0301-0082(94)90049-3 · Cited by 670 · see citing works
Resetting the Biological Clock: Mediation of Nocturnal Circadian Shifts by Glutamate and NO
Ding, J., Chen, D., Weber, E. T., Faiman, L. E., Rea, M. A., & Gillette, M. U. (1994) · Science · doi:10.1126/science.7527589 · Cited by 563 · see citing works
Circadian Systems: Entrainment
Pittendrigh, C. S. (1981) · Springer eBooks · doi:10.1007/978-1-4615-6552-9_7 · Cited by 556 · see citing works
The VPAC2 Receptor Is Essential for Circadian Function in the Mouse Suprachiasmatic Nuclei
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., et al. (2002) · Cell · doi:10.1016/s0092-8674(02)00736-5 · Cited by 549 · see citing works
Suprachiasmatic nucleus organization
Moore, R. Y., Speh, J. C., & Leak, R. K. (2002) · Cell and Tissue Research · doi:10.1007/s00441-002-0575-2 · Cited by 547 · see citing works
Orchestrating time: arrangements of the brain circadian clock
Antle, M. C., & Silver, R. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.01.003 · Cited by 463 · see citing works
Maywood, E. S., Reddy, A. B., Wong, G. K. Y., O'Neill, J. S., O'Brien, J. A., McMahon, D. G., Harmar, A. J., Okamura, H., & Hastings, M. H. (2006) · Current Biology · doi:10.1016/j.cub.2006.02.023 · Cited by 438 · see citing works
Chronic jet-lag increases mortality in aged mice
Davidson, A. J., Sellix, M. T., Daniel, J., Yamazaki, S., Menaker, M., & Block, G. D. (2006) · Current Biology · doi:10.1016/j.cub.2006.09.058 · Cited by 427 · see citing works
Disrupted circadian rhythms in VIP- and PHI-deficient mice
Colwell, C. S., Michel, S. H., Itri, J. N., Rodriguez, W. I., Nguyen‐Van‐Tam, J. S., Lelièvre, V., Hu, Z., Liu, X., & Waschek, J. A. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00200.2003 · Cited by 384 · see citing works
Self-citationGABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity
Wagner, S., Castel, M., Gainer, H., & Yarom, Y. (1997) · Nature · doi:10.1038/42468 · Cited by 370 · see citing works
GABA Synchronizes Clock Cells within the Suprachiasmatic Circadian Clock
Liu, C., & Reppert, S. M. (2000) · Neuron · doi:10.1016/s0896-6273(00)80876-4 · Cited by 340 · see citing works
Albus, H., Vansteensel, M. J., Michel, S. H., Block, G. D., & Meijer, J. H. (2005) · Current Biology · doi:10.1016/j.cub.2005.03.051 · Cited by 328 · see citing works
Self-citationCard, J. P., & Moore, R. Y. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90240-9 · Cited by 321 · see citing works
Nelson, D. E., & Takahashi, J. S. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018660 · Cited by 316 · see citing works
A functional analysis of circadian pacemakers in nocturnal rodents
Daan, S., & Pittendrigh, C. S. (1976) · Journal of Comparative Physiology A · doi:10.1007/bf01417858 · Cited by 301 · see citing works
Inagaki, N., Honma, S., Ono, D., Tanahashi, Y., & Honma, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607713104 · Cited by 274 · see citing works
An Abrupt Shift in the Day/Night Cycle Causes Desynchrony in the Mammalian Circadian Center
Nagano, M., Adachi, A. A., Nakahama, K., Nakamura, T., Tamada, M., Meyer-Bernstein, E. L., Sehgal, A., & Shigeyoshi, Y. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-14-06141.2003 · Cited by 273 · see citing works
Seasonal Encoding by the Circadian Pacemaker of the SCN
vanderLeest, H. T., Houben, T., Michel, S. H., Deboer, T., Albus, H., Vansteensel, M. J., Block, G. D., & Meijer, J. H. (2007) · Current Biology · doi:10.1016/j.cub.2007.01.048 · Cited by 253 · see citing works
Self-citationMorning and evening circadian oscillations in the suprachiasmatic nucleus in vitro
Jagota, A., de la Iglesia, H. O., & Schwartz, W. J. (2000) · Nature Neuroscience · doi:10.1038/73943 · Cited by 246 · see citing works
Clock genes, oscillators, and cellular networks in the suprachiasmatic nuclei
Hastings, M. H., & Herzog, E. D. (2004) · Journal of Biological Rhythms · doi:10.1177/0748730404268786 · Cited by 246 · see citing works
Yan, L., Takekida, S., Shigeyoshi, Y., & Okamura, H. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00223-7 · Cited by 237 · see citing works
Forced Desynchronization of Dual Circadian Oscillators within the Rat Suprachiasmatic Nucleus
de la Iglesia, H. O., Cambras, T., Schwartz, W. J., & Dı́ez-Noguera, A. (2004) · Current Biology · doi:10.1016/j.cub.2004.04.034 · Cited by 236 · see citing works
Reddy, A. B., Field, M. D., Maywood, E. S., & Hastings, M. H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07326.2002 · Cited by 220 · see citing works
Luminance coding in a circadian pacemaker: the suprachiasmatic nucleus of the rat and the hamster
Meijer, J. H., Groos, G. A., & Rusak, B. (1986) · Brain Research · doi:10.1016/0006-8993(86)90117-4 · Cited by 220 · see citing works
Self-citationNeuropeptides phase shift the mammalian circadian pacemaker
Piggins, H. D., Antle, M. C., & Rusak, B. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05612.1995 · Cited by 219 · see citing works
Schaap, J., Albus, H., vanderLeest, H. T., Eilers, P. H. C., Détári, L., & Meijer, J. H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2436298100 · Cited by 216 · see citing works
Self-citationElectrical synapses coordinate activity in the suprachiasmatic nucleus
Long, M. A., Jutras, M. J., Connors, B. W., & Burwell, R. D. (2004) · Nature Neuroscience · doi:10.1038/nn1361 · Cited by 194 · see citing works
Vasoactive intestinal peptide and the mammalian circadian system
Vosko, A. M., Schroeder, A., Loh, D. H., & Colwell, C. S. (2007) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2007.04.018 · Cited by 183 · see citing works
Ibata, Y., Takahashi, Y., Okamura, H., Kawakami, F., Terubayashi, H., Kubo, T., & Yanaihara, N. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90129-8 · Cited by 182 · see citing works
Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system
Davidson, A. J., Castanon‐Cervantes, O., Leise, T. L., Molyneux, P. C., & Harrington, M. E. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06534.x · Cited by 171 · see citing works
Excitatory Actions of GABA in the Suprachiasmatic Nucleus
Choi, H. J., Lee, C. J., Schroeder, A., Kim, Y. S., Jung, S. H., Kim, J. S., Kim, D. Y., Son, E. J., Han, H. C., Hong, S. K., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5750-07.2008 · Cited by 167 · see citing works
GABA and G i/o differentially control circadian rhythms and synchrony in clock neurons
Aton, S. J., Huettner, J. E., Straume, M., & Herzog, E. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607466103 · Cited by 156 · see citing works
Pittendrigh, C. S., Kyner, W. T., & Takamura, T. (1991) · Journal of Biological Rhythms · doi:10.1177/074873049100600402 · Cited by 155 · see citing works
Electrophysiology of the suprachiasmatic circadian clock
Brown, T. M., & Piggins, H. D. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.05.002 · Cited by 152 · see citing works
Kuhlman, S. J., Silver, R., LeSauter, J., Bult‐Ito, A., & McMahon, D. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01441.2003 · Cited by 142 · see citing works
Nuesslein‐Hildesheim, B., O’Brien, J., Ebling, F. J. P., Maywood, E. S., & Hastings, M. H. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00173.x · Cited by 141 · see citing works
Vasoactive intestinal polypeptide (VIP) phase‐shifts the rat suprachiasmatic nucleus clock in vitro
Reed, H. E., Meyer‐Spasche, A., Cutler, D. J., et al. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2000.01437.x · Cited by 139 · see citing works
The regulation of seasonal changes in food intake and body weight
Ebling, F. J. P., & Barrett, P. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01721.x · Cited by 139 · see citing works
Rhythmic coupling among cells in the suprachiasmatic nucleus
Colwell, C. S. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(20000615)43:4 · Cited by 139 · see citing works
New Insights into Ancient Seasonal Life Timers
Hazlerigg, D. G., & Loudon, A. S. I. (2008) · Current Biology · doi:10.1016/j.cub.2008.07.040 · Cited by 138 · see citing works
Yan, L., & Silver, R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03189.x · Cited by 136 · see citing works
Resetting of central and peripheral circadian oscillators in aged rats
Davidson, A. J., Yamazaki, S., Arble, D. M., Menaker, M., & Block, G. D. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.10.018 · Cited by 134 · see citing works
Selective deficits in the circadian light response in mice lacking PACAP
Colwell, C. S., Michel, S. H., Itri, J. N., Rodriguez, W., Tam, J., Lelièvre, V., Hu, Z., & Waschek, J. A. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00268.2004 · Cited by 127 · see citing works
Self-citationPhenotype Matters: Identification of Light-Responsive Cells in the Mouse Suprachiasmatic Nucleus
Karatsoreos, I. N., Yan, L., LeSauter, J., & Silver, R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1666-03.2004 · Cited by 121 · see citing works
Lee, M. L., Swanson, B. E., & de la Iglesia, H. O. (2009) · Current Biology · doi:10.1016/j.cub.2009.03.051 · Cited by 120 · see citing works
Differential Response of Period 1 Expression within the Suprachiasmatic Nucleus
Nakamura, W. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0889-05.2005 · Cited by 118 · see citing works
Mrugała, M. M., Złomańczuk, P., Jagota, A., & Schwartz, W. J. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.278.4.r987 · Cited by 115 · see citing works
The visual properties of rat and cat suprachiasmatic neurones
Groos, G. A., & Mason, R. J. (1980) · Journal of Comparative Physiology A · doi:10.1007/bf00657651 · Cited by 112 · see citing works
Brown, T. M., Colwell, C. S., Waschek, J. A., & Piggins, H. D. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01206.2006 · Cited by 109 · see citing works
Neuropeptide Y and glutamate block each other's phase shifts in the suprachiasmatic nucleus in vitro
Biello, S. M., Golombek, D. A., & Harrington, M. E. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00547-7 · Cited by 106 · see citing works
Sumová, A., Jáč, M., Sládek, M., Šauman, I., & Illnerová, H. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730403251801 · Cited by 104 · see citing works
Shibata, S., Watanabe, A., Hamada, T., et al. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.267.2.r360 · Cited by 103 · see citing works
vanderLeest, H. T., Rohling, J. H. T., Michel, S. H., & Meijer, J. H. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004976 · Cited by 102 · see citing works
Self-citationPhotoperiod differentially regulates gene expression rhythms in the rostral and caudal SCN
Hazlerigg, D. G., Ebling, F. J. P., & Johnston, J. D. (2005) · Current Biology · doi:10.1016/j.cub.2005.06.010 · Cited by 101 · see citing works
Gastrin-Releasing Peptide Phase-Shifts Suprachiasmatic Nuclei Neuronal RhythmsIn Vitro
McArthur, A. J., Coogan, A. N., Ajpru, S., Sugden, D., Biello, S. M., & Piggins, H. D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-14-05496.2000 · Cited by 101 · see citing works
Schwartz, W. J., Carpino, A., de la Iglesia, H. O., Baler, R., Klein, D. C., Nakabeppu, Y., & D, N. A. M. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00140-8 · Cited by 98 · see citing works
Shibata, S., & Moore, R. Y. (1993) · Brain Research · doi:10.1016/0006-8993(93)91118-c · Cited by 98 · see citing works
Reorganization of the Suprachiasmatic Nucleus Coding for Day Length
Naito, E., Watanabe, T., Tei, H., Yoshimura, T., & Ebihara, S. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730408314572 · Cited by 98 · see citing works
Gamble, K. L., Allen, G. C., Zhou, T., & McMahon, D. G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1109-07.2007 · Cited by 96 · see citing works
de Jeu, M. T. G., & Pennartz, C. M. A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00241.2001 · Cited by 95 · see citing works
Belenky, M. A., Yarom, Y., & Pickard, G. E. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21553 · Cited by 94 · see citing works
Brown, T. M., & Piggins, H. D. (2009) · Journal of Biological Rhythms · doi:10.1177/0748730408327918 · Cited by 92 · see citing works
Johnston, J. D., Ebling, F. J. P., & Hazlerigg, D. G. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04148.x · Cited by 91 · see citing works
Dardente, H., Poirel, V., Klosen, P., Pévet, P., & Masson‐Pévet, M. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03563-1 · Cited by 88 · see citing works
Antle, M. C., Kriegsfeld, L. J., & Silver, R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4696-04.2005 · Cited by 85 · see citing works
Organization of cell and tissue circadian pacemakers: A comparison among species
Vansteensel, M. J., Michel, S. H., & Meijer, J. H. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.10.009 · Cited by 85 · see citing works
Self-citationRash, J. E., Olson, C. O., Pouliot, W. A., Davidson, K. G. V., Yasumura, T., Furman, C. S., Royer, S., Kamasawa, N., Nagy, J. I., & Dudek, F. E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.06.052 · Cited by 82 · see citing works
Meijer, J. H., Rusak, B., & Gänshirt, G. (1992) · Brain Research · doi:10.1016/0006-8993(92)90191-b · Cited by 81 · see citing works
Self-citationRegulation of glutamatergic signalling by PACAP in the mammalian suprachiasmatic nucleus
Michel, S. H., Itri, J. N., Han, J. H., Gniotczynski, K., & Colwell, C. S. (2006) · BMC Neuroscience · doi:10.1186/1471-2202-7-15 · Cited by 80 · see citing works
Self-citationWatanabe, K., Vaněček, J., & Yamaoka, S. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02724-4 · Cited by 78 · see citing works
GABAergic signaling induces divergent neuronal Ca2+ responses in the suprachiasmatic nucleus network
Irwin, R. P., & Allen, C. N. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06944.x · Cited by 73 · see citing works
Shibata, S., Oomura, Y., Hattori, K., et al. (1984) · Brain Research · doi:10.1016/0006-8993(84)91287-3 · Cited by 71 · see citing works
Vansteensel, M. J., Yamazaki, S., Albus, H., Deboer, T., Block, G. D., & Meijer, J. H. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00560-8 · Cited by 67 · see citing works
Self-citationCrossed and uncrossed retinal projections to the hamster circadian system
Muscat, L., Huberman, A. D., Jordan, C. L., & Morin, L. P. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10894 · Cited by 66 · see citing works
Houben, T., Deboer, T., van Oosterhout, F., et al. (2009) · Journal of Biological Rhythms · doi:10.1177/0748730409349895 · Cited by 65 · see citing works
Self-citationA Reexamination of the Role of GABA in the Mammalian Suprachiasmatic Nucleus
Gribkoff, V. K., Pieschl, R. L., Wisialowski, T. A., et al. (1999) · Journal of Biological Rhythms · doi:10.1177/074873099129000515 · Cited by 60 · see citing works
Cell-type specific distribution of chloride transporters in the rat suprachiasmatic nucleus
Belenky, M. A., Sollars, P. J., Mount, D. B., et al. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.11.040 · Cited by 57 · see citing works
Daily Rhythm of Spontaneous Immediate-Early Gene Expression in the Rat Suprachiasmatic Nucleus
Guido, M. E., de Guido, L., Goguen, D., Robertson, H. A., & Rusak, B. (1999) · Journal of Biological Rhythms · doi:10.1177/074873099129000687 · Cited by 51 · see citing works
Seasonal molecular timekeeping within the rat circadian clock
Sumová, A., Bendová, Z., Sládek, M., Kovačíková, Z., & Illnerová, H. (2004) · Physiological Research · doi:10.33549/physiolres.930000.53.s167 · Cited by 51 · see citing works
Aı̈oun, J., Chambille, I., Peytevin, J., et al. (1998) · Cell and Tissue Research · doi:10.1007/s004410050994 · Cited by 49 · see citing works
Sosniyenko, S., Hut, R. A., Daan, S., & Sumová, A. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06945.x · Cited by 43 · see citing works
Simulation of Day-Length Encoding in the SCN: From Single-Cell to Tissue-Level Organization
Rohling, J. H. T., Wolters, L., & Meijer, J. H. (2006) · Journal of Biological Rhythms · doi:10.1177/0748730406290317 · Cited by 41 · see citing works
Self-citationBrown, T. M., Banks, J. R., & Piggins, H. D. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.02.024 · Cited by 38 · see citing works
Seasonal plasticity in the brain: the use of large animal models for neuroanatomical research.
Lehman, M. N., Coolen, L. M., Goodman, R. L., Viguié, C., Billings, H. J., & Karsch, F. J. (2002) · PubMed · Cited by 36 · see citing works
Enhanced circadian phase resetting in R192Q Cav2.1 calcium channel migraine mice
van Oosterhout, F., Michel, S. H., Deboer, T., Houben, T., van de Ven, R. C. G., Albus, H., Westerhout, J., Vansteensel, M. J., Ferrari, M. D., van den Maagdenberg, A. M. J. M., et al. (2008) · Annals of Neurology · doi:10.1002/ana.21418 · Cited by 35 · see citing works
Self-citationDay‐length encoding through tonic photic effects in the retinorecipient SCN region
Yan, L., & Silver, R. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06493.x · Cited by 31 · see citing works
Beersma, D. G. M., van Bunnik, B. A. D., Hut, R. A., & Daan, S. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730408317992 · Cited by 29 · see citing works
The response of a classical Hodgkin–Huxley neuron to an inhibitory input pulse
Börgers, C., Крупа, М. М., & Gielen, S. C. A. M. (2010) · Journal of Computational Neuroscience · doi:10.1007/s10827-010-0233-8 · Cited by 29 · see citing works
PHASE OF THE ELECTRICAL ACTIVITY RHYTHM IN THE SCN IN VITRO NOT INFLUENCED BY PREPARATION TIME
vanderLeest, H. T., Vansteensel, M. J., Duindam, H., Michel, S. H., & Meijer, J. H. (2009) · Chronobiology International · doi:10.3109/07420520903227746 · Cited by 24 · see citing works
Self-citationShibata, S., Oomura, Y., Kita, H., et al. (1984) · Brain Research Bulletin · doi:10.1016/0361-9230(84)90108-4 · Cited by 21 · see citing works
Kiss, J. Z., Csáki, Á., Csaba, Z., & Halász, B. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06463.x · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Widespread seasonal gene expression reveals annual differences in human immunity and physiology
Dopico, X. C., Evangelou, M., Ferreira, R. C., Guo, H., Pękalski, M. Ł., Smyth, D. J., Cooper, N., Burren, O. S., Fulford, A. J. C., Hennig, B. J., et al. (2015) · Nature Communications · doi:10.1038/ncomms8000 · Cited by 539 · see citing works
Linking neural activity and molecular oscillations in the SCN
Colwell, C. S. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3086 · Cited by 474 · see citing works
Melatonin: Both master clock output and internal time-giver in the circadian clocks network
Pévet, P., & Challet, É. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.07.001 · Cited by 372 · see citing works
Circadian Entrainment to the Natural Light-Dark Cycle across Seasons and the Weekend
Stothard, E. R., McHill, A. W., Depner, C. M., Birks, B. R., Moehlman, T. M., Ritchie, H. K., Guzzetti, J. R., Chinoy, E. D., LeBourgeois, M. K., Axelsson, J., et al. (2017) · Current Biology · doi:10.1016/j.cub.2016.12.041 · Cited by 303 · see citing works
“Such changes appear to be mediated by photoperiodic changes in the suprachiasmatic nuclei [30, 31] that control the circadian melatonin rhythm and by responses in peripheral tissues [5].”
BackgroundDynamic Interactions Mediated by Nonredundant Signaling Mechanisms Couple Circadian Clock Neurons
Evans, J. A., Leise, T., Castañón‐Cervantes, O., & Davidson, A. J. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.022 · Cited by 199 · see citing works
GABA-mediated repulsive coupling between circadian clock neurons in the SCN encodes seasonal time
Myung, J., Hong, S., DeWoskin, D., Schutter, E. D., Forger, D. B., & Takumi, T. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421200112 · Cited by 174 · see citing works
“Our results point to modulation of GABA polarity as the underlying physiological mechanism of tunable coupling (21, 22) that is responsible for day-length encoding via the phase gap between SCN oscillators (6).”
BackgroundAllebrandt, K. V., Amin, N., Müller‐Myhsok, B., Esko, T., Teder‐Laving, M., Azevedo, R. V. D. M., Hayward, C., van Mill, J., Vogelzangs, N., Green, E. W., et al. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.142 · Cited by 153 · see citing works
Seasonality in human cognitive brain responses
Meyer, C., Muto, V., Jaspar, M., Kussé, C., Lambot, E., Chellappa, S. L., Degueldre, C., Balteau, E., Luxen, A., Middleton, B., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518129113 · Cited by 139 · see citing works
“Consistently, effects of prior light exposure (“photic memory”) on cognitive brain responses have formerly been demonstrated on a much shorter timescale in humans (37) and photoperiod memory has previously been described as “aftereffects” of photoperiod on circadian clock neurons in rodents (38).”
BackgroundFunctional network inference of the suprachiasmatic nucleus
Abel, J. H., Meeker, K., Granados‐Fuentes, D., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521178113 · Cited by 89 · see citing works
Yoshii, T., Rieger, D., & Helfrich‐Förster, C. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59427-3.00027-7 · Cited by 76 · see citing works
“…that there are two or more types of cell populations in the SCN that respond differently to short and long photoperiods (e.g., Brown and Piggins, 2009; Burgoon et al., 2004; Hazlerigg et al., 2005; Inagaki et al., 2007; Naito et al., 2008; Sosniyenko et al., 2009; reviewed in Meijer et al., 2010).”
BackgroundSaaltink, D., Håvik, B., Veríssimo, C. S., Lucassen, P. J., & Vreugdenhil, E. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23144 · Cited by 73 · see citing works
“The SCN has a plastic nature, which facilitates daily structural rearrangements within the SCN (Meijer et al., 2010; Girardet et al., 2010a).”
BackgroundThe Concept of Coupling in the Mammalian Circadian Clock Network
Pilorz, V., Astiz, M., Heinen, K. O., Rawashdeh, O., & Oster, H. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.12.037 · Cited by 70 · see citing works
Using light to tell the time of day: sensory coding in the mammalian circadian visual network
Brown, T. M. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.132167 · Cited by 70 · see citing works
“…responsive to external Jo u rn al o f Ex p er im en ta lB io lo g y signals (primarily VIP cells) and a strongly rhythmic population (primarily AVP cells) that provides the major source of clock output and is more resistant to external perturbation (Evans and Gorman, 2016; Meijer et al., 2010).”
BackgroundBodenstein, C., Gosak, M., Schuster, S., et al. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002697 · Cited by 55 · see citing works
“Effects of a rapid transition from winter to summer topology on the electrical activity of the SCN.”
InfluentialmiR-132/212 Modulates Seasonal Adaptation and Dendritic Morphology of the Central Circadian Clock
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., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.057 · Cited by 55 · see citing works
“miR-132/212 Regulates Photoperiodic Entrainment Next, we investigated the role of miR-132/212 in entrainment to short (winter) and long (summer) photoperiods that, like entrainment to T-cycles, may involve plasticity of the SCN neuronal network (Meijer et al., 2010; Aton et al., 2004).”
BackgroundRole of vasoactive intestinal peptide in seasonal encoding by the suprachiasmatic nucleus clock
Lucassen, E. A., van Diepen, H. C., Houben, T., Michel, S. H., Colwell, C. S., & Meijer, J. H. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08054.x · Cited by 52 · see citing works
“European Journal of Neuroscience ª 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd Synchronization of neurons within the SCN is also important for seasonal encoding mechanisms of the SCN (VanderLeest et al., 2007; Brown & Piggins, 2009; Meijer et al., 2010).”
BackgroundInfluentialSelf-citationNagy, A. D., Iwamoto, A., Kawai, M., Goda, R., Matsuo, H., Otsuka, T., Nagasawa, M., Furuse, M., & Yasuo, S. (2014) · Chronobiology International · doi:10.3109/07420528.2014.992525 · Cited by 52 · see citing works
“The absence of bmal1 rhythmicity in the vehicletreated group was an unexpected finding in our study, as short photoperiodic entrainment itself is known rather to increase overall amplitude of the SCN neuronal population if compared to equinox photoperiodic conditions (Meijer et al., 2010; Naito et al., 2008; Steinlech…”
BackgroundResultKistenpfennig, C., Nakayama, M., Nihara, R., Tomioka, K., Helfrich‐Förster, C., & Yoshii, T. (2017) · Journal of Biological Rhythms · doi:10.1177/0748730417738612 · Cited by 49 · see citing works
Photoperiodic and circadian bifurcation theories of depression and mania
Kripke, D. F., Elliott, J. A., Welsh, D. K., & Youngstedt, S. D. (2015) · F1000Research · doi:10.12688/f1000research.6444.1 · Cited by 48 · see citing works
The role of the hypothalamic-pituitary-adrenal axis in modulating seasonal changes in immunity
Pierre, K. K., Schlesinger, N., & Androulakis, I. P. (2016) · Physiological Genomics · doi:10.1152/physiolgenomics.00006.2016 · Cited by 48 · see citing works
“Seasonal analysis on SCN neuronal activity measured from mice and rat hypothalamic slice explants have identified decompressed or less synchronized firing patterns among neurons during the longer summer days while winter days were more associated with compressed or synchronized activity (81, 109, 114, 142).”
BackgroundCircadian and Circannual Regulation in the Horse: Internal Timing in an Elite Athlete
Murphy, B. A. (2019) · Journal of Equine Veterinary Science · doi:10.1016/j.jevs.2019.02.026 · Cited by 48 · see citing works
Melatonin receptors as therapeutic targets in the suprachiasmatic nucleus
Pévet, P. (2016) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2016.1179284 · Cited by 49 · see citing works
Mammalian circadian networks mediated by the suprachiasmatic nucleus
Lu, Q., & Kim, J. Y. (2021) · FEBS Journal · doi:10.1111/febs.16233 · Cited by 50 · see citing works
Rohr, K. E., Pancholi, H., Haider, S., Karow, C., Modert, D., Raddatz, N. J., & Evans, J. A. (2019) · eLife · doi:10.7554/elife.49578 · Cited by 46 · see citing works
Post-transcriptional modulators and mediators of the circadian clock
Anna, G., & Kannan, N. N. (2021) · Chronobiology International · doi:10.1080/07420528.2021.1928159 · Cited by 42 · see citing works
“…rhythm, it senses changes in day length and seasonal adaptation relies predominantly on the structural plasticity of SCN neuronal network (Meijer et al. 2010). miR-132/212 modulates entrainment to various photoperiods and day length mediated regulation of PER2 expression in the SCN…”
BackgroundHasebe, M., & Shiga, S. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2018823118 · Cited by 41 · see citing works
Circadian gating of neuronal functionality: a basis for iterative metaplasticity1
Iyer, R., Wang, T. A., & Gillette, M. U. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00164 · Cited by 41 · see citing works
“…durations undergo seasonal variations, an anticipatory, endogenous rhythm generator would adapt and entrain to changing ratios of light: dark periods, generating seasonal plasticity in behaviors (Bartness et al., 1993; Ebling et al., 1995; Nuesslein-Hildesheim et al., 2000; Meijer et al., 2010).”
BackgroundCircadian Rhythm Disruption and Alzheimer's Disease: The Dynamics of a Vicious Cycle
Sharma, A., Sethi, G., Tambuwala, M. M., Aljabali, A. A. A., Chellappan, D. K., Dua, K., & Goyal, R. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200429013041 · Cited by 49 · see citing works
“This essential factor allows organisms to smoothly transition through the seasonal changes in light-dark cycles [23].”
BackgroundAssociation of Per3 length polymorphism with bipolar I disorder and schizophrenia
Pandi-Perumal, S. R., Ramanujam, K., Marimuthu, G., Ramasubramanian, C., Arunachal, G., BaHammam, A. S., Spence, D. W., Cardinali, D. P., & Brown, G. M. (2014) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s73765 · Cited by 37 · see citing works
“1,2 There is a close interdependency between the circadian system and the body’s homeostatic mechanisms.”
Circuit development in the master clock network of mammals
Carmona‐Alcocer, V., Rohr, K. E., Joye, D. A. M., & Evans, J. A. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14259 · Cited by 37 · see citing works
Vasopressin regulates daily rhythms and circadian clock circuits in a manner influenced by sex
Rohr, K. E., Telega, A., Savaglio, A., & Evans, J. A. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104888 · Cited by 35 · see citing works
Leach, G., Ramanathan, C., Langel, J.-L., & Yan, L. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.01.002 · Cited by 34 · see citing works
“Accumulating evidence on metabolic rate, electrical activity and clock gene expressions indicates that the day-length information is encoded by the SCN (Schwartz et al., 2001; Hofman, 2004; Sumova et al., 2004; Johnston, 2005; Meijer et al., 2007, 2010).”
Bipolar mood cycles associated with lunar entrainment of a circadian rhythm
Wehr, T. A. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0203-x · Cited by 33 · see citing works
Circadian clocks in changing weather and seasons: Lessons from the picoalga Ostreococcus tauri
Pfeuty, B., Thommen, Q., Corellou, F., Djouani-Tahri, E. B., Bouget, F., & Lefranc, M. (2012) · BioEssays · doi:10.1002/bies.201200012 · Cited by 32 · see citing works
Timing by rhythms: Daily clocks and developmental rulers
Webb, A. B., & Oates, A. C. (2015) · Development Growth & Differentiation · doi:10.1111/dgd.12242 · Cited by 29 · see citing works
“…responsiveness, and rhythmic properties across the SCN, investigating what function regional differences in these elements could impart on the circadian system (Moore et al. 2002; Karatsoreos et al. 2004; Kriegsfeld et al. 2004; Antle & Silver 2005; VanderLeest et al. 2007; Meijer et al. 2010).”
BackgroundGirardet, C., Lebrun, B., Cabirol, M.-J., et al. (2013) · Glia · doi:10.1002/glia.22509 · Cited by 31 · see citing works
“Then, the integrative capacities of the SCN would rely on functional plasticity in the network (Meijer et al., 2010; Yan et al., 2010).”
BackgroundShapiro-Reznik, M., Jilg, A., Lerner, H., Earnest, D. J., & Zisapel, N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037894 · Cited by 31 · see citing works
“Indeed, SCN oscillations are associated with plastic changes in configuration of the SCN cell network [28,29,31,42,43].”
Tacad, D. K., Tovar, A. P., Richardson, C. E., Horn, W. F., Keim, N. L., Krishnan, G. P., & Krishnan, S. (2022) · Advances in Nutrition · doi:10.1093/advances/nmac011 · Cited by 27 · see citing works
Circadian Rhythm Disruption and Alzheimers Disease: The Dynamics of a Vicious Cycle
Sharma, A. (2021) · Current Neuropharmacology · doi:10.2174/18756190mta21mjaf3 · Cited by 29 · see citing works
Neurophysiological Analysis of the Suprachiasmatic Nucleus
Meijer, J. H., & Michel, S. H. (2014) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2014.11.001 · Cited by 27 · see citing works
Self-citationGu, C., Tang, M., & Yang, H. (2016) · Scientific Reports · doi:10.1038/srep28878 · Cited by 25 · see citing works
Pierre, K. K., Rao, R., Hartmanshenn, C., & Androulakis, I. P. (2018) · Endocrinology · doi:10.1210/en.2017-03226 · Cited by 25 · see citing works
Enhanced Phase Resetting in the Synchronized Suprachiasmatic Nucleus Network
Ramkisoensing, A., Gu, C., Gastelaars, H. V. E., Michel, S. H., Deboer, T., Rohling, J. H. T., & Meijer, J. H. (2014) · Journal of Biological Rhythms · doi:10.1177/0748730413516750 · Cited by 25 · see citing works
“The light term L also differs between photoperiods; L S represents the light term under a short photoperiod, and L L represents the light term under a long photoperiod.”
BackgroundSelf-citationTemporal behaviour profiles of Mus musculus in nature are affected by population activity
Robbers, Y., Koster, E. A. S., Krijbolder, D. I., Ruijs, A., van Berloo, S., & Meijer, J. H. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.020 · Cited by 24 · see citing works
“The system underlying seasonal regulation is complex and has been intensively studied (for review, see [28,70]).”
BackgroundSelf-citationLeSauter, J., Silver, R., Cloues, R. K., et al. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00060.2011 · Cited by 24 · see citing works
Thommen, Q., Pfeuty, B., Corellou, F., Bouget, F., & Lefranc, M. (2012) · FEBS Journal · doi:10.1111/j.1742-4658.2012.08666.x · Cited by 23 · see citing works
Anatomical and Behavioral Investigation of C1ql3 in the Mouse Suprachiasmatic Nucleus
Chew, K. S., Fernandez, D. C., Hattar, S. S., Südhof, T. C., & Martinelli, D. C. (2017) · Journal of Biological Rhythms · doi:10.1177/0748730417704766 · Cited by 23 · see citing works
“Finally, from studies in humans it has been proposed that neural plasticity may underlie aftereffects (Meijer et al., 2010; Scheer et al., 2007).”
Reduced VIP Expression Affects Circadian Clock Function in VIP-IRES-CRE Mice (JAX 010908)
Joye, D. A. M., Rohr, K. E., Keller, D., Inda, T., Telega, A., Pancholi, H., Carmona‐Alcocer, V., & Evans, J. A. (2020) · Journal of Biological Rhythms · doi:10.1177/0748730420925573 · Cited by 23 · see citing works
“, period synchrony, phase relationships, precision/amplitude modulation) that contribute to master clock function in important ways (Evans, 2016; Hastings et al., 2018; Herzog et al., 2004; Meijer et al., 2010).”
BackgroundStructural plasticity of the circadian timing system. An overview from flies to mammals
Bosler, O., Girardet, C., Franc, J., Becquet, D., & François‐Bellan, A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.02.001 · Cited by 22 · see citing works
“This has been shown in particular for the liver as well as extra-SCN cerebral clocks (see Mendoza and Challet, 2009).”
BackgroundCoherency of circadian rhythms in the SCN is governed by the interplay of two coupling factors
Tokuda, I. T., Ono, D., Honma, S., Honma, K., & Herzel, H. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006607 · Cited by 20 · see citing works
Sleep and circadian rhythm disturbance in kidney stone disease: a narrative review
He, S., Wang, J., Li, T., Yin, S., Cui, J., Xiao, Y., Tang, Y., Wang, J. H., & Bai, Y. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1293685 · Cited by 18 · see citing works
Rapid Adjustment of Circadian Clocks to Simulated Travel to Time Zones across the Globe
Harrison, E. M., & Gorman, M. R. (2015) · Journal of Biological Rhythms · doi:10.1177/0748730415598875 · Cited by 18 · see citing works
“While this may be predicted by limit-cycle considerations, it contrasts with SCN network findings wherein greater phase coherence in short photoperiods is associated with increased phase-shift responses to light (Meijer et al., 2010).”
ResultNess, N., Díaz-Clavero, S., Hoekstra, M. M., & Brancaccio, M. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00324-w · Cited by 17 · see citing works
“Moreover, variance in the relative phases of neuronal oscillators within the SCN is essential to transform variations in day length into adaptive downstream seasonal physiology, a key example of circuit plasticity underpinning daily behavior in mammals (Meijer et al, 2010).”
Changing the Waveform of Circadian Rhythms: Considerations for Shift-Work
Harrison, E. M., & Gorman, M. R. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00072 · Cited by 17 · see citing works
“In rodents, the waveform of a given photoperiod is encoded in the SCN itself (Schwartz et al., 2001; Sumová et al., 2004; Meijer et al., 2010) with parallel patterns in such downstream outputs as melatonin and behavior (Illnerova et al.”
BackgroundThe Potential of Circadian Realignment in Rheumatoid Arthritis
Rao, R., Pierre, K. K., Schlesinger, N., & Androulakis, I. P. (2016) · Critical Reviews in Biomedical Engineering · doi:10.1615/critrevbiomedeng.2016018812 · Cited by 17 · see citing works
Li, Y., Lu, L., & Androulakis, I. P. (2024) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2023.08.005 · Cited by 17 · see citing works
Network Structure of the Master Clock Is Important for Its Primary Function
Gu, C., Li, J., Zhou, J., Yang, H., & Rohling, J. H. T. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.678391 · Cited by 16 · see citing works
“, 16 h:8 h light:dark cycle (representing summer days) (VanderLeest et al., 2007; Meijer et al., 2010; Gu et al., 2016).”
BackgroundSelf-citationSteady-State Pupil Size Varies with Circadian Phase and Sleep Homeostasis in Healthy Young Men
Egroo, M. V., Gaggioni, G., Cespedes-Ortiz, C., Ly, J. Q. M., & Vandewalle, G. (2019) · Clocks & Sleep · doi:10.3390/clockssleep1020021 · Cited by 16 · see citing works
“In mammal, as well as other animal Classes, the master circadian clock consists of the suprachiasmatic nuclei (SCN) located within the hypothalamus [43,44].”
BackgroundIngrained city rhythms: flexible activity timing but more persistent circadian pace in urban birds
Tomotani, B., Timpen, F., & Spoelstra, K. (2023) · Proceedings of the Royal Society B · doi:10.1098/rspb.2022.2605 · Cited by 11 · see citing works
Potdar, S., & Sheeba, V. (2012) · Journal of Biological Rhythms · doi:10.1177/0748730412449820 · Cited by 15 · see citing works
“While a hierarchical circadian circuit explains some phenomena, a more distributed and plastic clock network has been called for, taking into account mammalian studies (Nitabach and Taghert, 2008; Sheeba et al., 2008c; Meijer et al., 2010).”
BackgroundMoreno, J. P., Crowley, S. J., Alfano, C. A., & Thompson, D. I. (2019) · Obesity Reviews · doi:10.1111/obr.12973 · Cited by 17 · see citing works
“Within the SCN, the phase of the ventral and dorsal SCN regions diverge from one another during the longer days of summer.(36) If SCN firing during daylight hours inhibits melatonin release, the separation between the ventral and dorsal regions during long summer days will shorten the melatonin release duration during…”
BackgroundMorán‐Ramos, S., Guerrero‐Vargas, N. N., Méndez‐Hernández, R., Basualdo, M. D. C., Escobar, C., & Buijs, R. M. (2017) · Experimental Physiology · doi:10.1113/ep086026 · Cited by 14 · see citing works
“By receiving light input from the retinohypothalamic tract, its activity is synchronized to the LD cycle (Meijer et al. 2010) and drives circadian rhythms (Hastings et al. 2003; Kalsbeek et al. 2007).”
BackgroundReported light in the sleep environment: enhancement of the sleep diary
Harrison, E. M., Yablonsky, A. M., Powell, A. L., Ancoli‐Israel, S., & Glickman, G. L. (2019) · Nature and Science of Sleep · doi:10.2147/nss.s193902 · Cited by 13 · see citing works
Neural correlates of individual differences in circadian behaviour
Evans, J. A., Leise, T., Castañón‐Cervantes, O., & Davidson, A. J. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.0769 · Cited by 14 · see citing works
Generation and Disruption of Circadian Rhythms in the Suprachiasmatic Nucleus: A Core-Shell Model
Goltsev, A. V., Wright, E. A. P., Mendes, J. F. F., & Yoon, S. Y. (2022) · Journal of Biological Rhythms · doi:10.1177/07487304221107834 · Cited by 13 · see citing works
“The Kuramoto model has been used to explain the eastwest asymmetry in jet lag recovery times (Lu et al., 2016), seasonal adaptation of the circadian clock (Gu et al., 2016; Meijer et al., 2010), and phase splitting within the SCN (Rohling and Meylahn, 2020).”
MethodSeasonal effect—an overlooked factor in neuroimaging research
Zhang, R., Kojori, E. S., & Volkow, N. D. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02530-2 · Cited by 13 · see citing works
“If the SMN association with day length reflects a proactive brain response, SMN might receive information from upstream regions that signal the timing of twilight such as the entrainment of the internal clock by light [33].”
BackgroundCircadian rhythms and mood: Opportunities for multi‐level analyses in genomics and neuroscience
Li, J. Z. (2013) · BioEssays · doi:10.1002/bies.201300141 · Cited by 13 · see citing works
“In the SCN, adaptation to seasonal changes of day length or temperature is achieved not by changed oscillating properties of individual neurons but by the altered phase relationship among them [11, 12].”
BackgroundAre circadian amplitudes and periods correlated? A new twist in the story
del Olmo, M., Schmal, C., Mizaikoff, C., Grabe, S., Gabriel, C. H., Kramer, A., & Herzel, H. (2023) · F1000Research · doi:10.12688/f1000research.135533.1 · Cited by 12 · see citing works
Kingsbury, N. J., Taylor, S. R., & Henson, M. A. (2016) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2016.02.039 · Cited by 12 · see citing works
“Robust rhythms are necessary for ensuring that regular sleep and other behavioral schedules are followed even when external cues are absent; however networks must also be flexible so that organisms may adjust their schedule to seasonal changes or time shifts (Herzog, 2007; Meijer et al., 2010; Pfeuty et al., 2012).”
BackgroundMichel, S. H., & Kervezee, L. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01680-4 · Cited by 12 · see citing works
“However, using model systems deprived of, let us say melatonin, can help study and understand the underlying mechanisms at different levels of the photoperiodic encoding machinery (Meijer et al. 2010; VanderLeest et al. 2007).”
Self-citationBussi, I. L., Neitz, A. F., Sanchez, R. E. A., Casiraghi, L. P., Moldavan, M. G., Kunda, D., Allen, C. N., Evans, J. A., & de la Iglesia, H. O. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2314857120 · Cited by 11 · see citing works
Expression of prokineticin 2 and its receptor in the macaque monkey brain
Burton, K. J., Li, X., Li, B., Cheng, M., Urbanski, H. F., & Zhou, Q. (2016) · Chronobiology International · doi:10.3109/07420528.2015.1125361 · Cited by 11 · see citing works
Li, Y., & Androulakis, I. P. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.960351 · Cited by 11 · see citing works
“Therefore, the increased ensemble amplitude of the SCN in SP due to the narrowing of the neuronal phase distribution results in the physiology and behavior of organisms being shorter during SP than during LP (9, 11).”
BackgroundMulticellular models of intercellular synchronization in circadian neural networks
Henson, M. A. (2013) · Chaos Solitons & Fractals · doi:10.1016/j.chaos.2012.11.008 · Cited by 11 · see citing works
Athanasouli, C., Piltz, S. H., Behn, C. D., & Booth, V. (2022) · SIAM Journal on Applied Dynamical Systems · doi:10.1137/21m1446149 · Cited by 10 · see citing works
Chrobok, Ł., Ahern, J., & Piggins, H. D. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.931167 · Cited by 10 · see citing works
“Current evidence indicates that the plasticity in phase distribution and phase gap between the dorsal and ventral SCN enable the circadian clock in the SCN to code daylength and thereby potentially act as a seasonal calendar (Meijer et al., 2010; Coomans et al., 2015; Myung and Pauls, 2018).”
BackgroundRao, R., Scherholz, M. L., Hartmanshenn, C., Bae, S.-A., & Androulakis, I. P. (2017) · Computers & Chemical Engineering · doi:10.1016/j.compchemeng.2017.06.003 · Cited by 10 · see citing works
“Interestingly, and as explored in (Pierre et al., 2016), neurons in the hypothalamus show a more synchronized firing activity during the short winter days, resulting in increased ensemble amplitude (Meijer et al., 2010; Rohling et al., 2006).”
BackgroundSmith, S., Ramos, R. A., Refinetti, R., et al. (2013) · Applied Physiology Nutrition and Metabolism · doi:10.1139/apnm-2012-0420 · Cited by 9 · see citing works
Stochastic simulation of the circadian rhythmicity in the SCN neuronal network
Šimonka, V., Fras, M., & Gosak, M. (2015) · Physica A Statistical Mechanics and its Applications · doi:10.1016/j.physa.2014.12.034 · Cited by 9 · see citing works
Rethinking Temperature Sensitivity of the Suprachiasmatic Nucleus
Ruby, N. F. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730411411678 · Cited by 9 · see citing works
“…distinct local networks in the rostral and caudal SCN that dissociate from one another under long day photoperiods (Inagaki et al., 2007; Naito et al., 2008; Meijer et al., 2010) and that reducing the number of cells in the network alters the behavior of the SCN population (Meijer et al., 2010).”
BackgroundHannibal, J., Bisgaard, T. H., Georg, B., & Fahrenkrug, J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14482 · Cited by 9 · see citing works
Mood variation under dual regulation of circadian clock and light
Rahim, A. R., Will, V. W.-T., & Myung, J. (2025) · Chronobiology International · doi:10.1080/07420528.2025.2455144 · Cited by 7 · see citing works
“These studies have revealed a degree of plasticity in neuronal network properties, rather than in the properties of single cells (Meijer et al. 2010).”
Plasticity of neuroendocrine systems
Prévot, V. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07533.x · Cited by 7 · see citing works
“…plays as a circadian pacemaker, primarily entraining the organism to light ⁄ dark information and controlling rhythmicity of melatonin synthesis from the pineal gland (Challet, 2007), for the daily and seasonal regulation of neuroendocrine systems (Girardet et al., 2010; Meijer et al., 2010).”
BackgroundThe Suprachiasmatic Nucleus (SCN)
Colwell, C. S., Witkovsky, P., & Silver, R. (2015) · doi:10.1002/9781118467831.ch3 · Cited by 7 · see citing works
Modeling homeostatic and circadian modulation of human pain sensitivity
Crodelle, J. A., Vanty, C., & Booth, V. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1166203 · Cited by 6 · see citing works
“The circadian drive variable Cs(t) generates oscillations in the average firing rate of the SCN population, fSCN , between 1 and 7 Hz which is in agreement with experimental data on the neuronal activity in SCN in mammals (Meijer et al., 2010).”
ResultLi, Y., & Androulakis, I. P. (2023) · Journal of Biological Rhythms · doi:10.1177/07487304231188541 · Cited by 6 · see citing works
“During short photoperiod months (winter), the SCN neurons exhibit a narrower phase distribution compared to long photoperiod months (summer) (VanderLeest et al., 2007; Meijer et al., 2010).”
BackgroundZhang, X., Huang, S., & Kim, J. Y. (2024) · iScience · doi:10.1016/j.isci.2024.108829 · Cited by 6 · see citing works
Seasonality in regional brain glucose metabolism
Zhang, R., Tomasi, D. G., Kojori, E. S., Manza, P., Demiral, Ş. B., Wang, G., & Volkow, N. D. (2024) · Psychological Medicine · doi:10.1017/s0033291724000436 · Cited by 5 · see citing works
“Since the effects of acute light exposure are relatively short, the observed photoperiod memory could reflect ‘ after effects ’ of the photoperiod on the internal clock (Chellappa et al., 2014; Meijer, Michel, Vanderleest, & Rohling, 2010).”
The Relevance of Circadian Clocks to Stem Cell Differentiation and Cancer Progression
Malik, A., Nalluri, S., De, A., Beligala, D. H., & Geusz, M. E. (2022) · NeuroSci · doi:10.3390/neurosci3020012 · Cited by 6 · see citing works
Ashraf, H., Ahmad, J., Hassan, A., & Ali, A. (2019) · Biosystems · doi:10.1016/j.biosystems.2019.02.005 · Cited by 5 · see citing works
Time after time – circadian clocks through the lens of oscillator theory
del Olmo, M., Ector, C., & Herzel, H. (2026) · FEBS Letters · doi:10.1002/1873-3468.70257 · Cited by 5 · see citing works
“Such effects have been linked to age-related changes in SCN coherence [251,252], to altered phenotypes in Cry -deficient mice [253], and to the SCN’s adaptation to seasonal changes [188,190].”
Reghunandanan, V. (2024) · Exploration of neuroscience · doi:10.37349/en.2024.00059 · Cited by 4 · see citing works
Grant, A. D., Wilbrecht, L., & Kriegsfeld, L. J. (2022) · Journal of Biological Rhythms · doi:10.1177/07487304221092715 · Cited by 4 · see citing works
“, 2015) and more variable activity rhythms (Kim and Harrington, 2008; Meijer et al., 2010), and have altered weight gain trajectories (Brown-Douglas et al.”
Berardis, D. D. (2011) · ChronoPhysiology and Therapy · doi:10.2147/cpt.s16972 · Cited by 4 · see citing works
“Nerve fibers from the SCN project through multisynaptic descending pathways that pass through the sub-paraventricular zone, median forebrain bundle, and the reticular formation to the intermediolateral horn cells of the spinal cord.(18) From here, preganglionic fibers reach the superior cervical ganglion, which gives…”
Modeling the Influence of Synaptic Plasticity on After-effects
Foster, S., Christiansen, T., & Antle, M. C. (2019) · Journal of Biological Rhythms · doi:10.1177/0748730419871189 · Cited by 4 · see citing works
“Plasticity in α, ρ, and circadian amplitude under different photoperiods is due to the phase dispersion of individual oscillators (Meijer et al., 2010; Rohling et al., 2006; Schaap et al., 2003; VanderLeest et al., 2007).”
BackgroundBall, S., Caravaggi, A., & Butler, F. (2022) · Remote Sensing in Ecology and Conservation · doi:10.1002/rse2.293 · Cited by 4 · see citing works
“Circadian and seasonal activity patterns are photoresponsive cycles regulated by the suprachiasmatic nucleus of the hypothalamus in mammals (Meijer et al., 2010), allowing for species to fulfil daily requirements (e.g. feeding) while adapting to seasonal day length.”
BackgroundQuantitative systems pharmacology: Extending the envelope through systems engineering
Hartmanshenn, C., Rao, R., Bae, S.-A., Scherholz, M. L., Acevedo, A., Pierre, K. K., & Androulakis, I. P. (2018) · Computer-aided chemical engineering/Computer aided chemical engineering · doi:10.1016/b978-0-444-63964-6.00001-5 · Cited by 4 · see citing works
Feng, J., Zheng, W., & Gu, C. (2025) · Symmetry · doi:10.3390/sym17091418 · Cited by 2 · see citing works
Relevance of Network Organization in SCN Clock Function
Morgado, E., Juárez-Portilla, C. J., Silverman, A., & Silver, R. (2014) · Springer eBooks · doi:10.1007/978-3-319-08945-4_9 · Cited by 3 · see citing works
Do Circadian Rhythms Draw the Patterns of Sustained Mental Vigor and Ailment?
Sharma, A., & Goyal, R. (2016) · Drug Development Research · doi:10.1002/ddr.21342 · Cited by 2 · see citing works
“[Meijer et al., 2010].”
- Authors
- Meijer, J. H., Michel, S., VanderLeest, H. T., & Rohling, J. H. T.
- Affiliations
- Leiden University Medical Center (NL)
- Corresponding author
- Meijer, Johanna H.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2010-12
- Volume
- 32
- Issue
- 12
- Pages
- 2143-2151
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2157329350
- Semantic Scholar
- e6ae1ddf69a540699da985faa18f4dd0e558d367
- Cited by
- 119
- References
- 106
- Citations by year
- 2026: 6 · 2025: 2 · 2024: 4 · 2023: 11 · 2022: 8 · 2021: 9 · 2020: 4 · 2019: 8 · 2018: 9 · 2017: 6 · 2016: 11 · 2015: 9 · 2014: 8 · 2013: 6 · 2012: 10
- FWCI
- 0.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- Funders
- European Commission
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Physical Sciences › Computer Science › Computer Networks and Communications › Nonlinear Dynamics and Pattern Formation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- circadian clock, suprachiasmatic nucleus, neuroplasticity, light entrainment, seasonal adaptation, day length, neuronal coupling, circadian rhythm
- MeSH terms
- Adaptation, Physiological, Animals, Circadian Rhythm, Nerve Net, Neuronal Plasticity, Seasons, Suprachiasmatic Nucleus, Photoperiod, Neurotransmitter Agents, Jet Lag Syndrome, Circadian Clocks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
