Moderate neonatal stress decreases within-group variation in behavioral, immune and HPA responses in adult mice
Open accessAbstract
BACKGROUND: The significance of behavioral neuroscience and the validity of its animal models of human pathology largely depend on the possibility to replicate a given finding across different laboratories. Under the present test and housing conditions, this axiom fails to resist the challenge of experimental validation. When several mouse strains are tested on highly standardized behavioral test batteries in different laboratories, significant strain x lab interactions are often detected. This limitation, predominantly due to elevated within-group variability observed in control subjects, increases the number of animals needed to address fine experimental questions. Laboratory rodents display abnormal stress and fear reactions to experimental testing, which might depend on the discrepancy between the stability of the neonatal environment and the challenging nature of the adult test and housing conditions. METHODOLOGY/PRINCIPAL FINDINGS: Stimulating neonatal environments (e.g. brief maternal separations, increased foraging demands or maternal corticosterone supplementation) reduce stress and fear responses in adulthood. Here we tested whether reduced fearfulness associated with experimental testing would also reduce inter-individual variation. In line with our predictions, we show that a moderate elevation in neonatal corticosterone through maternal milk significantly reduces fear responses and inter-individual variability (average 44%) in adult mouse offspring. CONCLUSIONS/SIGNIFICANCE: We observed reduced variation in pain perception, novelty preference, hormonal stress response and resistance to pathogen infection. This suggests that the results of this study may apply to a relatively broad spectrum of neuro-behavioral domains. Present findings encourage a reconsideration of the basic principles of neonatal housing systems to improve the validity of experimental models and reduce the number of animals used.
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Cites
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
The Neuroendocrinology of Stress: A Never Ending Story
Lightman, S. L. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01711.x · Cited by 3,570 · see citing works
Nestler, E. J., Barrot, M., DiLeone, R. J., Eisch, A. J., Gold, S. J., & Monteggia, L. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00653-0 · Cited by 3,217 · see citing works
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Developmental plasticity and human health
Bateson, P., Barker, D., Clutton-Brock, T., Deb, D., D'Udine, B., Foley, R. A., Gluckman, P., Godfrey, K., Kirkwood, T., Lahr, M. M., et al. (2004) · Nature · doi:10.1038/nature02725 · Cited by 1,742 · see citing works
Genetics of Mouse Behavior: Interactions with Laboratory Environment
Crabbe, J. C., Wahlsten, D., & Dudek, B. C. (1999) · Science · doi:10.1126/science.284.5420.1670 · Cited by 1,666 · see citing works
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Sapolsky, R. M. (1994) · Medical Entomology and Zoology · Cited by 971 · see citing works
Population density and social pathology.
Calhoun, J. B. (1962) · PubMed · doi:10.1038/scientificamerican0262-139 · Cited by 743 · see citing works
Laviola, G., Macrı̀, S., Morley-Fletcher, S., & Adriani, W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00006-x · Cited by 621 · see citing works
Self-citationCaldji, C. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00110-4 · Cited by 606 · see citing works
Current Protocols in Toxicology
(2001) · John Wiley & Sons, Inc. eBooks · doi:10.1002/0471140856 · Cited by 522 · see citing works
Ideal homes? Housing effects on rodent brain and behaviour
Würbel, H. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01718-5 · Cited by 471 · see citing works
Pryce, C. R., & Feldon, J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00009-5 · Cited by 460 · see citing works
Garner, J. P. (2005) · ILAR Journal · doi:10.1093/ilar.46.2.106 · Cited by 329 · see citing works
Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.022 · Cited by 320 · see citing works
Wahłsten, D., Bachmanov, A. A., Finn, D. A., & Crabbe, J. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605342103 · Cited by 280 · see citing works
The postnatal development of the hypothalamic–pituitary–adrenal axis in the mouse
Schmidt, M. V., Enthoven, L., van der Mark, M. H., Levine, S. D., de Kloet, E. R., & Oitzl, M. S. (2003) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(03)00030-3 · Cited by 271 · see citing works
Macrı̀, S., & Würbel, H. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.015 · Cited by 253 · see citing works
Self-citationAdriani, W., Chiarotti, F., & Laviola, G. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.5.1152 · Cited by 247 · see citing works
Self-citationCage enrichment and mouse behaviour
Wolfer, D. P., Litvin, O. I., Morf, S., Nitsch, R. M., Lipp, H., & Würbel, H. (2004) · Nature · doi:10.1038/432821a · Cited by 245 · see citing works
Griebel, G., Belzung, C., Misslin, R., & Vogel, E. (1993) · Behavioural Pharmacology · doi:10.1097/00008877-199312000-00009 · Cited by 239 · see citing works
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 237 · see citing works
Self-citationAdriani, W., Chiarotti, F., & Laviola, G. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.5.1152 · Cited by 230 · see citing works
Self-citationA refined method for sequential blood sampling by tail incision in rats
Fluttert, M., Dalm, S., & Oitzl, M. S. (2000) · Laboratory Animals · doi:10.1258/002367700780387714 · Cited by 227 · see citing works
Galsworthy, M. J., Amrein, I., Kuptsov, P. A., Полетаева, И. И., Zinn, P. O., Rau, A., Vyssotski, A. L., & Lipp, H. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.06.021 · Cited by 171 · see citing works
Catalani, A., Casolini, P., Scaccianoce, S., Patacchioli, F. R., Spinozzi, P., & Angelucci, L. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00277-3 · Cited by 140 · see citing works
Novel approach to the behavioural characterization of inbred mice: automated home cage observations
de Visser, L., van den Bos, R., Kuurman, W. W., Kas, M. J., & Spruijt, B. M. (2005) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2005.00181.x · Cited by 135 · see citing works
Catalani, A., Marinelli, M., Scaccianoce, S., Nicolai, R., Muscolo, L. A. A., Porcu, A., Kora´nyi, L., Piazza, P. V., & Angelucci, L. (1993) · Brain Research · doi:10.1016/0006-8993(93)90079-3 · Cited by 133 · see citing works
Roy, V., & Chapillon, P. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.03.010 · Cited by 104 · see citing works
Environmental Enrichment, Immunocompetence, and Resistance to Babesia microti in Male Mice
Barnard, C. J., Behnke, J. M., & SEWELL, J. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00174-6 · Cited by 100 · see citing works
Maternal Mediation of Early Experience
Smotherman, W. P., & Bell, R. W. (1980) · Springer eBooks · doi:10.1007/978-94-011-6287-6_8 · Cited by 100 · see citing works
Carter, R. B. (1991) · Pain · doi:10.1016/0304-3959(91)90207-e · Cited by 91 · see citing works
Individual differences in the hotplate test and effects of habituation on sensitivity to morphine
Plone, M. A., Emerich, D. F., & Lindner, M. D. (1996) · Pain · doi:10.1016/0304-3959(96)03048-5 · Cited by 76 · see citing works
Tsai, P. P., Stelzer, H. D., Hedrich, H. J., & Hackbarth, H. (2003) · Laboratory Animals · doi:10.1258/002367703322389889 · Cited by 75 · see citing works
Pieretti, S., d’Amore, A., & Loizzo, A. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.1.215 · Cited by 62 · see citing works
Self-citationLéonhardt, M., Matthews, S. G., Meaney, M. J., & Walker, C. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.08.008 · Cited by 60 · see citing works
Role of dopamine D₁ and D₂ receptors in novelty-maintained place preference.
Bardo, M. T., Bowling, S. L., Robinet, P. M., Rowlett, J. K., Lacy, M., & Mattingly, B. A. (1993) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.1.1-4.101 · Cited by 55 · see citing works
Pieretti, S., d’Amore, A., & Loizzo, A. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.1.215 · Cited by 49 · see citing works
Self-citationMacrı̀, S., & Würbel, H. (2006) · Animal Behaviour · doi:10.1016/j.anbehav.2006.03.029 · Cited by 47 · see citing works
Self-citationAntinociceptive activity of a 3(2H)-pyridazinone derivative in mice
Pieretti, S., Piaz, V. D., Matucci, R., Giovannoni, M. P., & Galli, A. (1999) · Life Sciences · doi:10.1016/s0024-3205(99)00377-x · Cited by 44 · see citing works
Self-citationMethods in the Analysis of Maternal Behavior in the Rodent
Capone, F. T., Bonsignore, L. T., & Cirulli, F. (2005) · Current Protocols in Toxicology · doi:10.1002/0471140856.tx1309s26 · Cited by 37 · see citing works
Self-citationPasquali, P., Adone, R., Pistoia, C., Petrucci, P., & Ciuchini, F. (2003) · Infection and Immunity · doi:10.1128/iai.71.5.2326-2330.2003 · Cited by 37 · see citing works
Self-citationYorty, J. L., Schultz, S. A., & Bonneau, R. H. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.01.012 · Cited by 29 · see citing works
Consummatory behaviors and weight regulation in pregnant, lactating, and pregnant-lactating mice.
Biggerstaff, S., & Mann, M. A. (1992) · Physiology and Behavior · doi:10.1016/0031-9384(92)90335-y · Cited by 12 · see citing works
Early experience and parent-of-origin-specific effects influence female reproductive success in mice
Hager, R., & Johnstone, R. A. (2006) · Biology Letters · doi:10.1098/rsbl.2006.0457 · Cited by 8 · see citing works
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The Adaptive Calibration Model of stress responsivity
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.11.007 · Cited by 1,373 · see citing works
Measuring behavior in mice with chronic stress depression paradigm
Strekalova, T., & Steinbusch, H. W. M. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.12.014 · Cited by 207 · see citing works
Foster, M. T., Warne, J. P., Ginsberg, A. B., Horneman, H. F., Pecoraro, N. C., Akana, S. F., & Dallman, M. F. (2008) · Endocrinology · doi:10.1210/en.2008-1426 · Cited by 182 · see citing works
Goerlich, V. C., Nätt, D., Elfwing, M., Macdonald, B., & Jensen, P. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.03.006 · Cited by 165 · see citing works
Update in the methodology of the chronic stress paradigm: internal control matters
Strekalova, T., Couch, Y., Kholod, N., Boyks, M., Malin, D., Leprince, P., & Steinbusch, H. M. (2011) · Behavioral and Brain Functions · doi:10.1186/1744-9081-7-9 · Cited by 163 · see citing works
Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models
Marco, E. M., Macrì, S., & Laviola, G. (2011) · Neurotoxicity Research · doi:10.1007/s12640-010-9205-z · Cited by 144 · see citing works
Self-citationThe role of constraints and limitation in driving individual variation in immune response
Ardia, D. R., Parmentier, H. K., & Vogel, L. A. (2010) · Functional Ecology · doi:10.1111/j.1365-2435.2010.01759.x · Cited by 130 · see citing works
The maternal deprivation animal model revisited.
Marco, E. M., Llorente, R., López-Gallardo, M., Mela, V., Llorente-Berzal, Á., Prada, C., & Viveros, M.-P. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.015 · Cited by 132 · see citing works
Macrı̀, S., Zoratto, F., & Giovanni Laviola, A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.014 · Cited by 118 · see citing works
Self-citationFetal programming by maternal stress: Insights from a conflict perspective
Giudice, M. D. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.05.014 · Cited by 112 · see citing works
Catalani, A., Alemà, G., Cinque, C., Zuena, A. R., & Casolini, P. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.017 · Cited by 106 · see citing works
Cirulli, F., Berry, A., Bonsignore, L. T., Capone, F., D’Andrea, I., Aloe, L., Branchi, I., & Alleva, E. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.008 · Cited by 105 · see citing works
Self-citationEffects of early stress on behavioral syndromes: An integrated adaptive perspective
Sih, A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.015 · Cited by 99 · see citing works
Marco, E. M., Adriani, W., Llorente, R., Giovanni Laviola, A., & Viveros, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.008 · Cited by 95 · see citing works
Chemical signals in terrestrial vertebrates: search for design features.
Apps, P., Weldon, P., & Kramer, M. (2015) · Natural product reports (Print) · doi:10.1039/c5np00029g · Cited by 80 · see citing works
Hauser, J., Pisa, E., Vásquez, A. A., Tomasi, F., Traversa, A., Chiodi, V., Martin, F., Sprenger, N., Lukjančenko, O., Zollinger, A., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01054-9 · Cited by 91 · see citing works
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Macrı̀, S., Granstrem, O., Shumilina, M. V., Santos, F. J., Berry, A., Saso, L., & Giovanni Laviola, A. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.07.006 · Cited by 64 · see citing works
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Bartolini, T., Mwaffo, V., Showler, A., Macrı̀, S., Butail, S., & Porfiri, M. (2016) · Bioinspiration & Biomimetics · doi:10.1088/1748-3190/11/2/026003 · Cited by 51 · see citing works
Self-citationPerinatal Flavour Learning and Adaptation to Being Weaned: All the Pig Needs Is Smell
Oostindjer, M., Bolhuis, J. E., Simon, K., van den Brand, H., & Kemp, B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025318 · Cited by 49 · see citing works
Krolow, R., Noschang, C. G., Arcego, D. M., Andreazza, A. C., Peres, W., Gonçalves, C. A., & Dalmaz, C. (2010) · Appetite · doi:10.1016/j.appet.2010.03.013 · Cited by 44 · see citing works
Zoratto, F., Fiore, M., Ali, S. F., Giovanni Laviola, A., & Macrı̀, S. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.04.015 · Cited by 39 · see citing works
Self-citationCoutellier, L. D., Friedrich, A.-C., Failing, K., Marashi, V., & Würbel, H. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.08.042 · Cited by 35 · see citing works
Hormonal and nutritional regulation of postnatal hypothalamic development
Sominsky, L., Jasoni, C. L., Twigg, H., & Spencer, S. J. (2018) · Journal of Endocrinology · doi:10.1530/joe-17-0722 · Cited by 34 · see citing works
Macrı̀, S., Ceci, C., Altabella, L., Canese, R., & Giovanni Laviola, A. (2013) · Scientific Reports · doi:10.1038/srep02380 · Cited by 31 · see citing works
Self-citationFilippis, B. D., Ricceri, L., Fuso, A., & Giovanni Laviola, A. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.05.048 · Cited by 31 · see citing works
Macrı̀, S., Ceci, C., Onori, M. P., Invernizzi, R. W., Bartolini, E., Altabella, L., Canese, R., Imperi, M., Orefici, G., Creti, R., et al. (2015) · Scientific Reports · doi:10.1038/srep13257 · Cited by 30 · see citing works
Self-citationThe Snark was a Boojum - reloaded
Macrı̀, S., & Richter, S. H. (2015) · Frontiers in Zoology · doi:10.1186/1742-9994-12-s1-s20 · Cited by 25 · see citing works
Self-citationZoratto, F., Berry, A., Anzidei, F., Fiore, M., Alleva, E., Giovanni Laviola, A., & Macrı̀, S. (2011) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2011.02.016 · Cited by 24 · see citing works
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Romeo, R., Tang, A. C., & Sullivan, R. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00062-0 · Cited by 30 · see citing works
Bauer, C. M., Hayes, L. D., Ebensperger, L. A., Ramírez‐Estrada, J., León, C., Davis, G. T., & Romero, L. M. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.021 · Cited by 22 · see citing works
Macrì, S., Ceci, C., Canese, R., & Laviola, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041821 · Cited by 20 · see citing works
Self-citationBauer, C. M., Ebensperger, L. A., León, C., Ramírez‐Estrada, J., Hayes, L. D., & Romero, L. M. (2016) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.2018 · Cited by 19 · see citing works
Macrı̀, S., Lanuzza, L., Merola, G., Ceci, C., Gentili, S., Valli, A., Macchia, T., & Giovanni Laviola, A. (2013) · Neurotoxicity Research · doi:10.1007/s12640-012-9371-2 · Cited by 19 · see citing works
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Factors of Reproducibility of Anhedonia Induction in a Chronic Stress Depression Model in Mice
Strekalova, T. V., & Steinbusch, H. W. M. (2009) · Neuromethods · doi:10.1007/978-1-60761-303-9_9 · Cited by 17 · see citing works
Archer, T., Kostrzewa, R. M., Beninger, R. J., & Palomo, T. (2010) · Neurotoxicity Research · doi:10.1007/s12640-010-9162-6 · Cited by 16 · see citing works
Ceci, C., Mela, V., Macrı̀, S., Marco, E. M., Viveros, M., & Laviola, G. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3367-3 · Cited by 15 · see citing works
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Self-citationOn the incongruity between developmental plasticity and methodological rigidity
Macrı̀, S. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00093 · Cited by 10 · see citing works
Self-citationWu, R., Li, S., Huang, Y., Pang, J., Cai, Y., Zhang, X., Jiang, T., Yang, S., & Wei, W. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113532 · Cited by 11 · see citing works
Grindstaff, J. L., & Merrill, L. (2017) · Journal of Experimental Zoology Part A Ecological and Integrative Physiology · doi:10.1002/jez.2086 · Cited by 9 · see citing works
Zebrafish exhibit associative learning for an aversive robotic stimulus
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Self-citationMacrı̀, S. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.12.001 · Cited by 7 · see citing works
Self-citationWynne, O., Horvat, J. C., Kim, R., Ong, L. K., Smith, R., Hansbro, P. M., Clifton, V. L., & Hodgson, D. M. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.03.014 · Cited by 6 · see citing works
Critical Age Windows for Neurodevelopmental Psychiatric Disorders: Evidence from Animal Models
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Self-citationTomacheuski, R. M., Taffarel, M. O., Ferrante, M., & Luna, S. P. L. (2020) · Veterinary Anaesthesia and Analgesia · doi:10.1016/j.vaa.2020.05.007 · Cited by 5 · see citing works
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RHODES, E. L. (2016) · CU Scholar (University of Colorado Boulder)
- Authors
- Macrì, S., Pasquali, P., Bonsignore, L. T., Pieretti, S., Cirulli, F., Chiarotti, F., & Laviola, G.
- Affiliations
- Istituto Superiore di Sanità (IT)
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2007-10-10
- Volume
- 2
- Issue
- 10
- Pages
- e1015
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2000350
- OpenAlex
- W1999466466
- Cited by
- 60
- References
- 44
- Citations by year
- 2026: 1 · 2023: 1 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 2 · 2016: 6 · 2015: 5 · 2014: 1 · 2013: 5 · 2012: 5
- FWCI
- 2.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- neonatal stress, maternal corticosterone, interindividual variability, fear response, hypothalamic-pituitary-adrenal axis, immune response, novelty preference, pain perception, maternal separation, breast milk, animal model validity
- MeSH terms
- Adrenal Cortex Hormones, Animals, Animals, Newborn, Behavior, Animal, Female, Hypothalamo-Hypophyseal System, Immune System, Male, Pain, Pituitary-Adrenal System, Pregnancy, Research Design, Species Specificity, Genetic Variation, Mice
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