Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids

CUSHING, B; KRAMER, K

doi:10.1016/j.neubiorev.2005.04.001

Cited by 209Neuroendocrine regulation and behaviorStress Responses and CortisolAnimal Behavior and Reproduction

Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids

CUSHING, B, KRAMER, K·2005·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2005.04.001

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Abstract

In mammals the neonatal period is a time of significant social interaction. This is true even in solitary species as females spend a significant amount of time nursing and caring for their offspring. In social species interactions may also include the father, older siblings and extended family members. This period is a time of significant development, including organization of the central nervous system, and therefore a time when the degree and type of social interaction influences the development and expression of social behavior in adulthood. The purpose of this review is to examine the possible mechanisms for the epigenetic effects of early social experience on the subsequent expression of social behavior. We propose that social interactions during the neonatal period organize the subsequent expression of behavior by altering sensitivity to neuropeptides and steroids. Both neuropeptides (e.g. oxytocin and arginine vasopressin) and steroids (e.g. estrogen) regulate or influence the expression of behaviors such as affiliation, aggression, sociosexual behavior, parental behavior, and responses to stress. Therefore, changes in sensitivity to these hormones via reorganization of receptors or changes in hormone production and secretion are potentially powerful mechanisms through which early social experience can mold subsequent social behaviors.

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Because AVP/OT and the dopaminergic pathways they feed into are heavily influenced by sex steroids across the lifespan, their sexually dimorphic ontogeny and function may be particularly vulnerable to endocrine disruption.
“Because AVP/OT and the dopaminergic pathways they feed into are heavily influenced by sex steroids across the lifespan (50–59), it is highly plausible that their sexually dimorphic ontogeny and function may be particularly vulnerable to endocrine disruption.”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [51]
Work from Bruce Cushing's laboratory suggests that the BNST and medial amygdala are particularly important for the developmental effects of oxytocin and estrogen receptor alpha on social behavior.
“Work from Bruce Cushing’s laboratory suggests that the BNST and MeA are particularly important for the developmental effects of Oxt and ERα on social behavior (24, 26, 94)”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [94]

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Repeated intranasal oxytocin administration in early life dysregulates the HPA axis and alters social behavior
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The influence of prenatal intimate partner violence exposure on hypothalamic–pituitary–adrenal axis reactivity and childhood internalizing and externalizing symptoms
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The Monogamy Paradox: What Do Love and Sex Have to Do With It?
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Communal nesting, an early social enrichment, increases the adult anxiety-like response and shapes the role of social context in modulating the emotional behavior
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The influence of nest attendance and provisioning on nestling stress physiology in the Florida scrub-jay
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Ethanol Exposure Induces Neonatal Neurodegeneration by Enhancing CB1R Exon1 Histone H4K8 Acetylation and Up-regulating CB1R Function causing Neurobehavioral Abnormalities in Adult Mice
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A novel model for neuroendocrine toxicology: neurobehavioral effects of BPA exposure in a prosocial species, the prairie vole (Microtus ochrogaster)
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Does Maltreatment in Childhood Affect Sexual Orientation in Adulthood?
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Eaton, J. L., Holmqvist, B. I., & Glasgow, E. F. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21503 · Cited by 72 · see citing works
Vasopressin, but not oxytocin, increases empathic concern among individuals who received higher levels of paternal warmth: a randomized controlled trial
Tabak, B. A., Meyer, M. L., Castle, E., Dutcher, J. M., Irwin, M. R., Han, J. H., Lieberman, M. D., & Eisenberger, N. I. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.10.006 · Cited by 67 · see citing works
Hormonal and Genetic Influences on Processing Reward and Social Information
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Estrogen Receptor-α in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie Voles (Microtus ochrogaster)
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Organizational effects of oxytocin on serotonin innervation
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Maternal behaviour in domestic dogs
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Osteopathic Care as (En)active Inference: A Theoretical Framework for Developing an Integrative Hypothesis in Osteopathy
Esteves, J. E., Cerritelli, F., Kim, J., & Friston, K. J. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.812926 · Cited by 58 · see citing works
Endocrine Disruption of Vasopressin Systems and Related Behaviors
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The role of trauma in the hormonal interplay of cortisol, testosterone, and oxytocin in adolescent aggression
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Duration of exclusive breastfeeding is associated with differences in infants’ brain responses to emotional body expressions
Krol, K. M., Rajhans, P., Missana, M., & Großmann, T. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00459 · Cited by 51 · see citing works
Early Social Environment Affects the Endogenous Oxytocin System: A Review and Future Directions
Alves, E., Fielder, A. L., Ghabriel, N., Sawyer, M., & Buisman‐Pijlman, F. T. A. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00032 · Cited by 48 · see citing works
Short- and long-term consequences of different early environmental conditions on central immunoreactive oxytocin and arginine vasopressin levels in male rats
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Pre-administration of G9a/GLP inhibitor during synaptogenesis prevents postnatal ethanol-induced LTP deficits and neurobehavioral abnormalities in adult mice
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Oxytocin Signaling in the Early Life of Mammals: Link to Neurodevelopmental Disorders Associated with ASD
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Epigenetics in blood–brain barrier disruption
Ihezie, S. A., Mathew, I. E., McBride, D. W., Dienel, A., Blackburn, S., & Pandit, P. K. T. (2021) · Fluids and Barriers of the CNS · doi:10.1186/s12987-021-00250-7 · Cited by 47 · see citing works
Neonatal paternal deprivation or early deprivation reduces adult parental behavior and central estrogen receptor α expression in mandarin voles (Microtus mandarinus)
Jia, R., Tai, F., An, S.-C., & Zhang, X. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.05.042 · Cited by 45 · see citing works
High variability and non-neutral evolution of the mammalian avpr1a gene
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Forensic Use of the Five Domains Model for Assessing Suffering in Cases of Animal Cruelty
Ledger, R. A., & Mellor, D. J. (2018) · Animals · doi:10.3390/ani8070101 · Cited by 44 · see citing works
Maternal Bonding in Early Infancy Predicts Childrens' Social Competences in Preschool Age
Joas, J., & Möhler, E. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.687535 · Cited by 43 · see citing works
The evolved developmental niche and child sociomoral outcomes in Chinese 3-year-olds
Narvaez, D. F., Wang, L., Gleason, T. R., Cheng, Y., Lefever, J. B., & Deng, L. (2013) · European Journal of Developmental Psychology · doi:10.1080/17405629.2012.761606 · Cited by 42 · see citing works
Oxytocin and emotion processing
Simplicio, M. C. D., & Harmer, C. J. (2016) · Journal of Psychopharmacology · doi:10.1177/0269881116641872 · Cited by 38 · see citing works
Social makes smart: rearing conditions affect learning and social behaviour in jumping spiders
Liedtke, J., & Schneider, J. M. (2017) · Animal Cognition · doi:10.1007/s10071-017-1125-3 · Cited by 38 · see citing works
Reduced DNA methylation of the oxytocin receptor gene is associated with obsessive-compulsive disorder
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Authors: CUSHING, B., & KRAMER, K.
Affiliations: University of Illinois Chicago (US)
Corresponding author: CUSHING, B
ORCID: CUSHING, B
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2005
Volume: 29
Issue: 7
Pages: 1089-1105
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2005.04.001
OpenAlex: W2048444812
Cited by: 209
References: 202
Citations by year: 2026: 3 · 2025: 4 · 2024: 1 · 2023: 4 · 2022: 8 · 2021: 11 · 2020: 6 · 2019: 6 · 2018: 9 · 2017: 7 · 2016: 13 · 2015: 14 · 2014: 15 · 2013: 18 · 2012: 13
FWCI: 14.30
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (MH 01992, K01MH001992)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 41293, P01HD038490, HD38490, F32HD041293)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: early social experience, epigenetic mechanisms, neuropeptides, oxytocin, vasopressin, estrogen, steroid hormones, social behavior development, receptor sensitivity, parental behavior, aggression, sociosexual behavior, stress response, affiliation
MeSH terms: Animals, Animals, Newborn, Behavior, Animal, Female, Humans, Limbic System, Male, Neurosecretory Systems, Oxytocin, Sex Characteristics, Social Behavior, Social Environment, Vasotocin, Gene Expression Regulation, Developmental, Epigenesis, Genetic

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Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids

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