Enduring effects of infant memories: infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning
Abstract
Background Early life adverse experience alters adult emotional and cognitive development. Here we assess early life learning about adverse experience and its consequences on adult fear conditioning and amygdala activity. Methods Neonatal rats were conditioned daily from 8-12 days-old with paired odor (conditioned stimulus, CS) .5mA shock, unpaired, odor-only, or naive (no infant conditioning). In adulthood, each infant training group was divided into three adult training groups: paired, unpaired or odor-only, using either the same infant CS odor, or a novel adult CS odor without or with the infant CS present as context. Adults were cue tested for freezing (odor in novel environment), with amygdala (14)C 2-DG autoradiography and electrophysiology assessment. Results Infant paired odor-shock conditioning attenuated adult fear conditioning, but only if the same infant CS odor was used. The (14)C 2-DG activity correlated with infant paired odor-shock conditioning produced attenuated amygdala but heightened olfactory bulb activity. Electrophysiological amygdala assessment further suggests early experience causes changes in amygdala processing as revealed by increased paired-pulse facilitation in adulthood. Conclusions This suggests some enduring effects of early life adversity (shock) are under CS control and dependent upon learning for their impact on later adult fear learning.
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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 Sevelinges et al., 2007
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Mysliveček, J. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00036-1 · Cited by 42 · see citing works
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Dissociation of behavioral and neural correlates of early associative learning
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Plasma-Free Corticosteroid Response to Electric Shock in Rats Stimulated in Infancy
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Handbook of Olfaction and Gustation
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Sensory Physiology of Central Olfactory Pathways
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Infant Stress, Neuroplasticity, and Behavior
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Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.008 · Cited by 579 · see citing works
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Raineki, C., Cortés, M. R., Belnoue, L., & Sullivan, R. M. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5843-11.2012 · Cited by 217 · see citing works
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Developing a neurobehavioral animal model of infant attachment to an abusive caregiver
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Human amygdala development in the absence of species‐expected caregiving
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Self-citationDevelopmental emergence of fear learning corresponds with changes in amygdala synaptic plasticity
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Raineki, C., Sarro, E., Rincón-Cortés, M., Perry, R., Boggs, J., Holman, C. J., Wilson, D. A., & Sullivan, R. M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.266 · Cited by 71 · see citing works
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Raineki, C., Shionoya, K., Sander, K., & Sullivan, R. M. (2009) · Learning & Memory · doi:10.1101/lm.977909 · Cited by 71 · see citing works
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Self-citationChapuis, J., Garcia, S., Messaoudi, B., Thévenet, M., Ferreira, G., Gervais, R., & Ravel, N. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0505-09.2009 · Cited by 64 · see citing works
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“neural activity (Sevelinges et al., 2007), suggesting that it has endorsed the properties of a safety signal (Pollak et al.”
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Memory and Plasticity in the Olfactory System: From Infancy to Adulthood
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Developmental Neurobiology of the Rat Attachment System and Its Modulation by Stress
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Hegoburu, C., Denoroy, L., Mouly, A., & Parrot, S. (2014) · InTech eBooks · doi:10.5772/57490 · Cited by 1 · see citing works
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Regulation of circadian rhythm through SCN and non-SCN factors
Pantazopoulos, H. (2010) · doi:10.17760/d20000802
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Self-citation
- Authors
- Sevelinges, Y., Moriceau, S., Holman, P., Miner, C., Muzny, K., Gervais, R., Mouly, A.-M., & Sullivan, R. M.
- Affiliations
- Lyon 1 Université (FR)
- University of Oklahoma (US)
- Corresponding author
- Sullivan, Regina M.
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2007-11
- Volume
- 62
- Issue
- 10
- Pages
- 1070-1079
- ISSN
- 0006-3223 (ISSN-L)
- OpenAlex
- W2166197054
- Cited by
- 74
- References
- 132
- Citations by year
- 2026: 1 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 3 · 2019: 6 · 2018: 3 · 2017: 4 · 2016: 7 · 2015: 3 · 2014: 5 · 2013: 6 · 2012: 6
- FWCI
- 3.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-05-PNRA-1)
- National Institute of Child Health and Human Development (HD33402)
- Oklahoma Center for the Advancement of Science and Technology
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- childhood adversity, fear conditioning, amygdala, olfactory bulb, paired-pulse facilitation, contextual fear, freezing behavior, neonatal rats, [14C]2-deoxyglucose autoradiography
- MeSH terms
- Aging, Amygdala, Analysis of Variance, Animals, Animals, Newborn, Autoradiography, Avoidance Learning, Behavior, Animal, Conditioning, Classical, Deoxyglucose, Electric Stimulation, Evoked Potentials, Fear, Male, Memory, Odorants, Olfactory Bulb, Radiography, Reaction Time, Maze Learning, Rats, Long-Evans, Freezing Reaction, Cataleptic, Rats
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