Brain systems mediating aversive conditioning: an event-related fMRI study
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We have used event-related functional magnetic resonance imaging (fMRI) to characterize neural responses associated with emotional learning. Employing a classical conditioning paradigm in which faces were conditioned by pairing with an aversive tone (US), we compared responses evoked by conditioned (CS+) and nonconditioned (CS-) stimuli. Pairing 50% of the CS+ with the US enabled us to constrain our analysis to responses evoked by a CS+ not followed by a US. Differential evoked responses, related to conditioning, were found in the anterior cingulate and the anterior insula, regions with known involvement in emotional processing. Differential responses of the amygdalae were best characterized by a time by stimulus interaction indicating a rapid adaptation of CS+-specific responses in this region.
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fMRI studies showed increased BOLD signal in the amygdala to a conditioned stimulus relative to stimulus never paired with shock, and the magnitude of this BOLD response was correlated with the strength of the conditioned response.
“functional magnetic resonance imaging (fMRI) studies soon followed that showed increased blood oxygenation level dependent (BOLD) signal in the amygdala to a conditioned stimulus (relative to stimulus never paired with shock) [75, 76], and the magnitude of this BOLD response was correlated with the strength of the conditioned response [76].”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [75]
The Summary (p. 1) and Amygdala results (pp. 6–7) report a conditioned-stimulus-specific amygdala response, but it habituated rapidly; the comparison over the full conditioning phase did not show amygdala activation. The Results (p. 1) say the stimulus was paired with an aversive tone, not shock. The skin-conductance analysis (p. 4) reports a relationship between the time courses of amygdala activation and conditioned responses, not a correlation between their magnitudes. (LLM, conf=0.90)
Experimental — accuracy not yet measuredHuman neuroimaging studies have implicated the amygdala in fear acquisition and extinction.
“neuroimaging studies in humans have likewise implicated the amygdala in fear acquisition and extinction (Buchel et al., 1998; LaBar et al., 1998; Milad et al., 2007; Phelps et al., 2004)”
From Phasic and sustained fear in humans elicits distinct patterns of brain activity (2011) · cites this paper as Buchel et al., 1998
Previous studies show a rapid reduction in amygdala activation over time in fear conditioning and threat of shock.
“It is also consistent with previous studies showing a rapid reduction in amygdala activation over time in fear conditioning (Buchel et al., 1998; LaBar et al., 1998) and threat of shock (Phelps et al., 2001).”
From Phasic and sustained fear in humans elicits distinct patterns of brain activity (2011) · cites this paper as Buchel et al., 1998
During threat acquisition, a neutral cue comes to be associated with an aversive outcome (conditioned stimulus (CS)), which leads to greater amygdala activity to the cue.
“During threat acquisition, a neutral cue comes to be associated with an aversive outcome (conditioned stimulus (CS)), which leads to greater amygdala activity to the cue2.”
From Multimodal evidence for delayed threat extinction learning in adolescence and young adulthood (2019) · cites this paper as [2]
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“Consistent with these early patient studies, functional magnetic resonance imaging (fMRI) studies soon followed that showed increased blood oxygenation level dependent (BOLD) signal in the amygdala to a conditioned stimulus (relative to stimulus never paired with shock) [75, 76], and the magnitude of this BOLD respons…”
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- Authors
- Büchel, C., Morris, J., Dolan, R. J., & Friston, K. J.
- Affiliations
- National Hospital for Neurology and Neurosurgery (GB)
- The Royal Free Hospital (GB)
- Corresponding author
- Büchel, Christian
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1998-05
- Volume
- 20
- Issue
- 5
- Pages
- 947-957
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2052869567
- Cited by
- 951
- References
- 58
- Citations by year
- 2026: 8 · 2025: 18 · 2024: 17 · 2023: 9 · 2022: 9 · 2021: 16 · 2020: 15 · 2019: 16 · 2018: 36 · 2017: 29 · 2016: 40 · 2015: 29 · 2014: 42 · 2013: 44 · 2012: 48
- FWCI
- 21.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Keywords
- aversive conditioning, emotional learning, classical conditioning, anterior cingulate cortex, anterior insula, amygdala, neural adaptation, emotional processing
- MeSH terms
- Amygdala, Cerebral Cortex, Conditioning, Classical, Evoked Potentials, Auditory, Evoked Potentials, Visual, Facial Expression, Female, Galvanic Skin Response, Gyrus Cinguli, Hemodynamics, Humans, Magnetic Resonance Imaging, Male, Motor Cortex, Red Nucleus
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