The DOI matches its Crossref record.
Entrainment of Syrian hamster circadian activity rhythms by neonatal melatonin injections
Abstract
The circadian rhythms of fetal and neonatal rodents are entrained by their mother. This entrainment is dependent upon the maternal suprachiasmatic nucleus (SCN), but the mechanism of entrainment is unknown. Administration of the pineal hormone melatonin to pregnant, SCN-lesioned female Syrian hamsters entrains the activity rhythms of their hamster pups. The aim of this study was to determine whether melatonin injected directly in neonatal Syrian hamsters is able to entrain circadian rhythms and, if so, for how long this effect persists during development. Injection of melatonin in two groups of hamster pups at opposite phases on postnatal days 1-5 entrained the onset of activity rhythms on the day of weaning to two phases 10.67 h apart. Melatonin injection did not entrain activity rhythms to opposite phases on either postnatal days 6-10 or 21-25. Vehicle injection did not entrain animals to opposite phases at any of the ages studied. These results demonstrate that melatonin is able to act directly on the neonate to cause entrainment and that this effect disappears after postnatal day 6.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
The failure of stable maternal rhythms to rescue offspring outcomes is in contrast with ELS and maternal melatonin literature, in which neonatal interventions rescue circadian- and ELS-induced effects in offspring.
“The failure of stable maternal rhythms to rescue offspring outcomes are in contrast with both the ELS and maternal melatonin literature, in which neonatal interventions rescue circadian-22, 53–55 and ELS-induced effects in offspring56.”
From Maternal and Early-Life Circadian Disruption Have Long-Lasting Negative Consequences on Offspring Development and Adult Behavior in Mice (2017) · cites this paper as [55]
Citations
Cited by
Sorted by citations
Molecular Dissection of Two Distinct Actions of Melatonin on the Suprachiasmatic Circadian Clock
Liu, C., Weaver, D. R., Jin, X., Shearman, L. P., Pieschl, R. L., Gribkoff, V. K., & Reppert, S. M. (1997) · Neuron · doi:10.1016/s0896-6273(00)80350-5 · Cited by 723
Cellular Mechanisms of Melatonin Action
Vaněček, J. (1998) · Physiological Reviews · doi:10.1152/physrev.1998.78.3.687 · Cited by 579
Dubocovich, M. L., Hudson, R. L., Sumaya, I. C., Masana, M. I., & Manna, E. (2005) · Journal of Pineal Research · doi:10.1111/j.1600-079x.2005.00230.x · Cited by 129
Entrainment of the Circadian System of Mammals by Nonphotic Cues
Hastings, M. H., Duffield, G. E., Smith, E. J. D., Maywood, E. S., & Ebling, F. J. P. (1998) · Chronobiology International · doi:10.3109/07420529808998700 · Cited by 123
Multiple Effects of Melatonin on Rhythmic Clock Gene Expression in the Mammalian Pars Tuberalis
Johnston, J. D., Tournier, B. B., Andersson, H., Masson‐Pévet, M., Lincoln, G. A., & Hazlerigg, D. G. (2005) · Endocrinology · doi:10.1210/en.2005-1100 · Cited by 117
“Exogenous melatonin administration has been shown to synchronize circadian behavioral rhythmicity in rodents (33, 34) and in humans (35), and melatonin can reportedly phaseshift circadian rhythms of electrical activity in mouse SCN slice preparations (36).”
BackgroundMelatonin's Role in Vertebrate Orcadian Rhythms
Cassone, V. M. (1998) · Chronobiology International · doi:10.3109/07420529808998702 · Cited by 115
Development of the circadian system in early life: maternal and environmental factors
Wong, S. D., Wright, K. P., Spencer, R. L., Vetter, C., Hicks, L. M., Jenni, O. G., & LeBourgeois, M. K. (2022) · Journal of PHYSIOLOGICAL ANTHROPOLOGY · doi:10.1186/s40101-022-00294-0 · Cited by 111
“Injection of melatonin in neonatal hamsters born to SCN-lesioned mothers resulted in entrained circadian rhythms of wheel-running activity on the day of weaning, PND21 [129].”
BackgroundMelatonin: role in development
Davis, F. C. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200603 · Cited by 90
“Interestingly, melatonin given to pups on postnatal Days 6 to 10 does not cause entrainment (Grosse et al., 1996).”
BackgroundConstructing the suprachiasmatic nucleus: a watchmaker's perspective on the central clockworks
Bedont, J. L., & Blackshaw, S. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00074 · Cited by 91
“Melatonin is also present in the milk of mammals, including humans, and exogenous melatonin is sufficient to entrain rat and hamster rhythms both embryonically and in early postnatal life (Davis and Mannion, 1988; Illnerova et al., 1993; Grosse et al., 1996; Viswanathan and Davis, 1997).”
BackgroundSmarr, B. L., Grant, A. D., Perez, L., Zucker, I., & Kriegsfeld, L. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-03406-4 · Cited by 86
Ontogenetic Development of the Mammalian Circadian System
Weinert, D. (2005) · Chronobiology International · doi:10.1081/cbi-200053473 · Cited by 87
“E-mail: weinert@zoologie.uni-halle.de Chronobiology International, 22(2): 179–205, (2005) Copyright # 2005 Taylor & Francis, Inc. ISSN 0742-0528 print/1525-6073 online DOI: 10.1081/CBI-200053473 179”
InfluentialCircadian Entrainment and Phase Shifting in Mammals with Melatonin
Redman, J. R. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200613 · Cited by 77
“neonate (Grosse et al., 1996) or indirectly via the mother to the fetus (Davis and Mannion, 1988).”
BackgroundDeveloping circadian rhythmicity
Rivkees, S. A., & Hao, H. (2000) · Seminars in Perinatology · doi:10.1053/sper.2000.8598 · Cited by 76
Ohta, H., Honma, S., Abe, H., & Honma, K. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02016.x · Cited by 69
Non‐photic signalling in the suprachiasmatic nucleus
Hastings, M. H., Duffield, G. E., Ebling, F. J. P., Kidd, A., Maywood, E. S., & Schurov, I. (1997) · Biology of the Cell · doi:10.1016/s0248-4900(98)80005-1 · Cited by 69
Johnston, J. D., & Skene, D. J. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0119 · Cited by 66
“1992), neonate hamsters are readily entrained to melatonin injections (Grosse et al. 1996).”
BackgroundViswanathan, N., & Davis, F. C. (1997) · Journal of Comparative Physiology A · doi:10.1007/s003590050053 · Cited by 59
“1994; this study), and injections of melatonin (Grosse et al. 1996) or SKF 38393 (J.”
BackgroundInfluentialSelf-citationMcNulty, S., Schurov, I., Sloper, P., & Hastings, M. H. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00114.x · Cited by 48
Pévet, P. (2003) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2003.5.4/ppevet · Cited by 41
Melatonin Action in the Pituitary: Neuroendocrine Synchronizer and Developmental Modulator?
Johnston, J. D., Messager, S., Barrett, P., & Hazlerigg, D. G. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.00972.x · Cited by 38
Melatonin in rat milk and the likelihood of its role in postnatal maternal entrainment of rhythms
Rowe, S. A., & Kennaway, D. J. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00228.2001 · Cited by 38
“This conclusion does not contradict the observation that daily administration of exogenous melatonin can entrain the neonatal rodent (8, 25).”
BackgroundDevelopmental expression of clock genes in the Syrian hamster
Li, X., & Davis, F. C. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.05.005 · Cited by 39
“The present results raise new questions about the effects of prenatal phase-setting stimuli such as melatonin and dopamine agonists [7,15–17,42,43].”
BackgroundSelf-citationGauer, F., Schuster, C., Poirel, V., et al. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(98)00177-6 · Cited by 38
Genetic deletion of MT1/MT2 melatonin receptors enhances murine cognitive and motor performance
O’Neal-Moffitt, G., Pilli, J., Kumar, S. S., & Olcese, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.018 · Cited by 37
Neurogenesis and ontogeny of specific cell phenotypes within the hamster suprachiasmatic nucleus
Antle, M. C., LeSauter, J., & Silver, R. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.02.017 · Cited by 33
“Fetal hamsters can be entrained in utero with injections of dopamine agonists [49] or melatonin [12,15,49], suggesting that the circadian clock is functioning prior to birth.”
BackgroundSong, C. K., Bartness, Petersen, & Bittman (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00479.x · Cited by 33
Duffield, G. E., & Ebling, F. J. P. (1998) · Journal of Biological Rhythms · doi:10.1177/074873049801300406 · Cited by 29
“This revealed either a small effect (Davis and Gorski, 1985, 1986) or no effect (Davis and Gorski, 1988; Viswanathan and Davis, 1992; Grosse et al., 1996), depending on the individual study.”
BackgroundInfluentialGrosse, J., & Davis, F. C. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00162-2 · Cited by 28
“postnatal days (PN) 1–5, but not on PN 6–10 [8,16].”
BackgroundMethodResultInfluentialSelf-citationSchuhler, S., Pitrosky, B., Kirsch, R., & Pévet, P. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00017-7 · Cited by 28
Duffield, Hastings, M. H., & Ebling, E. (1998) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1998.00274.x · Cited by 28
Grosse, J., & Davis, F. C. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-19-08032.1998 · Cited by 26
“Second, because the ability of melatonin to entrain the rhythms of neonatal hamsters is lost after postnatal day 5 (P5) (Grosse et al., 1996), and melatonin binding site density falls during postnatal development (Duncan and Davis, 1993), the effect of melatonin injections on more established grafts was also examined.”
BackgroundMethodResultInfluentialSelf-citationDevelopment of Mammalian Circadian Rhythms
Davis, F. C., & Reppert, S. M. (2001) · Handbook of behavioral neurobiology · doi:10.1007/978-1-4615-1201-1_10 · Cited by 25
Self-citationMaternal entrainment in the circadian activity rhythm of laboratory mouse (C57BL/6J)
Viswanathan, N. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00157-2 · Cited by 25
Rajaratnam, S. M. W., & Redman, J. R. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200406 · Cited by 21
Schurov, I., Hepworth, T. J., & Hastings, M. H. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01848.x · Cited by 17
“In the Syrian hamster, these cues cease to be effective entraining signals 1 week after birth (Grosse et al., 1996), at which point retinal innervation to the SCN is complete and the expression of melatonin receptors in the SCN is reduced markedly (Maywood et al., 1995).”
BackgroundKolker, D. E., Olson, S. L., Dutton-Boilek, J., Bennett, K. M., Wallen, E. P., Horton, T. H., & Turek, F. W. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00362.2001 · Cited by 13
“Although melatonin can entrain the pacemaker of neonatal golden hamsters (9), adult hamsters show little or no phase shifts in response to melatonin (3, 9, 41).”
BackgroundThe Roles of Melatonin in Development
Weaver, D. R. (2002) · Advances in experimental medicine and biology · doi:10.1007/0-306-46814-x_22 · Cited by 12
Cellular and molecular mechanisms mediating melatonin action: A review
Olcese, J. (1998) · The Aging Male · doi:10.3109/13685539809148610 · Cited by 12
Circadian Activity Rhythms and Phase‐Shifting of Cultured Neurons of the Rat Suprachiasmatic Nucleus
Klisch, C., Mahr, S., & Meissl, H. (2006) · Chronobiology International · doi:10.1080/07420520500464502 · Cited by 10
“However, in the Syrian hamster, in vivo administration of melatonin entrains circadian rhythms only in fetal and neonatal, but not in adult, hamsters (Grosse et al., 1996; Hastings et al., 1992).”
BackgroundGaridou, M., Ribelayga, C., Pévet, P., et al. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00850.x · Cited by 9
Melatonin Regulation of Circadian Rhythmicity in Vertebrates
Weaver, D. R., & Lockley, S. W. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.01608-9 · Cited by 7
Gauer, F., Schuster, C., Poirel, V., et al. (2005) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-46814-x_29 · Cited by 5
Melatonin Regulation of Circadian Rhythmicity in Vertebrates☆
Weaver, D. R., & Lockley, S. W. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.02297-5 · Cited by 2
Diversity in the Circadian Response to Melatonin in Mammals
Rajaratnam, S. M. W., & Redman, J. (2002) · Springer eBooks · doi:10.1007/978-3-662-06085-8_19 · Cited by 1
Development of Circadian Time Structure and Blood Pressure Rhythms
Haus, E. L., & Smolensky, M. H. (2004) · Humana Press eBooks · doi:10.1007/978-1-59259-797-0_3 · Cited by 1
“, melatonin [38], cortisol [39], and dopamine [40]) act as entraining agents of fetal rhythms.”
BackgroundEpigenetic Control of Circadian Clock Operation during Development
Li, C., Gong, C., Yu, S., Wu, J., & Li, X. (2012) · Genetics Research International · doi:10.1155/2012/845429
“Light signaling to the central clock in the SCN has been shown to cause MeCP2 phosphorylation [103], in addition to inducing histone modifications that parallel the induction of immediate early genes [104].”
Influential
Metadata
- Authors
- Grosse, J., Velickovic, A., & Davis, F. C.
- Affiliations
- Northeastern University (US)
- Venue
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
- Publisher
- American Physiological Society
- Published
- 1996-03-01
- Volume
- 270
- Issue
- 3
- Pages
- R533-R540
- ISSN
- 0363-6119 (ISSN-L)
- 1522-1490
- OpenAlex
- W2200251599
- Cited by
- 47
- References
- 0
- Citations by year
- 2022: 1 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 1 · 2012: 1
- FWCI
- 1.96
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 18686)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- melatonin, circadian entrainment, neonatal development, golden hamster, activity rhythms, suprachiasmatic nucleus, pineal gland, postnatal development, weaning
- MeSH terms
- Animals, Animals, Newborn, Circadian Rhythm, Female, Cricetinae, Male, Melatonin, Mesocricetus, Pregnancy, Suprachiasmatic Nucleus
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