Selective early-acquired fear memories undergo temporary suppression during adolescence
Open accessAbstract
Highly conserved neural circuitry between rodents and humans has allowed for in-depth characterization of behavioral and molecular processes associated with emotional learning and memory. Despite increased prevalence of affective disorders in adolescent humans, few studies have characterized how associative-emotional learning changes during the transition through adolescence or identified mechanisms underlying such changes. By examining fear conditioning in mice, as they transitioned into and out of adolescence, we found that a suppression of contextual fear occurs during adolescence. Although contextual fear memories were not expressed during early adolescence, they could be retrieved and expressed as the mice transitioned out of adolescence. This temporary suppression of contextual fear was associated with blunted synaptic activity in the basal amygdala and decreased PI3K and MAPK signaling in the hippocampus. These findings reveal a unique form of brain plasticity in fear learning during early adolescence and may prove informative for understanding endogenous mechanisms to suppress unwanted fear memories.
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Adolescents have been reported to show either stronger or weaker aversive fear conditioning to the training context than adults, depending on the study.
“adolescents have been varyingly reported to exhibit either stronger (Brasser & N. Spear, 2005; Esmoris et al, 2008; see also Barrett et al, 1984) or weaker (Pattwell et al, 2011) aversive (fear) conditioning to the training context than adults”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Pattwell et al, 2011
In classical conditioning, adolescents have been reported to show either stronger or weaker aversive fear conditioning to the training context than adults.
“adolescents have been varyingly reported to exhibit either stronger (Brasser & N. Spear, 2005; Esmoris et al, 2008; see also Barrett et al, 1984) or weaker (Pattwell et al, 2011) aversive (fear) conditioning to the training context than adults”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Pattwell et al, 2011
Recent research with rodents and humans has shown distinctive developmental profiles of blunted threat extinction recall in adolescents relative to children and adults.
“Recent research with rodents and humans has shown distinctive developmental profiles of blunted threat extinction recall in adolescents6–11, relative to children and adults.”
From Multimodal evidence for delayed threat extinction learning in adolescence and young adulthood (2019) · cites this paper as [8]
In vulnerable populations such as children and adolescents, sound stimuli are recommended over mild electric shocks in threat conditioning paradigms.
“In vulnerable populations, such as children and adolescents, sound stimuli are recommended over mild electric shocks in threat conditioning paradigms7,8,13,43.”
From Multimodal evidence for delayed threat extinction learning in adolescence and young adulthood (2019) · cites this paper as [8]
During extinction over time, increased recruitment of the mPFC to CS+ vs. CS− occurred in early trials for older participants and in late trials for younger participants.
“The analysis of extinction over time (Stimulus × Time × Age interaction), showed increased recruitment of the mPFC to CS+ vs. CS− in the early trials for older participants and in the late trials for younger participants (see Fig. 2 and Table 1).”
From Multimodal evidence for delayed threat extinction learning in adolescence and young adulthood (2019) · cites this paper as [8]
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- Authors
- Pattwell, S. S., Bath, K. G., Casey, B. J., Ninan, I., & Lee, F. S.
- Affiliations
- Department of Psychiatry,
- Brown University (US)
- New York University (US)
- Cornell University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-01-10
- Volume
- 108
- Issue
- 3
- Pages
- 1182-1187
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3024661
- OpenAlex
- W2130394290
- Cited by
- 161
- References
- 52
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 6 · 2023: 4 · 2022: 7 · 2021: 8 · 2020: 9 · 2019: 15 · 2018: 17 · 2017: 13 · 2016: 20 · 2015: 12 · 2014: 12 · 2013: 16 · 2012: 5
- FWCI
- 5.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- New York Community Trust
- International Mental Health Research Organization
- National Alliance for Research on Schizophrenia and Depression
- Monique Weill-Caulier Trust
- National Institutes of Health (MH079513)
- National Institute of Mental Health (P50MH079513, MH079513, R25MH060478, MH060478)
- National Institute of Neurological Disorders and Stroke (NS052819, R01NS052819)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD055177, T32HD055177)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- contextual fear conditioning, emotional learning, basal amygdala, hippocampus, PI3K signaling, MAPK signaling, synaptic plasticity, mood disorders, memory retrieval
- MeSH terms
- Psychology, Adolescent, Amygdala, Analysis of Variance, Animals, Association Learning, Conditioning, Psychological, Electrophysiology, Fear, Hippocampus, Memory, Blotting, Western, Signal Transduction, Phosphatidylinositol 3-Kinases, MAP Kinase Signaling System, Mice
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