CoChat
Sign Up
Cited by 11Stress Responses and CortisolNeuroendocrine regulation and behaviorChild Abuse and Trauma

Early life adversity reduces affiliative behavior with a stressed cagemate and leads to sex-specific alterations in corticosterone responses in adult mice

Open access
Breton, Jocelyn M., Cort, Zoey, Demaestri, Camila, Critz, Madalyn, Nevins, Samuel, Downend, Kendall, Ofray, Dayshalis, Romeo, Russell D. +1 more·2024·Hormones and Behavior
DOI 10.1016/j.yhbeh.2023.105464PMC PMC10872397

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Experiencing early life adversity (ELA) alters stress physiology and increases the risk for developing psychiatric disorders. The social environment can influence dynamics of stress responding and buffer and/or transfer stress across individuals. Yet, the impact of ELA on sensitivity to the stress of others and social behavior following stress is unknown. Here, to test the impact of ELA on social and physiological responses to stress, circulating blood corticosterone (CORT) and social behaviors were assessed in adult male and female mice reared under limited bedding and nesting (LBN) or control conditions. To induce stress, one cagemate of a pair-housed cage underwent a footshock paradigm and was then returned to their unshocked partner. CORT was measured in both mice 20 or 90 minutes after stress exposure, and social behaviors were recorded and analyzed. ELA rearing influenced the CORT response to stress in a sex-specific manner. In males, both control and ELA-reared mice exhibited similar stress transfer to unshocked cagemates and similar CORT dynamics. In contrast, ELA females showed a heightened stress transfer to unshocked cagemates, and sustained elevation of CORT relative to controls, indicating enhanced stress contagion and a failure to terminate the stress response. Behaviorally, ELA females displayed decreased allogrooming and increased investigative behaviors, while ELA males showed reduced huddling. Together, these findings demonstrate that ELA influenced HPA axis dynamics, social stress contagion and social behavior. Further research is needed to unravel the underlying mechanisms and long-term consequences of ELA on stress systems and their impact on behavioral outcomes.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.yhbeh.2023.105464

Cites

13 of 13 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 93

  1. An X-L, Zou J-X, Wu R-Y, Yang Y, Tai F-D, Zeng S-Y, Jia R, Zhang X, Liu E-Q, Broders H, 2011. Strain and sex differences in anxiety-like and social behaviors in C57BL/6J and BALB/cJ mice. Exp. Anim. 60, 111– 123. 10.1538/expanim.60.111. 21512266 · DOI
  2. Ardizzi M, Umiltà MA, Evangelista V, Di Liscia A, Ravera R, Gallese V, 2016. Less empathic and more reactive: the different impact of childhood maltreatment on facial mimicry and vagal regulation. PloS One 11, e0163853. 10.1371/journal.pone.0163853. 27685802 PMC5042550 · DOI
  3. Avishai-Eliner S, Hatalski CG, Tabachnik E, Eghbal-Ahmadi M, Baram TZ, 1999. Differential Regulation of Glucocorticoid Receptor Messenger RNA žGR-mRNA/by Maternal Deprivation in Immature Rat Hypothalamus and Limbic Regions. PMC3139462 10320766
  4. Bath KG, 2020. Synthesizing views to understand sex differences in response to early life adversity. Trends Neurosci. 43, 300– 310. 10.1016/j.tins.2020.02.004. 32353334 PMC7195459 · DOI
  5. Bath KG, Manzano-Nieves G, Goodwill H, 2016. Early life stress accelerates behavioral and neural maturation of the hippocampus in male mice. Horm. Behav. 82, 64– 71. 10.1016/j.yhbeh.2016.04.010. 27155103 PMC5308418 · DOI
  6. Beery AK, Kaufer D, 2015. Stress, social behavior, and resilience: insights from rodents. Neurobiol. Stress 1, 116– 127. 10.1016/j.ynstr.2014.10.004. 25562050 PMC4281833 · DOI
  7. Bolton JL, Molet J, Regev L, Chen Y, Rismanchi N, Haddad E, Yang DZ, Obenaus A, Baram TZ, 2018. Anhedonia following early-life adversity involves aberrant interaction of reward and anxiety circuits and is reversed by partial silencing of amygdala corticotropin-releasing hormone gene. Biol. Psychiatry 83, 137– 147. 10.1016/j.biopsych.2017.08.023. 29033027 PMC5723546 · DOI
  8. Bondar NP, Lepeshko AA, Reshetnikov VV, 2018. Effects of early-life stress on social and anxiety-like behaviors in adult mice: sex-specific effects. Behav. Neurol. 2018, e1538931 10.1155/2018/1538931. PMC5818933 29619126 · DOI
  9. Brunson KL, Kramár E, Lin B, Chen Y, Colgin LL, Yanagihara TK, Lynch G, Baram TZ, 2005. Mechanisms of late-onset cognitive decline after early-life stress. J. Neurosci. 25, 9328– 9338. 10.1523/JNEUROSCI.2281-05.2005. 16221841 PMC3100717 · DOI · Paper page
  10. Burkett JP, Andari E, Johnson ZV, Curry DC, De Waal FBM, Young LJ, 2016. Oxytocin-dependent consolation behavior in rodents. Science 351. 10.1126/science.aac4785. PMC4737486 26798013 · DOI · Paper page
  11. Carneiro De Oliveira PE, Carmona IM, Casarotto M, Silveira LM, Oliveira ACB, Canto-de-Souza A, 2022. Mice cohabiting with familiar conspecific in chronic stress condition exhibit methamphetamine-induced locomotor sensitization and augmented consolation behavior. Front. Behav. Neurosci. 16, 835717 10.3389/fnbeh.2022.835717. 35517576 PMC9062221 · DOI
  12. Carnevali L, Montano N, Statello R, Coudé G, Vacondio F, Rivara S, Ferrari PF, Sgoifo A, 2017. Social stress contagion in rats: Behavioural, autonomic and neuroendocrine correlates. Psychoneuroendocrinology 82, 155– 163. 10.1016/j.psyneuen.2017.05.017. 28550792 · DOI
  13. Carpenter T, Grecian SM, Reynolds RM, 2017. Sex differences in early-life programming of the hypothalamic–pituitary–adrenal axis in humans suggest increased vulnerability in females: a systematic review. J. Dev. Orig. Health Dis. 8, 244– 255. 10.1017/S204017441600074X. 28103963 · DOI · Paper page
  14. Demaestri C, Pan T, Critz M, Ofray D, Gallo M, Bath KG, 2020. Type of early life adversity confers differential, sex-dependent effects on early maturational milestones in mice. Horm. Behav. 124, 104763 10.1016/j.yhbeh.2020.104763. 32407728 PMC7487052 · DOI
  15. Demaestri C, Gallo M, Mazenod E, Hong AT, Arora H, Short AK, Stern H, Baram TZ, Bath KG, 2022. Resource scarcity but not maternal separation provokes unpredictable maternal care sequences in mice and both upregulate Crh-associated gene expression in the amygdala. Neurobiol. Stress 20, 100484. 10.1016/j.ynstr.2022.100484. 36120094 PMC9475315 · DOI
  16. DeSantis SM, Baker NL, Back SE, Spratt E, Ciolino JD, Moran-Santa Maria M, Dipankar B, Brady KT, 2011. Gender differences in the effect of early life trauma on hypothalamic-pituitary-adrenal axis functioning. Depress. Anxiety 28, 383– 392. 10.1002/da.20795. 21328636 PMC3243643 · DOI
  17. Du R, Luo W-J, Geng K-W, Li C-L, Yu Y, Wei N, Chen J, 2020. Empathic contagious pain and consolation in laboratory rodents: species and sex comparisons. Neurosci. Bull. 36, 649– 653. 10.1007/s12264-020-00465-y. 31953799 PMC7270450 · DOI
  18. Eck SR, Ardekani CS, Salvatore M, Luz S, Kim ED, Rogers CM, Hall A, Lee DE, Famularo ST, Bhatnagar S, Bangasser DA, 2020. The effects of early life adversity on growth, maturation, and steroid hormones in male and female rats. Eur. J. Neurosci. 52, 2664– 2680. 10.1111/ejn.14609. 31660665 PMC8027906 · DOI
  19. Enthoven L, Schmidt MV, Cheung YH, van der Mark MH, de Kloet ER, Oitzl MS, 2010. Ontogeny of the HPA axis of the CD1 mouse following 24h maternal deprivation at pnd 3. Int. J. Dev. Neurosci. 28, 217– 224. 10.1016/j.ijdevneu.2009.10.006. 19897026 · DOI
  20. Fogelman N, Canli T, 2018. Early life stress and cortisol: a meta-analysis. Horm. Behav. 98, 63– 76. 10.1016/j.yhbeh.2017.12.014. 29289660 · DOI
  21. Fourie MM, Stein DJ, Solms M, Gobodo-Madikizela P, Decety J, 2019. Effects of early adversity and social discrimination on empathy for complex mental states: an fMRI investigation. Sci. Rep. 9, 12959. 10.1038/s41598-019-49298-4. 31506497 PMC6737126 · DOI
  22. Francis D, Diorio J, Liu D, Meaney MJ, 1999. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155– 1158. 10.1126/science.286.5442.1155. 10550053 · DOI · Paper page
  23. Gallo M, Shleifer DG, Godoy LD, Ofray D, Olaniyan A, Campbell T, Bath KG, 2019. Limited bedding and nesting induces maternal behavior resembling both hypervigilance and abuse. Front. Behav. Neurosci. 13, 1– 13. 10.3389/fnbeh.2019.00167. 31402857 PMC6673755 · DOI
  24. Gilles EE, Schultz L, Baram TZ, 1996. Abnormal corticosterone regulation in an immature rat model of continuous chronic stress. Pediatr. Neurol. 15, 114– 119. 10.1016/0887-8994(96)00153-1. 8888044 PMC3415889 · DOI
  25. Gjerstad JK, Lightman SL, Spiga F, 2018. Role of glucocorticoid negative feedback in the regulation of HPA axis pulsatility. Stress 21, 403– 416. 10.1080/10253890.2018.1470238. 29764284 PMC6220752 · DOI · Paper page
  26. Gobinath AR, Mahmoud R, Galea LAM, 2015. Influence of sex and stress exposure across the lifespan on endophenotypes of depression: focus on behavior, glucocorticoids, and hippocampus. Front. Neurosci. 8. PMC4285110 25610363
  27. Goodwill HL, Manzano-Nieves G, LaChance P, Teramoto S, Lin S, Lopez C, Stevenson RJ, Theyel BB, Moore CI, Connors BW, Bath KG, 2018. Early life stress drives sex-selective impairment in reversal learning by affecting parvalbumin interneurons in orbitofrontal cortex of mice. Cell Rep. 25, 2299– 2307.e4. 10.1016/j.celrep.2018.11.010. 30485800 PMC6310486 · DOI
  28. Goodwill HL, Manzano-Nieves G, Gallo M, Lee HI, Oyerinde E, Serre T, Bath KG, 2019. Early life stress leads to sex differences in development of depressive-like outcomes in a mouse model. Neuropsychopharmacology 44, 711– 720. 10.1038/s41386-018-0195-5. 30188513 PMC6372611 · DOI
  29. Grimm S, Wirth K, Fan Y, Weigand A, Gärtner M, Feeser M, Dziobek I, Bajbouj M, Aust S, 2017. The interaction of corticotropin-releasing hormone receptor gene and early life stress on emotional empathy. Behav. Brain Res. 329, 180– 185. 10.1016/j.bbr.2017.04.047. 28461011 · DOI
  30. Gump BB, Matthews KA, 1999. Do background stressors influence reactivity to and recovery from acute stressors? J. Appl. Soc. Psychol. 29, 469– 494. 10.1111/j.1559-1816.1999.tb01397.x. · DOI
  31. Gunnar MR, Hostinar CE, Sanchez MM, Tottenham N, Sullivan RM, 2015. Parental buffering of fear and stress neurobiology: reviewing parallels across rodent, monkey, and human models. Soc. Neurosci. 10, 474– 478. 10.1080/17470919.2015.1070198. 26234160 PMC5198892 · DOI · Paper page
  32. Hall BS, Romeo RD, 2014. The influence of poststress social factors on hormonal reactivity in prepubertal male rats. Dev. Psychobiol. 56, 1061– 1069. 24374653
  33. Heim C, Nemeroff CB, 2001. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49, 1023– 1039. 10.1016/S0006-3223(01)01157-X. 11430844 · DOI · Paper page
  34. Hennessy MB, Kaiser S, Sachser N, 2009. Social buffering of the stress response: diversity, mechanisms, and functions. Front. Neuroendocrinol. Hormones Soc. Behav. 30, 470– 482. 10.1016/j.yfrne.2009.06.001. 19545584 · DOI · Paper page
  35. Herman JP, McKlveen JM, Solomon MB, Carvalho-Netto E, Myers B, 2012. Neural regulation of the stress response: glucocorticoid feedback mechanisms. Brazil. J. Med. Biol. Res. Scielo. PMC3854162 22450375
  36. Hostinar CE, Sullivan RM, Gunnar MR, 2014. Psychobiological mechanisms underlying the social buffering of the hypothalamic–pituitary–adrenocortical axis: a review of animal models and human studies across development. Psychol. Bull. 140, 256– 282. 10.1037/a0032671. 23607429 PMC3844011 · DOI · Paper page
  37. Inagaki H, Nakamura K, Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y, 2009. The volatility of an alarm pheromone in male rats. Physiol. Behav. 96, 749– 752. 10.1016/j.physbeh.2008.12.006. 19135073 · DOI
  38. Iñiguez SD, Flores-Ramirez FJ, Riggs LM, Alipio JB, Garcia-Carachure I, Hernandez MA, Sanchez DO, Lobo MK, Serrano PA, Braren SH, Castillo SA, 2018. Vicarious social defeat stress induces depression-related outcomes in female mice. Biol. Psychiatry 83, 9– 17. 10.1016/j.biopsych.2017.07.014. 28888327 PMC5730407 · DOI
  39. Jeon D, Kim S, Chetana M, Jo D, Ruley HE, Lin SY, Rabah D, Kinet JP, Shin HS, 2010. Observational fear learning involves affective pain system and Ca v 1.2 Ca 2+ channels in ACC. Nat. Neurosci. 13, 482– 488. 10.1038/nn.2504. 20190743 PMC2958925 · DOI · Paper page
  40. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE, 2005. Lifetime prevalence and age-of-onset distributions of. Arch. Gen. Psychiatry 62, 593– 602. 10.1001/archpsyc.62.6.593. 15939837 · DOI · Paper page
  41. Keysers C, Knapska E, Moita MA, Gazzola V, 2022. Emotional contagion and prosocial behavior in rodents. Trends Cogn. Sci. 26, 688– 706. 10.1016/j.tics.2022.05.005. 35667978 · DOI
  42. Kiyokawa Y, 2017. Social odors: alarm pheromones and social buffering. In: Wöhr M., Krach S (Eds.), Social Behavior from Rodents to Humans: Neural Foundations and Clinical Implications, Current Topics in Behavioral Neurosciences. Springer International Publishing, Cham, pp. 47– 65. 10.1007/7854_2015_406. 26602247 · DOI · Paper page
  43. Kiyokawa Y, Hennessy MB, 2018. Comparative studies of social buffering: a consideration of approaches, terminology, and pitfalls. Neurosci. Biobehav. Rev. 86, 131– 141. 10.1016/j.neubiorev.2017.12.005. 29223771 PMC5801062 · DOI
  44. Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y, 2004a. Alarm pheromones with different functions are released from different regions of the body surface of male rats. Chem. Senses 29, 35– 40. 10.1093/chemse/bjh004. 14752038 · DOI
  45. Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y, 2004b. Partner’s stress status influences social buffering effects in rats. Behav. Neurosci. 118, 798– 804. 10.1037/0735-7044.118.4.798. 15301605 · DOI
  46. Knapska E, Nikolaev E, Boguszewski P, Walasek G, Blaszczyk J, Kaczmarek L, Werka T, 2006. Between-subject transfer of emotional information evokes specific pattern of amygdala activation. Proc. Natl. Acad. Sci. U. S. A. 103, 3858– 3862. 10.1073/pnas.0511302103. 16497832 PMC1533786 · DOI
  47. Koss KJ, Gunnar MR, 2018. Annual research review: early adversity, the hypothalamic–pituitary–adrenocortical axis, and child psychopathology. J. Child Psychol. Psychiatr. 59, 327– 346. 10.1111/jcpp.12784. PMC5771995 28714126 · DOI · Paper page
  48. Kudielka BM, Kirschbaum C, 2005. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 69, 113– 132. 10.1016/j.biopsycho.2004.11.009. 15740829 · DOI · Paper page
  49. Lapp HE, Bartlett AA, Zup SL, Hunter RG, Moore CL, 2020. Early experience alters developmental trajectory of central oxytocin systems involved in hypothalamic-pituitary-adrenal axis regulation in Long-Evans rats. Horm. Behav. 126, 104822 10.1016/j.yhbeh.2020.104822. 32730760 · DOI
  50. Laviola G, Zoratto F, Ingiosi D, Carito V, Huzard D, Fiore M, Macrì S, 2017. Low empathy-like behaviour in male mice associates with impaired sociability, emotional memory, physiological stress reactivity and variations in neurobiological regulations. PloS One 12, e0188907. 10.1371/journal.pone.0188907. 29200428 PMC5714342 · DOI
  51. Laviola G, Busdraghi LM, Meschino N, Petrella C, Fiore M, 2021. Aberrant early in life stimulation of the stress-response system affects emotional contagion and oxytocin regulation in adult male mice. IJMS 22, 5039. 10.3390/ijms22095039. 34068684 PMC8126076 · DOI
  52. Lee I-C, Yu T-H, Liu W-H, Hsu K-S, 2021. Social transmission and buffering of hippocampal metaplasticity after stress in mice. J. Neurosci. 41, 1317– 1330. 10.1523/JNEUROSCI.1751-20.2020. 33310752 PMC7888214 · DOI
  53. Li L-F, Yuan W, He Z-X, Wang L-M, Jing X-Y, Zhang J, Yang Y, Guo Q-Q, Zhang X-N, Cai W-Q, Hou W-J, Jia R, Tai F-D, 2019. Involvement of oxytocin and GABA in consolation behavior elicited by socially defeated individuals in mandarin voles. Psychoneuroendocrinology 103, 14– 24. 10.1016/j.psyneuen.2018.12.238. 30605804 · DOI
  54. Lim KY, Hong W, 2023. Neural mechanisms of comforting: prosocial touch and stress buffering. Horm. Behav. 153, 105391 10.1016/j.yhbeh.2023.105391. 37301130 PMC10853048 · DOI
  55. Liu H, Yuan T-F, 2016. Physical interaction is required in social buffering induced by a familiar conspecific. Sci. Rep. 6, 39788. 10.1038/srep39788. 28008991 PMC5180222 · DOI
  56. Lovallo WR, 2013. Early life adversity reduces stress reactivity and enhances impulsive behavior: implications for health behaviors. Int. J. Psychophysiol. 90, 8– 16. 10.1016/j.ijpsycho.2012.10.006. 23085387 PMC3587283 · DOI · Paper page
  57. Lu Y-F, Ren B, Ling B-F, Zhang J, Xu C, Li Z, 2018. Social interaction with a cagemate in pain increases allogrooming and induces pain hypersensitivity in the observer rats. Neurosci. Lett. 662, 385– 388. 10.1016/j.neulet.2017.10.063. 29102786 · DOI
  58. Lukkes JL, Meda S, Thompson BS, Freund N, Andersen SL, 2017. Early life stress and later peer distress on depressive behavior in adolescent female rats: effects of a novel intervention on GABA and D2 receptors. Behav. Brain Res. 330, 37– 45. 10.1016/j.bbr.2017.04.053. 28499915 PMC5546234 · DOI
  59. Maccari S, Krugers HJ, Morley-Fletcher S, Szyf M, Brunton PJ, 2014. The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations. J. Neuroendocrinol. 26, 707– 723. 10.1111/jne.12175. 25039443 · DOI
  60. Maren S, Holmes A, 2016. Stress and fear extinction. Neuropsychopharmacol 41, 58– 79. 10.1038/npp.2015.180. PMC4677122 26105142 · DOI · Paper page
  61. Marusak HA, Martin KR, Etkin A, Thomason ME, 2015. Childhood trauma exposure disrupts the automatic regulation of emotional processing. Neuropsychopharmacology 40, 1250– 1258. 10.1038/npp.2014.311. 25413183 PMC4367470 · DOI · Paper page
  62. Matsumoto M, Yoshida M, Jayathilake BW, Inutsuka A, Nishimori K, Takayanagi Y, Onaka T, 2021. Indispensable role of the oxytocin receptor for allogrooming toward socially distressed cage mates in female mice. J. Neuroendocrinol. 33 10.1111/jne.12980. PMC8243938 34057769 · DOI
  63. McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonté B, Szyf M, Turecki G, Meaney MJ, 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12, 342– 348. 10.1038/nn.2270. 19234457 PMC2944040 · DOI · Paper page
  64. McLaughlin RJ, Verlezza S, Gray JM, Hill MN, Walker C-D, 2016. Inhibition of anandamide hydrolysis dampens the neuroendocrine response to stress in neonatal rats subjected to suboptimal rearing conditions. Stress 19, 114– 124. 10.3109/10253890.2015.1117448. 26552023 · DOI
  65. Molet J, Maras PM, Avishai-Eliner S, Baram TZ, 2014. Naturalistic rodent models of chronic early-life stress: chronic early postnatal stress model. Dev. Psychobiol. 56, 1675– 1688. 10.1002/dev.21230. 24910169 PMC4777289 · DOI
  66. Molet J, Heins K, Zhuo X, Mei YT, Regev L, Baram TZ, Stern H, 2016a. Fragmentation and high entropy of neonatal experience predict adolescent emotional outcome. Transl. Psychiatry 6, e702. 10.1038/tp.2015.200. 26731439 PMC5068874 · DOI
  67. Molet J, Maras PM, Kinney-Lang E, Harris NG, Rashid F, Ivy AS, Solodkin A, Obenaus A, Baram TZ, 2016b. MRI uncovers disrupted hippocampal microstructure that underlies memory impairments after early-life adversity. Hippocampus 26, 1618– 1632. 10.1002/hipo.22661. 27657911 PMC5452614 · DOI
  68. Morrison I, 2016. Keep calm and cuddle on: social touch as a stress buffer. Adapt. Hum. Behav. Physiol. 2, 344– 362. 10.1007/s40750-016-0052-x. · DOI · Paper page
  69. Netser S, Meyer A, Magalnik H, Zylbertal A, De La Zerda SH, Briller M, Bizer A, Grinevich V, Wagner S, 2020. Distinct dynamics of social motivation drive differential social behavior in laboratory rat and mouse strains. Nat. Commun. 11, 5908. 10.1038/s41467-020-19569-0. 33219219 PMC7679456 · DOI
  70. Parfitt DB, Walton JR, Corriveau EA, Helmreich DL, 2007. Early life stress effects on adult stress-induced corticosterone secretion and anxiety-like behavior in the C57BL/6 mouse are not as robust as initially thought. Horm. Behav. 52, 417– 426. 10.1016/j.yhbeh.2007.06.002. 17692317 · DOI
  71. Patterson SK, Strum SC, Silk JB, 2022. Early life adversity has long-term effects on sociality and interaction style in female baboons. Proc. R. Soc. B 289, 20212244. 10.1098/rspb.2021.2244. PMC8808103 35105243 · DOI
  72. Pechtel P, Pizzagalli DA, 2011. Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology 214, 55– 70. 10.1007/s00213-010-2009-2. 20865251 PMC3050094 · DOI · Paper page
  73. Perry RE, Rincón-Cortés M, Braren SH, Brandes-Aitken AN, Opendak M, Pollonini G, Chopra D, Raver CC, Alberini CM, Blair C, Sullivan RM, 2019. Corticosterone administration targeting a hypo-reactive HPA axis rescues a socially-avoidant phenotype in scarcity-adversity reared rats. Dev. Cogn. Neurosci. 40, 100716 10.1016/j.dcn.2019.100716. 31704654 PMC6939642 · DOI
  74. Ramsey LA, Holloman FM, Lee SS, Venniro M, 2023. An operant social self-administration and choice model in mice. Nat. Protoc. 18, 1669– 1686. 10.1038/s41596-023-00813-y. 36964403 PMC12637245 · DOI
  75. Rice CJ, Sandman CA, Lenjavi MR, Baram TZ, 2008. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 149, 4892– 4900. 10.1210/en.2008-0633. 18566122 PMC2582918 · DOI · Paper page
  76. Romeo RD, Karatsoreos IN, McEwen BS, 2006. Pubertal maturation and time of day differentially affect behavioral and neuroendocrine responses following an acute stressor. Horm. Behav. 50, 463– 468. 10.1016/j.yhbeh.2006.06.002. 16836997 · DOI
  77. Romero LM, Dickens MJ, Cyr NE, 2009. The reactive scope model — a new model integrating homeostasis, allostasis, and stress. Horm. Behav. 55, 375– 389. 10.1016/j.yhbeh.2008.12.009. 19470371 · DOI
  78. Sanchez MM, 2006. The impact of early adverse care on HPA axis development: nonhuman primate models. Horm. Behav. 50, 623– 631. 10.1016/j.yhbeh.2006.06.012. 16914153 · DOI
  79. Sanchez MM, McCormack KM, Howell BR, 2015. Social buffering of stress responses in nonhuman primates: maternal regulation of the development of emotional regulatory brain circuits. Soc. Neurosci. 10, 512– 526. 10.1080/17470919.2015.1087426. 26324227 PMC4618704 · DOI
  80. Sapolsky RM, 1994. Individual differences and the stress response. Semin. Neurosci. 6, 261– 269. 10.1006/smns.1994.1033. · DOI
  81. Sapolsky RM, 2015. Stress and the brain: individual variability and the inverted-U. Nat. Neurosci. 18, 1344– 1346. 10.1038/nn.4109. 26404708 · DOI · Paper page
  82. Sapolsky RM, Krey LC, McEwen BS, 1984. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl. Acad. Sci. 81 10.1073/pnas.81.19.6174, 6174 LP – 6177. PMC391882 6592609 · DOI · Paper page
  83. Schmidt M, Okimoto DK, Dent GW, Gordon MK, Levine S, 2002. Maternal regulation of the hypothalamic-pituitary-adrenal axis in the 20-day-old rat: consequences of laboratory weaning: maternal regulation of the HPA axis: consequences of weaning. J. Neuroendocrinol. 14, 450– 457. 10.1046/j.1365-2826.2002.00797.x. 12047720 · DOI
  84. Shanks N, Griffiths J, Zalcman S, Zacharko RM, Anisman H, 1990. Mouse strain differences in plasma corticosterone following uncontrollable footshock. Pharmacol. Biochem. Behav. 36, 515– 519. 10.1016/0091-3057(90)90249-H. 2377652 · DOI
  85. Smith ML, Asada N, Malenka RC, 2021. Anterior cingulate inputs to nucleus accumbens control the social transfer of pain and analgesia. Science 371, 153– 159. 10.1126/science.abe3040. 33414216 PMC7952019 · DOI · Paper page
  86. Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M, Gilhooly T, Millner A, Galvan A, Davidson MC, Eigsti I-M, Thomas KM, Freed PJ, Booma ES, Gunnar MR, Altemus M, Aronson J, Casey BJ, 2010. Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation: previous institutionalization. Dev. Sci. 13, 46– 61. 10.1111/j.1467-7687.2009.00852.x. 20121862 PMC2817950 · DOI · Paper page
  87. van Oers HJJ, Ronald de Kloet E, Levine S, 1997. Persistent, but paradoxical, effects on HPA regulation of infants maternally deprived at different ages. Stress 1, 249– 261. 10.3109/10253899709013745. 9787249 · DOI
  88. Van Oers HJJ, De Kloet ER, Whelan T, Levine S, 1998. Maternal deprivation effect on the infant’s neural stress markers is reversed by tactile stimulation and feeding but not by suppressing corticosterone. J. Neurosci. 18, 10171– 10179. 10.1523/JNEUROSCI.18-23-10171.1998. 9822770 PMC6793306 · DOI
  89. Walsh JJ, Christoffel DJ, Malenka RC, 2023. Neural circuits regulating prosocial behaviors. Neuropsychopharmacol 48, 79– 89. 10.1038/s41386-022-01348-8. PMC9700801 35701550 · DOI · Paper page
  90. Wu YE, Dang J, Kingsbury L, Zhang M, Sun F, Hu RK, Hong W, 2021. Neural control of affiliative touch in prosocial interaction. Nature 599, 262– 267. 10.1038/s41586-021-03962-w. 34646019 PMC8605624 · DOI
  91. Yazgan I, Hanson JL, Bates JE, Lansford JE, Pettit GS, Dodge KA, 2021. Cumulative early childhood adversity and later antisocial behavior: the mediating role of passive avoidance. Dev. Psychopathol. 33, 340– 350. 10.1017/S0954579419001809. 32200772 · DOI
  92. Zeng Q, Shan W, Zhang H, Yang J, Zuo Z, 2021. Paraventricular thalamic nucleus plays a critical role in consolation and anxious behaviors of familiar observers exposed to surgery mice. Theranostics 11, 3813– 3829. 10.7150/thno.45690. 33664863 PMC7914349 · DOI
  93. Zhang H, Yao Z, Lin L, Sun X, Shi X, Zhang L, 2019. Early life stress predicts cortisol response to psychosocial stress in healthy young adults. PsyCh J. 8, 353– 362. 10.1002/pchj.278. 30932372 · DOI

Cited by

Sorted by citations

Authors
Breton, J. M., Cort, Z., Demaestri, C., Critz, M., Nevins, S., Downend, K., Ofray, D., Romeo, R. D., & Bath, K. G.
Affiliations
  • New York State Psychiatric Institute (US)
  • Columbia University (US)
  • Brown University (US)
Corresponding author
Bath, Kevin G.
ORCID
Venue
Hormones and Behavior
Publisher
Elsevier BV
Published
2024-02
Volume
158
Pages
105464
ISSN
0018-506X (ISSN-L)
DOI
10.1016/j.yhbeh.2023.105464
PMC
PMC10872397
OpenAlex
W4389473377
Cited by
11
References
13
Citations by year
2026: 5 · 2025: 3 · 2024: 3
FWCI
2.05
Type
journal article
Language
en
Open access
Licence
Locations
  • Hormones and Behavior (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
Funders
  • National Institute of Mental Health (T32-MH018870-35, RO1-MH115049, RO1-MH115914 1098, F31-MH127888)
  • National Institutes of Health
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Keywords
childhood adversity, stress transfer, corticosterone, hypothalamic-pituitary-adrenal axis, sex differences, allogrooming, huddling, exploratory behavior, social behavior, footshock stress

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