Paradoxical neurobehavioral rescue by memories of early-life abuse: the safety signal value of odors learned during abusive attachment
Open accessAbstract
Caregiver-associated cues, including those learned in abusive attachment, provide a sense of safety and security to the child. Here, we explore how cues associated with abusive attachment, such as maternal odor, can modify the enduring neurobehavioral effects of early-life abuse. Two early-life abuse models were used: a naturalistic paradigm, where rat pups were reared by an abusive mother; and a more controlled paradigm, where pups underwent peppermint odor-shock conditioning that produces an artificial maternal odor through engagement of the attachment circuit. Animals were tested for maternal odor preference in infancy, forced swim test (FST), social behavior, and sexual motivation in adulthood-in the presence or absence of maternal odors (natural or peppermint). Amygdala odor-evoked local field potentials (LFPs) via wireless electrodes were also examined in response to the maternal odors in adulthood. Both early-life abuse models induced preference for the maternal odors in infancy. In adulthood, these early-life abuse models produced FST deficits and decreased social behavior, but did not change sexual motivation. Presentation of the maternal odors rescued FST and social behavior deficits induced by early-life abuse and enhanced sexual motivation in all animals. In addition, amygdala LFPs from both abuse animal models showed unique activation within the gamma frequency (70-90 Hz) bands in response to the specific maternal odor present during early-life abuse. These results suggest that attachment-related cues learned during infancy have a profound ability to rescue neurobehavioral dysregulation caused by early-life abuse. Paradoxically, abuse-associated cues seem to acquire powerful and enduring antidepressive properties and alter amygdala modulation.
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Caregiver abuse decreases sexual motivation in adult rodents.
“Furthermore, caregiver abuse decreases sexual motivation in adult rodents (Raineki et al., 2015), suggesting that these animals may fail to engage receptive females, a benefit of dominance in typically-reared individuals (Blanchard et al., 1995, Blanchard et al., 1988, White et al., 1986).”
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., 2015
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- Authors
- Raineki, C., Sarro, E., Rincón-Cortés, M., Perry, R., Boggs, J., Holman, C. J., Wilson, D. A., & Sullivan, R. M.
- Affiliations
- Nathan Kline Institute for Psychiatric Research (US)
- University of Oklahoma (US)
- New York University (US)
- Corresponding author
- Raineki, Charlis
- Sullivan, Regina M
- Venue
- Neuropsychopharmacology
- Published
- 2014-10-06
- Volume
- 40
- Issue
- 4
- Pages
- 906-914
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC4330504
- OpenAlex
- W2057632757
- Cited by
- 71
- References
- 54
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 6 · 2023: 4 · 2022: 4 · 2021: 9 · 2020: 5 · 2019: 11 · 2018: 8 · 2017: 9 · 2016: 7 · 2015: 2
- FWCI
- 7.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (1137475)
- National Institutes of Health
- School of Medicine, New York University
- Medical Research Council
- National Institute of Mental Health (NIH-DC009910, R01MH091451, T32MH096331, MH091451)
- National Institute on Deafness and Other Communication Disorders (R01DC009910, NIH-DC009910)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- maternal odor, olfactory cues, forced swim test, social behavior, sexual motivation, gamma oscillations, antidepressant effects
- MeSH terms
- Action Potentials, Amygdala, Animals, Animals, Newborn, Conditioning, Classical, Disease Models, Animal, Electric Wiring, Male, Memory, Motivation, Odorants, Sexual Behavior, Animal, Social Behavior, Swimming, Maze Learning, Substance-Related Disorders, Rats, Long-Evans, Maternal-Fetal Relations, Rats
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