The DOI matches its Crossref record; 45 of the 45 references it cites were found in a registry or an index.
Behavioural and Neurochemical Consequences of Early Weaning in Rodents
Abstract
Among all mammalian species, pups are highly dependent on their mother not only for nutrition, but also for physical interaction. Therefore, disruption of the mother-pup interaction changes the physiology and behaviour of pups. We review how maternal separation in the early developmental period brings about changes in the behaviour and neuronal systems of the offspring of rats and mice. Early weaning in mice results in adulthood a persistent increase in anxiety-like and aggressive behaviour. The early-weaned mice also show higher hypothalamic-pituitary-adrenal activity in response to novelty stress. Neurochemically, the early-weaned male mice, but not female mice, show precocious myelination in the amygdala, decreased brain-derived neurotrophic factor protein levels in the hippocampus and prefrontal cortex, and reduced bromodeoxyuridine immunoreactivity in the dentate gyrus. Because higher corticosterone levels are persistently observed up to 48 h when the mice are weaned on postnatal day 14, the exposure of the developing brain to higher corticosterone levels may be one of the effects of early weaning. These results suggest that deprivation of the mother-infant interaction during the late lactating period results in behavioural and neurochemical changes in adulthood and that these stress responses are sexually dimorphic (i.e. the male is more vulnerable to early weaning stress).
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?
In the citing paper
“Maternal separation in rodent pups is associated with greater LHPA axis reactivity (Moriceau et al., 2010), accelerated amygdala development (Moriceau and Sullivan, 2006, Ono et al., 2008), increased anxiety-like behaviors (Romeo et al., 2003), and more social instability in adulthood (Kikusui and Mori, 2009).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Kikusui and Mori, 2009
Citations
Cites
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170
Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus
Malberg, J. E., Eisch, A. J., Nestler, E. J., & Duman, R. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09104.2000 · Cited by 3,111
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965
Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action
Tsankova, N. M., Berton, O., Renthal, W., Kumar, A., Neve, R. L., & Nestler, E. J. (2006) · Nature Neuroscience · doi:10.1038/nn1659 · Cited by 1,780
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638
Maternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195
Adult brain neurogenesis and psychiatry: a novel theory of depression
Jacobs, B. L., van Praag, H., & Gage, F. H. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000712 · Cited by 964
Bremner, J. D., Vythilingam, M., Vermetten, E. H. G. J. M., Southwick, S. M., McGlashan, T. H., Nazeer, A., Khan, S., Vaccarino, V., Soufer, R., Garg, P. K., et al. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.5.924 · Cited by 755
Long-term behavioral and neuroendocrine adaptations to adverse early experience
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky, P. M. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62132-9 · Cited by 726
Maternal care and the development of stress responses
Francis, D. D., & Meaney, M. J. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80016-6 · Cited by 683
Early life experience alters response of adult neurogenesis to stress
Mirescu, C., Peters, J. D., & Gould, E. (2004) · Nature Neuroscience · doi:10.1038/nn1290 · Cited by 625
Ladd, C. O., Owens, M. J., & Nemeroff, C. (1996) · Endocrinology · doi:10.1210/endo.137.4.8625891 · Cited by 536
Liu, Caldji, Sharma, Plotsky, & Meaney (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00422.x · Cited by 456
Wigger, A., & Neumann, I. D. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00300-x · Cited by 443
Agonistic Behavior of Mice and Rats: A Review
Scott, J. G. (1966) · American Zoologist · doi:10.1093/icb/6.4.683 · Cited by 430
Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats
Huot, R. L., Plotsky, P. M., Lenox, R. H., & McNamara, R. K. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02985-2 · Cited by 392
Weaver, I. C. G., Diorio, J. C., Seckl, J. R., Szyf, M., & Meaney, M. J. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1321.099 · Cited by 332
Maternal Care, Gene Expression, and the Development of Individual Differences in Stress Reactivity
Francis, D. D., Champagne, F. A., Liu, D., & Meaney, M. J. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08106.x · Cited by 296
Romeo, R. D., Mueller, A., Sisti, H. M., Ogawa, S., McEwen, B. S., & Brake, W. G. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00063-1 · Cited by 285
Glucocorticoids and progestins signal the initiation and enhance the rate of myelin formation
Chan, J. R., Phillips, L. J., & Gläser, M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10459 · Cited by 177
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175
Fish, E. W., Faccidomo, S., & Miczek, K. A. (1999) · Psychopharmacology · doi:10.1007/pl00005484 · Cited by 161
Psychosocial stress, glucocorticoids, and structural alterations in the tree shrew hippocampus
Fuchs, E., Flügge, G., Ohl, F., Lucassen, P. J., Vollmann-Honsdorf, G. K., & Michaelis, T. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00497-8 · Cited by 150
de Almeida, R. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00291-9 · Cited by 149
Ono, M., Kikusui, T., Sasaki, N., Ichikawa, M., Mori, Y., & Murakami-Murofushi, K. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.078 · Cited by 149
Self-citationCaldji, C., Diorio, J. C., Anisman, H., & Meaney, M. J. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300436 · Cited by 145
Kikusui, T., Ichikawa, S., & Mori, Y. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.12.009 · Cited by 115
Self-citationPlay in the domestic cat is enhanced by rationing of the mother during lactation
Bateson, P., Mendl, M., & Feaver, J. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80532-9 · Cited by 112
Weaning in rats: I. Maternal behavior
Cramer, C. P., Thiels, E., & Alberts, J. R. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230604 · Cited by 100
Kikusui, T., Isaka, Y., & Mori, Y. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.013 · Cited by 100
Self-citationMultidimensional structure of anxiety-related behavior in early-weaned rats
Kanari, K., Kikusui, T., Takeuchi, Y., & Mori, Y. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.008 · Cited by 90
Self-citationEarly weaning augments neuroendocrine stress responses in mice
Kikusui, T., Nakamura, K., Kakuma, Y., & Mori, Y. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.007 · Cited by 85
Self-citationKikusui, T., Faccidomo, S., & Miczek, K. A. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1989-1 · Cited by 83
Self-citationKikusui, T., Kiyokawa, Y., & Mori, Y. (2006) · Brain Research · doi:10.1016/j.brainres.2006.11.031 · Cited by 78
Self-citationAkiyama, K., Ichinose, S., Omori, A., Sakurai, Y., & Asou, H. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10188 · Cited by 64
Effects of early weaning on anxiety and autonomic responses to stress in rats
Ito, A., Kikusui, T., Takeuchi, Y., & Mori, Y. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.03.023 · Cited by 62
Self-citationDifferences in maternal behavior of rats and the sociosexual development of the offspring
Birke, L. I. A., & Sadler, D. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200111 · Cited by 58
Smith, E. F. S. (1991) · Animal Behaviour · doi:10.1016/s0003-3472(05)80854-1 · Cited by 50
∂-Opioid modulation of social interactions in juvenile mice weaned at different ages
Terranova, M. L., & Giovanni Laviola, A. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00447-4 · Cited by 49
Effects of cohabitation with females on aggressive behavior between male mice
Goyens, J., & Noirot, É. (1975) · Developmental Psychobiology · doi:10.1002/dev.420080111 · Cited by 48
Early separation of young rats from the mother and the development of play fighting
Janus, K. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90375-1 · Cited by 46
Shimozuru, M., Kodama, Y., Iwasa, T., Kikusui, T., Takeuchi, Y., & Mori, Y. (2007) · Developmental Psychobiology · doi:10.1002/dev.20202 · Cited by 44
Self-citationNakamura, K., Kikusui, T., TAKEUCHI, Y., & MORI, Y. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.10.002 · Cited by 43
Self-citationEffects of mother-litter separation on survival, growth, and brain amino acid levels
Plaut, S. M., & Davis, J. M. (1972) · Physiology & Behavior · doi:10.1016/0031-9384(72)90128-x · Cited by 38
The Influence of Early Weaning on Aggressive Behavior in Mice
Nakamura, K., Kikusui, T., Takeuchi, Y., & Mori, Y. (2003) · Journal of Veterinary Medical Science · doi:10.1292/jvms.65.1347 · Cited by 29
Self-citation
Research works printed but not linked: 2
- Crowcroft P, 1966, Mice all over
- Novakova V, 1975, Maternal behavior in normally and prematurely weaned female laboratory rats, Physiol Bohemoslov, 24, 73
Cited by
Sorted by citations
Epigenetic transmission of the impact of early stress across generations
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., Vizi, S., & Mansuy, I. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.036 · Cited by 1,125
Heim, C., & Binder, E. B. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2011.10.032 · Cited by 986
A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing
Tottenham, N. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.068.2009 · Cited by 651
Elevated amygdala response to faces following early deprivation
Tottenham, N., Hare, T. A., Millner, A., Gilhooly, T., Zevin, J. D., & Casey, B. J. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.00971.x · Cited by 468
Lupien, S. J., Parent, S., Evans, A. C., Tremblay, R. E., Zelazo, P. D., Corbo, V., Pruessner, J. C., & Séguin, J. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105371108 · Cited by 379
Metadata
- Authors
- Kikusui, T., & Mori, Y.
- Affiliations
- Azabu University (JP)
- Corresponding author
- Kikusui, T.
- ORCID
- Kikusui, T.
- Venue
- Journal of Neuroendocrinology
- Publisher
- Wiley
- Published
- 2009-03-27
- Volume
- 21
- Issue
- 4
- Pages
- 427-431
- ISSN
- 0953-8194 (ISSN-L)
- 1365-2826
- OpenAlex
- W2037070770
- Cited by
- 158
- References
- 45
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 8 · 2023: 6 · 2022: 5 · 2021: 11 · 2020: 11 · 2019: 10 · 2018: 9 · 2017: 15 · 2016: 9 · 2015: 9 · 2014: 11 · 2013: 14 · 2012: 16
- FWCI
- 0.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- early weaning, maternal separation, mother-pup interaction, anxiety-like behavior, aggression, hypothalamic-pituitary-adrenal axis, novelty stress, corticosterone, amygdala, brain-derived neurotrophic factor, hippocampus, prefrontal cortex, dentate gyrus, sexual dimorphism, developmental stress, rats, mice
- MeSH terms
- Aggression, Animals, Anxiety, Brain, Corticosterone, Female, Male, Maternal Deprivation, Myelin Sheath, Play and Playthings, Sex Characteristics, Sex Factors, Stress, Psychological, Time Factors, Weaning, Brain-Derived Neurotrophic Factor, Neurogenesis
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