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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.
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“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]
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“, 16 h:8 h light:dark cycle (representing summer days) (VanderLeest et al., 2007; Meijer et al., 2010; Gu et al., 2016).”
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Egroo, M. V., Gaggioni, G., Cespedes-Ortiz, C., Ly, J. Q. M., & Vandewalle, G. (2019) · Clocks & Sleep · doi:10.3390/clockssleep1020021 · Cited by 16
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“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
“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].”
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“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
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
“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
“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
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
Li, Y., & Androulakis, I. P. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.960351 · Cited by 11
“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
Athanasouli, C., Piltz, S. H., Behn, C. D., & Booth, V. (2022) · SIAM Journal on Applied Dynamical Systems · doi:10.1137/21m1446149 · Cited by 10
Chrobok, Ł., Ahern, J., & Piggins, H. D. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.931167 · Cited by 9
“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
“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
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
Rethinking Temperature Sensitivity of the Suprachiasmatic Nucleus
Ruby, N. F. (2011) · Journal of Biological Rhythms · doi:10.1177/0748730411411678 · Cited by 9
“…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
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
“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
“…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) · Wiley eBooks · doi:10.1002/9781118467831.ch3 · Cited by 7
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
“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
“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
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
“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 8
Ashraf, H., Ahmad, J., Hassan, A., & Ali, A. (2019) · Biosystems · doi:10.1016/j.biosystems.2019.02.005 · Cited by 5
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
“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
Grant, A. D., Wilbrecht, L., & Kriegsfeld, L. J. (2022) · Journal of Biological Rhythms · doi:10.1177/07487304221092715 · Cited by 4
“, 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
“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 5
“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
“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
Feng, J., Zheng, W., & Gu, C. (2025) · Symmetry · doi:10.3390/sym17091418 · Cited by 2
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
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
“[Meijer et al., 2010].”
Collins, B. H., & Brown, S. A. (2018) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.10.002 · Cited by 2
Metadata
- 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 › Physics and Astronomy › Statistical and Nonlinear Physics › 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
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