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Memory of early maltreatment: Neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning
Abstract
Background While children form an attachment to their abusive caregiver, they are susceptible to mental illness and brain abnormalities. To understand this important clinical issue, we have developed a rat animal model of abusive attachment where odor paired with shock paradoxically produces an odor preference. Here, we extend this model to a seminaturalistic paradigm using a stressed, "abusive" mother during an odor presentation and assess the underlying learning neural circuit.Methods We used a classical conditioning paradigm pairing a novel odor with a stressed mother that predominantly abused pups to assess olfactory learning in a seminaturalistic environment. Additionally, we used Fos protein immunohistochemistry to assess brain areas involved in learning this pain-induced odor preference within a more controlled maltreatment environment (odor-shock conditioning).Results Odor-maternal maltreatment pairings within a seminatural setting and odor-shock pairings both resulted in paradoxical odor preferences. Learning-induced gene expression was altered in the olfactory bulb and anterior piriform cortex (part of olfactory cortex) but not the amygdala.Conclusions Infants appear to use a unique brain circuit that optimizes learned odor preferences necessary for attachment. A fuller understanding of infant brain function may provide insight into why early maltreatment affects psychiatric well-being.
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“In particular, the anterior piriform is activated by odors learned during this sensitive period, while the posterior piriform is engaged in response to learned odor in older pups and adults (Moriceau and Sullivan, 2006, Moriceau et al., 2006, Roth and Sullivan, 2005).”
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 Roth and Sullivan, 2005
In the citing paper
“Once pups are born, a new maternal odor can be rapidly learned; a novel odor (e.g. peppermint) placed either on the mother or in the air surrounding her will readily take on the properties of maternal odor (Cheslock et al., 2000, Roth and Sullivan, 2005, Sullivan et al., 1990).”
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 Roth and Sullivan, 2005
In the citing paper
“It is important to note that both natural maternal odor and a learned artificial maternal odor generate the same responses from the olfactory bulb (Raineki et al., 2010c, Roth and Sullivan, 2005).”
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 Roth and Sullivan, 2005
In the citing paper
“Pairing this painful maternal care with a novel peppermint odor does not activate the important survival circuit within the brain to support aversion learning. Rather, pups not only learn to approach this odor, but this odor takes on the qualities of maternal odor to support nipple attachment and prosocial behaviors (Roth and Sullivan, 2005, Sullivan et al., 1986, Sullivan et al., 2000a).”
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 Roth and Sullivan, 2005
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Metadata
- Authors
- Roth, T. L., & Sullivan, R. M.
- Affiliations
- University of Oklahoma (US)
- Corresponding author
- Roth, Tania L.
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2005-04
- Volume
- 57
- Issue
- 8
- Pages
- 823-831
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W1991479884
- Cited by
- 204
- References
- 129
- Citations by year
- 2026: 10 · 2025: 3 · 2024: 8 · 2023: 8 · 2022: 3 · 2021: 9 · 2020: 8 · 2019: 16 · 2018: 10 · 2017: 13 · 2016: 17 · 2015: 8 · 2014: 12 · 2013: 15 · 2012: 8
- FWCI
- 8.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Drug Abuse (F31 DA06082, F31DA006082)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD33402, R01HD033402)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Keywords
- maternal abuse, odor preference, classical conditioning, olfactory learning, Fos expression, olfactory bulb, anterior piriform cortex, amygdala, infant brain development, rat model
- MeSH terms
- Animals, Animals, Newborn, Child Abuse, Conditioning, Classical, Disease Models, Animal, Electroshock, Female, Humans, Immunohistochemistry, Infant, Infant, Newborn, Male, Maternal Behavior, Memory, Nerve Net, Odorants, Oncogene Proteins v-fos, Maze Learning, Rats, Long-Evans, Rats
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 ›
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