Effects of early-life abuse differ across development: infant social behavior deficits are followed by adolescent depressive-like behaviors mediated by the amygdala
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Abuse during early life, especially from the caregiver, increases vulnerability to develop later-life psychopathologies such as depression. Although signs of depression are typically not expressed until later life, signs of dysfunctional social behavior have been found earlier. How infant abuse alters the trajectory of brain development to produce pathways to pathology is not completely understood. Here we address this question using two different but complementary rat models of early-life abuse from postnatal day 8 (P8) to P12: a naturalistic paradigm, where the mother is provided with insufficient bedding for nest building; and a more controlled paradigm, where infants undergo olfactory classical conditioning. Amygdala neural assessment (c-Fos), as well as social behavior and forced swim tests were performed at preweaning (P20) and adolescence (P45). Our results show that both models of early-life abuse induce deficits in social behavior, even during the preweaning period; however, depressive-like behaviors were observed only during adolescence. Adolescent depressive-like behavior corresponds with an increase in amygdala neural activity in response to forced swim test. A causal relationship between the amygdala and depressive-like behavior was suggested through amygdala temporary deactivation (muscimol infusions), which rescued the depressive-like behavior in the forced swim test. Our results indicate that social behavior deficits in infancy could serve as an early marker for later psychopathology. Moreover, the implication of the amygdala in the ontogeny of depressive-like behaviors in infant abused animals is an important step toward understanding the underlying mechanisms of later-life mental disease associated with early-life abuse.
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Early-life stress effects have been observed after abuse and after maternal deprivation.
“Early-life stress effects have been found following both abuse (Anda et al., 2006; Maniglio, 2009; Raineki, et al., 2012) and maternal deprivation (Johnson, 2002; Loman and Gunnar, 2010)”
From Reduced nucleus accumbens reactivity and adolescent depression following early-life stress (2013) · cites this paper as Raineki, et al., 2012
Amygdala-dependent deficits are task-specific: amygdala hyperactivity underlies decreased social exploration in adolescence and depressive/anxiety-like behavior in adulthood, in parallel with impaired threat aversion learning and blunted amygdala activation during fear conditioning.
“Amygdala-dependent deficits are expressed in a task-specific manner: amygdala hyperactivity underlies decreased social exploration in adolescence and depressive and anxiety-like behavior in adulthood (Fig. 2), in parallel with impaired ability to learn aversions to threat and blunted amygdala activation during fear conditioning (Raineki et al., 2012, Sevelinges et al., 2007, Sevelinges et al., 201”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Raineki et al., 2012
Only early life trauma associated with attachment leads to lifelong amygdala-dependent behavioral deficits, such as poor social behavior (onset prior to weaning) and depressive-like behaviors (onset post-weaning).
“Testing later in life shows that only the early life trauma associated with attachment will lead to lifelong amygdala-dependent behavioral deficits, such as poor social behavior (onset prior to weaning) and depressive-like behaviors (onset post- weaning (Raineki et al., 2012, Raineki et al., 2010b, Sevelinges et al., 2011, Sullivan et al., 2000a, Sullivan et al., 2000b).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Raineki et al., 2012
Pups exposed to abuse in the low bedding procedure and repeated odor-shock pairings form a disordered attachment to the mother, expressed in decreased approach to maternal odor, less nipple attachment, and amygdala hyperactivity if given CORT injections before testing.
“This can also be modeled in rodents: pups that were exposed to abuse in the low bedding procedure and repeated odor-shock pairings form a disordered attachment to the mother, expressed in decreased approach behavior towards the maternal odor, less nipple attachment, and amygdala hyperactivity if given CORT injections before testing (Raineki et al., 2012).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Raineki et al., 2012
Caregiver abuse in early life produces enhanced aggression, impaired threat response, depressive/anxiety-like behavior, and decreased social exploration.
“These factors may be compromised in cases of caregiver abuse in early life, which produces enhanced aggression (Marquez et al., 2013), impaired threat response (Perry, in press), depressive and anxiety-like behavior (Raineki et al., 2012, Raineki et al., 2015 and decreased social exploration (Raineki et al., 2015).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Raineki et al., 2012
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“shock persists into adulthood, which confers to this odor the ability to rescue the trauma-induced depression-like behaviors observed in adolescent and adult rats (Raineki et al., 2012; Rincon-Cortes et al., 2015; Sevelinges et al., 2011).”
Aberrant H3.3 dynamics in NAc promote vulnerability to depressive-like behavior
Lepack, A. E., Bagot, R. C., Peña, C. J., Loh, Y.-H. E., Farrelly, L. A., Lu, Y., Powell, S. K., Lorsch, Z. S., Issler, O., Cates, H. M., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1608270113 · Cited by 63 · see citing works
Maternal regulation of infant brain state
Sarro, E. C., Wilson, D. A., & Sullivan, R. M. (2014) · Current Biology · doi:10.1016/j.cub.2014.06.017 · Cited by 61 · see citing works
Self-citationDevelopmental emergence of fear/threat learning: neurobiology, associations and timing
Tallot, L., Doyère, V., & Sullivan, R. M. (2016) · Genes, Brain and Behavior · doi:10.1111/gbb.12261 · Cited by 57 · see citing works
Self-citationRelationship of Trauma Symptoms to Amygdala‐Based Functional Brain Changes in Adolescents
Nooner, K. B., Mennes, M., Brown, S., Castellanos, F. X., Leventhal, B., Milham, M. P., & Colcombe, S. J. (2013) · Journal of Traumatic Stress · doi:10.1002/jts.21873 · Cited by 43 · see citing works
van der Kooij, M. A., Grosse, J., Zanoletti, O., Papilloud, A., & Sandi, C. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.10.058 · Cited by 39 · see citing works
Stein, C. R., Sheridan, M. A., Copeland, W. E., Machlin, L. S., Carpenter, K. L. H., & Egger, H. L. (2022) · Depression and Anxiety · doi:10.1002/da.23269 · Cited by 26 · see citing works
- Authors
- Raineki, C., Cortés, M. R., Belnoue, L., & Sullivan, R. M.
- Affiliations
- New York University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-05-30
- Volume
- 32
- Issue
- 22
- Pages
- 7758-7765
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3488459
- OpenAlex
- W2063400326
- Cited by
- 217
- References
- 73
- Citations by year
- 2026: 14 · 2025: 15 · 2024: 16 · 2023: 7 · 2022: 19 · 2021: 15 · 2020: 15 · 2019: 22 · 2018: 14 · 2017: 15 · 2016: 18 · 2015: 17 · 2014: 19 · 2013: 9 · 2012: 2
- FWCI
- 17.02
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (1137475)
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- National Institutes of Health
- National Institute of Mental Health (R01MH091451, MH091451)
- National Institute on Deafness and Other Communication Disorders (DC-009910, R01DC009910)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- depression-like behavior, amygdala, forced swim test, nest building, c-fos, developmental trajectories, depression vulnerability, pre-weaning period, adolescence, rat model
- MeSH terms
- Adolescent, Age Factors, Amygdala, Animals, Animals, Newborn, Developmental Disabilities, Conditioning, Classical, Depressive Disorder, Disease Models, Animal, Female, Humans, Male, Maternal Behavior, Maternal Deprivation, Muscimol, Neurons, Olfactory Pathways, Social Behavior Disorders, Social Isolation, Swimming, Vocalization, Animal, Proto-Oncogene Proteins c-fos, Rats, Long-Evans, Rats, GABA-A Receptor Agonists
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