Human amygdala activity during the expression of fear responses.
Abstract
The initial learning and subsequent behavioral expression of fear are often viewed as independent processes with potentially unique neural substrates. Laboratory animal studies of Pavlovian fear conditioning suggest that the amygdala is important for both forming stimulus associations and for subsequently expressing learned behavioral responses. In the present article, human amygdala activity was studied during the autonomic expression of conditional fear in two differential conditioning experiments with event-related functional magnetic resonance imaging and concurrent recording of skin conductance responses (SCRs). Trials were classified on the basis of individual participants' SCRs. Significant amygdala responding was detected only during trials on which a signal both predicted shock and elicited significant conditional SCR. Conditional stimulus presentation or autonomic activity alone was not sufficient. These results indicate that amygdala activity may specifically reflect the expression of learned fear responses and support the position that this region plays a central role in the expression of emotional reactions.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Studies using a delay differential cue-conditioning paradigm were focused on because other paradigms (trace or single-cue) appear to engage non-overlapping neural responses.
“We focused on studies using a delay differential cue-conditioning paradigm given that other paradigms (for example, trace or single-cue) appear to engage non-overlapping neural responses.6,19”
From Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies (2016) · cites this paper as [19]
Cites
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913 · see citing works
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
Talairach, J., Tournoux, P., & Rayport, M. (1988) · Thieme eBooks · Cited by 5,058 · see citing works
Falk, J. L. (1973) · Contemporary Psychology · doi:10.1037/0011818 · Cited by 2,288 · see citing works
Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making
Bechara, A., Damasio, H., Damasio, A. R., & Lee, G. P. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05473.1999 · Cited by 2,001 · see citing works
Neurobiology of Pavlovian Fear Conditioning
Maren, S. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.897 · Cited by 1,805 · see citing works
Conscious and unconscious emotional learning in the human amygdala
Morris, J. S., Öhman, A., & Dolan, R. J. (1998) · Nature · doi:10.1038/30976 · Cited by 1,665 · see citing works
Building Memories: Remembering and Forgetting of Verbal Experiences as Predicted by Brain Activity
Wagner, A. D., Schacter, D. L., Rotte, M., Koutstaal, W., Maril, A., Dale, A. M., Rosen, B. R., & Buckner, R. L. (1998) · Science · doi:10.1126/science.281.5380.1188 · Cited by 1,620 · see citing works
LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E., & Phelps, E. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80475-4 · Cited by 1,402 · see citing works
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., & Damasio, A. R. (1995) · Science · doi:10.1126/science.7652558 · Cited by 1,400 · see citing works
Neural correlates of conscious self-regulation of emotion
Beauregard, M., Lévesque, J., & Bourgouin, P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-j0001.2001 · Cited by 1,033 · see citing works
The Amygdala: a functional analysis
Aggleton, J. P. (2000) · Cited by 964 · see citing works
Brain systems mediating aversive conditioning: an event-related fMRI study
Büchel, C., Morris, J., Dolan, R. J., & Friston, K. J. (1998) · Neuron · doi:10.1016/s0896-6273(00)80476-6 · Cited by 951 · see citing works
Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala
Fanselow, M. S., & LeDoux, J. E. (1999) · Neuron · doi:10.1016/s0896-6273(00)80775-8 · Cited by 914 · see citing works
Activation of the left amygdala to a cognitive representation of fear
Phelps, E. A., O'Connor, K. J., Gatenby, J. C., Gore, J. C., Grillon, C., & Davis, M. (2001) · Nature Neuroscience · doi:10.1038/86110 · Cited by 895 · see citing works
Neocortical modulation of the amygdala response to fearful stimuli
Hariri, A. R., Mattay, V. S., Tessitore, A., Fera, F., & Weinberger, D. R. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01786-9 · Cited by 828 · see citing works
Critchley, H. D., Elliott, R., Mathias, C. J., & Dolan, R. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-08-03033.2000 · Cited by 813 · see citing works
Impaired fear conditioning following unilateral temporal lobectomy in humans
LaBar, K., LeDoux, J., Spencer, D., & Phelps, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06846.1995 · Cited by 631 · see citing works
Electrodermal Activity in Psychological Research
(1973) · Elsevier eBooks · doi:10.1016/b978-0-12-565950-5.x5001-7 · Cited by 514 · see citing works
Campeau, S., & Davis, M. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-03-02301.1995 · Cited by 479 · see citing works
Long-term potentiation in the amygdala: a mechanism for emotional learning and memory
Maren, S. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01465-4 · Cited by 456 · see citing works
Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study
Armony, J. L. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(01)00178-6 · Cited by 411 · see citing works
Büchel, C., Dolan, R. J., Armony, J. L., & Friston, K. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-10869.1999 · Cited by 404 · see citing works
Williams, L. M., Phillips, M. L., Brammer, M. J., Skerrett, D., Lagopoulos, J., Rennie, C., Bahramali, H., Olivieri, G., David, A. S., Peduto, A., et al. (2001) · NeuroImage · doi:10.1006/nimg.2001.0904 · Cited by 300 · see citing works
Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning
Knight, D. C., Smith, C. N., Cheng, D. T., Stein, E. A., & Helmstetter, F. J. (2004) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.4.3.317 · Cited by 249 · see citing works
Self-citationNeural Substrates Mediating Human Delay and Trace Fear Conditioning
Knight, D. C., Cheng, D. T., Smith, C. N., Stein, E. A., & Helmstetter, F. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0433-03.2004 · Cited by 239 · see citing works
Self-citationMorris, J. S., Büchel, C., & Dolan, R. J. (2001) · NeuroImage · doi:10.1006/nimg.2000.0721 · Cited by 212 · see citing works
Cheng, D. T., Knight, D. C., Smith, C. N., Stein, E. A., & Helmstetter, F. J. (2003) · Behavioral Neuroscience · doi:10.1037//0735-7044.117.1.3 · Cited by 160 · see citing works
Self-citationTask-Independent Functional Brain Activity Correlation with Skin Conductance Changes: An fMRI Study
Patterson, J. (2002) · NeuroImage · doi:10.1006/nimg.2002.1306 · Cited by 153 · see citing works
An analysis of GSR conditioning.
Stewart, M., Stern, J. A., Winokur, G., & Fredman, S. (1961) · Psychological Review · doi:10.1037/h0048816 · Cited by 145 · see citing works
Tranel, D., & Damasio, A. R. (1993) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1993.5.1.79 · Cited by 134 · see citing works
Contribution of the amygdala to learning and performance of conditional fear.
Helmstetter, F. J. (1992) · Physiology and Behavior · doi:10.1016/0031-9384(92)90320-2 · Cited by 123 · see citing works
Self-citationIntact electrodermal skin conductance responses after bilateral amygdala damage
Tranel, D., & Damásio, H. (1989) · Neuropsychologia · doi:10.1016/0028-3932(89)90046-8 · Cited by 97 · see citing works
Neural systems for the expression of hypoalgesia during nonassociative fear.
Bellgowan, P. S. F., & Helmstetter, F. J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.4.727 · Cited by 76 · see citing works
Self-citationSotty, F., Sandner, G., & Gosselin, O. (1996) · Brain Research · doi:10.1016/0006-8993(96)00737-8 · Cited by 54 · see citing works
Basolateral amygdala lesions disrupt latent inhibitionin rats
Coutureau, É., Blundell-Birtill, P., & Killcross, S. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00592-5 · Cited by 42 · see citing works
Amount of conditioning and intensity of conditioned stimulus.
Kimmel, H. D. (1959) · Journal of Experimental Psychology · doi:10.1037/h0048529 · Cited by 33 · see citing works
Wolter, J., & Lachnit, H. (1993) · Integrative Psychological and Behavioral Science · doi:10.1007/bf02691221 · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Neurocircuitry of Fear, Stress, and Anxiety Disorders
Shin, L. M., & Liberzon, I. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.83 · Cited by 2,083 · see citing works
Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies
Fullana, M. A., Harrison, B. J., Soriano-Mas, C., Vervliet, B., Cardoner, N., Àvila-Parcet, A., & Radua, J. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.88 · Cited by 702 · see citing works
Human Fear Conditioning and Extinction in Neuroimaging: A Systematic Review
Sehlmeyer, C., Schöning, S., Zwitserlood, P., Pfleiderer, B., Kircher, T., Arolt, V., & Konrad, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005865 · Cited by 543 · see citing works
A Role for the Human Dorsal Anterior Cingulate Cortex in Fear Expression
Milad, M. R., Quirk, G. J., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.032 · Cited by 485 · see citing works
Implications of memory modulation for post-traumatic stress and fear disorders
Parsons, R. G., & Ressler, K. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3296 · Cited by 476 · see citing works
Overlapping neural systems mediating extinction, reversal and regulation of fear
Schiller, D., & Delgado, M. R. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.04.002 · Cited by 294 · see citing works
Pineles, S. L., Orr, M. R., & Orr, S. P. (2009) · Psychophysiology · doi:10.1111/j.1469-8986.2009.00852.x · Cited by 149 · see citing works
Dunsmoor, J. E., Bandettini, P. A., & Knight, D. C. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.4.635 · Cited by 137 · see citing works
Self-citationWegerer, M., Blechert, J., Kerschbaum, H., & Wilhelm, F. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079025 · Cited by 85 · see citing works
Sensitive periods in affective development: nonlinear maturation of fear learning
Hartley, C. A., & Lee, F. S. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.179 · Cited by 80 · see citing works
van Well, S., Visser, R. M., Scholte, H. S., & Kindt, M. (2012) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-012-0089-7 · Cited by 75 · see citing works
Current emotion research in behavioral neuroscience: the role(s) of the amygdala
Armony, J. L. (2013) · Emotion Review · doi:10.1177/1754073912457208 · Cited by 44 · see citing works
Harnett, N. G., Wood, K. H., Ference, E. W., Reid, M. A., Lahti, A. C., Knight, A. J., & Knight, D. C. (2017) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.04.010 · Cited by 31 · see citing works
Self-citation
- Authors
- Cheng, D. T., Knight, D. C., Smith, C. N., & Helmstetter, F. J.
- Affiliations
- University of Wisconsin–Milwaukee (US)
- Venue
- Behavioral Neuroscience
- Published
- 2006
- Volume
- 120
- Issue
- 6
- Pages
- 1187-1195
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- OpenAlex
- W2012065259
- Cited by
- 131
- References
- 38
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 6 · 2022: 2 · 2021: 3 · 2020: 8 · 2019: 9 · 2018: 4 · 2017: 9 · 2016: 6 · 2015: 7 · 2014: 11 · 2013: 12 · 2012: 9
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- McDonnell-Pew Foundation
- National Institute of Mental Health (MH060668)
- Bill and Melinda Gates Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Keywords
- amygdala, fear expression, fear conditioning, skin conductance response, emotional learning, conditioned stimulus
- MeSH terms
- Adolescent, Adult, Amygdala, Analysis of Variance, Animals, Brain Mapping, Conditioning, Classical, Electric Stimulation, Fear, Galvanic Skin Response, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Oxygen, Photic Stimulation, Expressed Emotion
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review