Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC
Open accessAbstract
Fear can be acquired vicariously through social observation of others suffering from aversive stimuli. We found that mice (observers) developed freezing behavior by observing other mice (demonstrators) receive repetitive foot shocks. Observers had higher fear responses when demonstrators were socially related to themselves, such as siblings or mating partners. Inactivation of anterior cingulate cortex (ACC) and parafascicular or mediodorsal thalamic nuclei, which comprise the medial pain system representing pain affection, substantially impaired this observational fear learning, whereas inactivation of sensory thalamic nuclei had no effect. The ACC neuronal activities were increased and synchronized with those of the lateral amygdala at theta rhythm frequency during this learning. Furthermore, an ACC-limited deletion of Ca(v)1.2 Ca(2+) channels in mice impaired observational fear learning and reduced behavioral pain responses. These results demonstrate the functional involvement of the affective pain system and Ca(v)1.2 channels of the ACC in observational social fear.
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In mice, observational fear learning requires activity of the ACC, suggesting a conserved network for social learning.
“in mice, observational fear learning requires activity of the ACC (Jeon et al., 2010), suggesting a conserved network for social learning”
From Social functioning in major depressive disorder (2016) · cites this paper as Jeon et al., 2010
Social transfer of fear is routinely assayed as increased freezing by an observer and can occur via direct observation of a demonstrator being shocked or indirectly via interaction with a conditioned subject responding to a cue.
“Social transfer of fear, routinely assayed as increased freezing by an observer, is a particularly robust form of emotional contagion and can occur via direct observation of a demonstrator being shocked or indirectly via interaction with a conditioned subject responding to a cue [103-105].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [103]
Projections from the anterior cingulate cortex and insula to the basolateral amygdala have been implicated in social transfer of fear.
“Projections from the ACC and insula to the BLA have been implicated in this form of emotional contagion.”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [103]
Inhibition of anterior cingulate cortex projections to the basolateral amygdala prevents the acquisition of fear, as assessed by freezing, in observer mice.
“Specifically, there is an increase in ACC activity in voles exposed to a stressed partner [93] and inhibition of ACC projections to the BLA prevents the acquisition of fear, as assessed by freezing, in observer mice [98,102,103].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [103]
Downregulation of oxytocin receptors in the CeA is specific to neurons that are also activated by socio-emotional cues, perhaps via the ACC.
“This suggests that downregulation of oxytocin receptors in the CeA is specific to neurons that are also activated by socio-emotional cues, perhaps via the ACC5.”
From Oxytocin enhances observational fear in mice (2017) · cites this paper as [5]
When conspecifics are cage-mates or siblings housed together, the threat response of the observer significantly increases in response to the demonstrator's conditioning compared with unfamiliar subjects.
“When conspecifics are cage-mates or siblings housed together threat response of the observer significantly increases in response to the demonstrator's conditioning in comparison with unfamiliar subjects.152,161”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [152]
In the imminent threat paradigm, observers respond to the demonstrators' fear with freezing and decreased heart rate, both indicating high fear levels.
“It has been shown that in the imminent threat paradigm the observers respond to the demonstrators' fear with freezing 152,158 and decreased heart rate, 159 both of which indicate high fear levels.”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [152]
Responses of observers can be elicited by rapid, random body movements, as well as the lack of movement.
“Responses of the observers can be also elicited by rapid, random body movements, 152,174 as well as the lack of movement.175”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [152]
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- Authors
- Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H. E., Lin, S.-Y., Rabah, D., Kinet, J.-P., & Shin, H.-S.
- Affiliations
- Seoul National University Hospital (KR)
- Korea Institute of Science and Technology (KR)
- Vanderbilt University (US)
- Beth Israel Deaconess Medical Center (US)
- Corresponding author
- Shin, Hee-Sup
- Venue
- Nature Neuroscience
- Published
- 2010-02-28
- Volume
- 13
- Issue
- 4
- Pages
- 482-488
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC2958925
- OpenAlex
- W2064384972
- Cited by
- 651
- References
- 50
- Citations by year
- 2026: 27 · 2025: 43 · 2024: 53 · 2023: 50 · 2022: 43 · 2021: 47 · 2020: 39 · 2019: 42 · 2018: 61 · 2017: 42 · 2016: 45 · 2015: 37 · 2014: 36 · 2013: 31 · 2012: 27
- FWCI
- 16.25
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (R37GM053950)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Keywords
- social fear, anterior cingulate cortex, Cav1.2 calcium channel, parafascicular thalamic nucleus, mediodorsal thalamus, lateral amygdala, theta oscillations, freezing behavior, footshock, social relatedness
- MeSH terms
- Animals, Cerebral Cortex, Conditioning, Classical, Fear, Female, Gyrus Cinguli, Learning, Male, Mice, Inbred C57BL, Pain, Pain Measurement, Social Behavior, Rats, Sprague-Dawley, Mice, Knockout, Calcium Channels, L-Type, Protein Subunits, Freezing Reaction, Cataleptic, Mice, Rats
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