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Cited by 57Memory and Neural MechanismsNeural and Behavioral Psychology StudiesNeuroscience and Neuropharmacology Research

Developmental emergence of fear/threat learning: neurobiology, associations and timing

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Tallot, L., Doyère, V., Sullivan, R. M.·2016·Genes, Brain and Behavior
DOI 10.1111/gbb.12261PMC PMC5154388
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Abstract

Pavlovian fear or threat conditioning, where a neutral stimulus takes on aversive properties through pairing with an aversive stimulus, has been an important tool for exploring the neurobiology of learning. In the past decades, this neurobehavioral approach has been expanded to include the developing infant. Indeed, protracted postnatal brain development permits the exploration of how incorporating the amygdala, prefrontal cortex and hippocampus into this learning system impacts the acquisition and expression of aversive conditioning. Here, we review the developmental trajectory of these key brain areas involved in aversive conditioning and relate it to pups' transition to independence through weaning. Overall, the data suggests that adult‐like features of threat learning emerge as the relevant brain areas become incorporated into this learning. Specifically, the developmental emergence of the amygdala permits cue learning and the emergence of the hippocampus permits context learning. We also describe unique features of learning in early life that block threat learning and enhance interaction with the mother or exploration of the environment. Finally, we describe the development of a sense of time within this learning and its involvement in creating associations. Together these data suggest that the development of threat learning is a useful tool for dissecting adult‐like functioning of brain circuits, as well as providing unique insights into ecologically relevant developmental changes.

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Crossref · 10.1111/gbb.12261

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  • The amygdala and hippocampus also develop during the same period following non-linear patterns until early adulthood.

    “Together with the HPA axis, however, the amygdala and the hippocampus also develop during the same period following non-linear patterns until early adulthood (96–100).”

    From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [100]

    The 'Developmental emergence of aversive learning' section describes developmental changes in the amygdala and hippocampus, while 'Ontogeny of interval timing' calls the hippocampus late developing. But the latter section says the amygdala matures very early; the paper does not establish that both structures follow non-linear patterns through early adulthood. Page numbers were not available in our copy. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Periods of greater HPA axis plasticity may represent specific periods of greater vulnerability.

    “Thereby, periods of greater HPA axis plasticity may represent specific periods of greater vulnerability (96, 100, 101), while mounting evidence suggests a differential impact of ELS/CT on HPA axis activity according to the specific developmental age of exposure (102).”

    From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [100]

    In “The stress hormone CORT permits infant cue learning” (page unavailable), the paper describes age-dependent HPA-axis activation in rat pups and a period when corticosterone affects aversive learning. It does not establish that periods of greater HPA-axis plasticity are periods of greater vulnerability; the plasticity discussed is amygdala learning plasticity. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

  • HPA axis activity trajectory develops from infancy to early adulthood and beyond.

    “The HPA axis activity trajectory develops from infancy to early adulthood and beyond.”

    From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [100]

    In “The stress hormone CORT permits infant cue learning” (page unavailable), the paper describes low stress-induced HPA-axis activity in infant rats and contrasts it with older pups and adults. It does not describe an HPA-axis activity trajectory through early adulthood and beyond, so the claimed lifespan scope is unsupported. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Non-linear patterns in neurodevelopment lead to specific periods of greater stress system plasticity, which represent important vulnerability periods.

    “Thereby, non-linear patterns in neurodevelopment lead to specific periods of greater stress system plasticity, which represent important vulnerability periods (96, 100, 101).”

    From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [100]

    The sections on developmental emergence of aversive learning and stress-hormone effects describe age-specific changes in rat pups’ stress responses and in the role of corticosterone in amygdala learning plasticity (page unavailable). The Concluding remarks also emphasize distinct developmental epochs, but the paper does not establish that these are periods of greater stress-system plasticity or identify them broadly as vulnerability periods. (LLM, conf=0.84)

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Cites

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Research works printed but not linked: 2

  1. Hinde RA Biological Basis of Human Social Behavior 1974 New York McGraw-Hill
  2. Levine S Plasma-free corticosteroid response to electric shock in rats stimulated in infancy Science 1962 135 795 796 14464660

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Authors
Tallot, L., Doyère, V., & Sullivan, R. M.
Affiliations
  • Université Paris-Sud (FR)
  • Nathan Kline Institute for Psychiatric Research (US)
Corresponding author
  • Tallot, L.
  • Sullivan, R. M.
ORCID
Venue
Genes, Brain and Behavior
Publisher
Wiley
Published
2015-11-13
Volume
15
Issue
1
Pages
144-154
ISSN
  • 1601-183X (ISSN-L)
  • 1601-1848
DOI
10.1111/gbb.12261
PMC
PMC5154388
OpenAlex
W1937784482
Cited by
57
References
176
Citations by year
2026: 3 · 2025: 2 · 2024: 6 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 17 · 2019: 5 · 2018: 5 · 2017: 4 · 2016: 6
FWCI
0.50
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Genes Brain & Behavior (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • HAL (submittedVersion)
Funders
  • Agence Nationale de la Recherche
  • National Institutes of Health (DC009910, MH091451, HD083217)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
fear conditioning, threat learning, infant development, amygdala, hippocampus, prefrontal cortex, weaning, cue learning, contextual learning, maternal interaction, time perception, postnatal brain development, aversive conditioning
MeSH terms
Amygdala, Animals, Association Learning, Child Development, Fear, Humans, Infant, Neurogenesis

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