Molecular mechanisms of fear learning and memory

Johansen, Joshua P.; Cain, Christopher K.; Ostroff, Linnaea E.; LeDoux, Joseph E.

doi:10.1016/j.cell.2011.10.009

Cited by 1,012Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Molecular mechanisms of fear learning and memory

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Johansen, Joshua P., Cain, Christopher K., Ostroff, Linnaea E., LeDoux, Joseph E.·2011·Cell

DOI 10.1016/j.cell.2011.10.009PMC PMC3215943

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Abstract

Pavlovian fear conditioning is a particularly useful behavioral paradigm for exploring the molecular mechanisms of learning and memory because a well-defined response to a specific environmental stimulus is produced through associative learning processes. Synaptic plasticity in the lateral nucleus of the amygdala (LA) underlies this form of associative learning. Here, we summarize the molecular mechanisms that contribute to this synaptic plasticity in the context of auditory fear conditioning, the form of fear conditioning best understood at the molecular level. We discuss the neurotransmitter systems and signaling cascades that contribute to three phases of auditory fear conditioning: acquisition, consolidation, and reconsolidation. These studies suggest that multiple intracellular signaling pathways, including those triggered by activation of Hebbian processes and neuromodulatory receptors, interact to produce neural plasticity in the LA and behavioral fear conditioning. Collectively, this body of research illustrates the power of fear conditioning as a model system for characterizing the mechanisms of learning and memory in mammals and potentially for understanding fear-related disorders, such as PTSD and phobias.

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Owing to animal experiments and optogenetics, the molecular and cellular mechanisms of fear conditioning in the amygdala are increasingly understood.
“Owing to the availability of elegant animal experiments (Karpova et al., 2011) and experimental techniques such as optogenetics, the molecular and cellular mechanisms of fear conditioning in the amygdala, are increasingly understood (Johansen et al., 2011;Rodrigues et al., 2004).”
From Serotonin and neuroplasticity – Links between molecular, functional and structural pathophysiology in depression (2017) · cites this paper as Johansen et al., 2011
Dopamine has been implicated in the learning of affective associations, such as fear-associated stimuli.
“dopamine has been implicated in the learning of affective associations, such as fear-associated stimuli (for a review, see, e.g., Johansen, Cain, Ostroff, & LeDoux, 2011).”
From Selection history: How reward modulates selectivity of visual attention. (2018) · cites this paper as Johansen, Cain, Ostroff, & LeDoux, 2011
5-HT1A receptors fine-tune LTP in the amygdala during fear conditioning.
“For example 5-HT 1A -receptors fine-tune LTP in the amygdala during fear conditioning (Huang and Kandel, 2007;Johansen et al., 2011).”
From Serotonin and neuroplasticity – Links between molecular, functional and structural pathophysiology in depression (2017) · cites this paper as Johansen et al., 2011
The Neuromodulatory-Dependent Mechanisms section says serotonin’s role in the lateral amygdala during auditory fear conditioning has not been carefully examined. A search for 5-HT1A and serotonergic modulation found no passage stating that 5-HT1A receptors fine-tune amygdala LTP during fear conditioning; the source does not establish or rule out that specific claim. No page number was available in our copy. (LLM, conf=0.75)
Experimental — accuracy not yet measured
The amygdala is required for the acquisition and expression of learned fear.
“required for the acquisition and expression of learned fear”
From Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience (2014) · cites this paper as Johansen et al., 2011
An extensive rodent literature has characterized the neural circuitry underlying fear learning using Pavlovian fear conditioning tasks.
“An extensive literature in rodents has characterized the neural circuitry that underlies fear learning using Pavlovian fear conditioning tasks”
From Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience (2014) · cites this paper as Johansen et al., 2011

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Authors: Johansen, J. P., Cain, C. K., Ostroff, L. E., & LeDoux, J. E.
Affiliations: RIKEN Center for Brain Science (JP)
Nathan Kline Institute for Psychiatric Research (US)
New York University (US)
Corresponding author: LeDoux, Joseph E.
ORCID: Johansen, Joshua P.
Cain, Christopher K.
Ostroff, Linnaea E.
Venue: Cell
Publisher: Elsevier BV
Published: 2011-10
Volume: 147
Issue: 3
Pages: 509-524
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2011.10.009
PMC: PMC3215943
OpenAlex: W2011200277
Cited by: 1,012
References: 214
Citations by year: 2026: 35 · 2025: 45 · 2024: 52 · 2023: 52 · 2022: 58 · 2021: 57 · 2020: 94 · 2019: 71 · 2018: 74 · 2017: 73 · 2016: 81 · 2015: 89 · 2014: 98 · 2013: 88 · 2012: 40
FWCI: 6.22
Type: journal article
Language: en
Update notices: erratum (2011-11-11)
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 655 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH038774, R01MH046516)
National Institute on Drug Abuse (R01DA029053)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: fear conditioning, auditory fear conditioning, synaptic plasticity, lateral amygdala, associative learning, memory consolidation, memory reconsolidation, Hebbian plasticity, intracellular signaling, post-traumatic stress disorder, phobia
MeSH terms: Animals, Brain, Conditioning, Psychological, Fear, Humans, Learning, Memory, Signal Transduction, Rats

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Molecular mechanisms of fear learning and memory

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