The DOI matches its Crossref record; 73 of the 73 references it cites were found in a registry or an index.
Noradrenaline mediates amygdala activation in men and women during encoding of emotional material
Abstract
The amygdala is a pivotal structure in humans for encoding of emotional information, as shown by recent imaging studies. It is unknown which neurotransmitters are specifically involved in the human amygdala, although in animal studies noradrenaline was shown to be essential. In our study, participants received the betablocker propranolol (which blocks the noradrenergic response) or placebo when watching neutral to highly negative arousing pictures. Amygdala activation, monitored with functional magnetic resonance imaging (fMRI), increased with emotional intensity of the pictures under placebo condition. Betablockade selectively decreased amygdala activation for emotional pictures of the second highest category, but not for the highest or lower (neutral) category pictures. Two findings add to the existing knowledge in this area. First, the activation pattern in the amygdala under placebo condition shows a nonlinearity related to the emotional categories of the pictures. Second, propranolol disturbs this activation pattern in the amygdala. Explorations with respect to gender show a similar effect of betablockade on amygdala activation in both men and women, but a difference in its effect on long-term memory for emotional pictures. This study supports the hypothesis that the neurotransmitter noradrenaline also mediates amygdala activity in humans when processing emotional stimuli and that betablockers can disrupt the normal activation pattern in the amygdala.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
In the citing paper
“prior studies have shown that propranolol can reduce amygdala response to visual stimuli associated with negative emotions such as fear and anger (Van Stegeren et al. 2005)”
From Propranolol reduces implicit negative racial bias (2012) · cites this paper as Van Stegeren et al. 2005
In the citing paper
“functional neuroimaging studies have also shown that propranolol leads to a reduction in amygdala responses to both facial expressions and visual emotional stimuli (Hurlemann et al. 2010a, b; van Stegeren et al. 2005).”
From Propranolol reduces implicit negative racial bias (2012) · cites this paper as van Stegeren et al. 2005
Citations
Cites
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002) · NeuroImage · doi:10.1006/nimg.2002.1132 · Cited by 11,888
Fast robust automated brain extraction
Smith, S. M. (2002) · Human Brain Mapping · doi:10.1002/hbm.10062 · Cited by 10,496
A global optimisation method for robust affine registration of brain images
Jenkinson, M., & Smith, S. M. (2001) · Medical Image Analysis · doi:10.1016/s1361-8415(01)00036-6 · Cited by 7,018
Goodman and Gilman's the Pharmacological Basis of Therapeutics
Stigelman, W. H., & Pharm, D. (1986) · Military Medicine · doi:10.1093/milmed/151.1.386 · Cited by 6,796
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250
Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910330508 · Cited by 3,202
Looking at pictures: Affective, facial, visceral, and behavioral reactions
LANG, P. J., GREENWALD, M. K., BRADLEY, M. M., & HAMM, A. O. (1993) · Psychophysiology · doi:10.1111/j.1469-8986.1993.tb03352.x · Cited by 3,190
Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data
Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001) · NeuroImage · doi:10.1006/nimg.2001.0931 · Cited by 2,859
Goodman and Gilman's The Pharmacological Basis of Therapeutics
Hastings, R. C. (1996) · JAMA · doi:10.1001/jama.1996.03540120077042 · Cited by 2,375
A three-dimensional statistical analysis for CBF activation studies in human brain
Worsley, K. J., Evans, A. C., Marrett, S., & Neelin, P. (1992) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1992.127 · Cited by 2,036
Assessing the significance of focal activations using their spatial extent
Friston, K. J., Worsley, K. J., Frackowiak, R. S. J., Mazziotta, J. C., & Evans, A. C. (1994) · Human Brain Mapping · doi:10.1002/hbm.460010306 · Cited by 1,907
Human emotion and memory: Interactions of the amygdala and hippocampal complex
Phelps, E. A. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.015 · Cited by 1,577
General multilevel linear modeling for group analysis in FMRI
Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00435-x · Cited by 1,464
Lesions of the human amygdala impair enhanced perception of emotionally salient events
Anderson, A. K., & Phelps, E. A. (2001) · Nature · doi:10.1038/35077083 · Cited by 1,379
β-Adrenergic activation and memory for emotional events
Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994) · Nature · doi:10.1038/371702a0 · Cited by 1,271
Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics
Friston, K. J., Mechelli, A., Turner, R., & Price, C. J. (2000) · NeuroImage · doi:10.1006/nimg.2000.0630 · Cited by 1,131
The human amygdala and the emotional evaluation of sensory stimuli
Zald, D. H. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00248-5 · Cited by 1,062
Amygdala activity related to enhanced memory for pleasant and aversive stimuli
Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D. (1999) · Nature Neuroscience · doi:10.1038/6404 · Cited by 941
Amygdala activity at encoding correlated with long-term, free recall of emotional information.
Cahill, L. F., Haier, R. J., Fallon, J., Alkire, M. T., Tang, C. Y., Keator, D., Wu, J. C., & McGaugh, J. L. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.8016 · Cited by 928
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
Two routes to emotional memory: Distinct neural processes for valence and arousal
Kensinger, E. A., & Corkin, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306408101 · Cited by 848
Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval
Roozendaal, B. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4080 · Cited by 838
Neuroanatomical correlates of happiness, sadness, and disgust
Lane, R. D., Reiman, E. M., Ahern, G. L., SCHWARTZ, G. E. R., & Davidson, R. J. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.7.926 · Cited by 756
Involvement of the amygdala in memory storage: Interaction with other brain systems
McGaugh, J. L., Cahill, L. F., & Roozendaal, B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13508 · Cited by 747
Dolcos, F., LaBar, K. S., & Cabeza, R. (2004) · Neuron · doi:10.1016/s0896-6273(04)00289-2 · Cited by 714
Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D. E., & Cahill, L. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-19-j0004.2000 · Cited by 697
Representation of Pleasant and Aversive Taste in the Human Brain
O’Doherty, J. P., Rolls, E. T., Francis, S., Bowtell, R. W., & McGlone, F. P. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.3.1315 · Cited by 688
Sex differences in the neural basis of emotional memories
Canli, T., Desmond, J. E., Zhao, Z., & Gabrieli, J. D. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162356599 · Cited by 664
Cahill, L., Gorski, L., & Le, K. (2003) · Learning & Memory · doi:10.1101/lm.62403 · Cited by 660
Men and women differ in amygdala response to visual sexual stimuli
Hamann, S., Herman, R. A., Nolan, C. L., & Wallen, K. (2004) · Nature Neuroscience · doi:10.1038/nn1208 · Cited by 603
Encoding of emotional memories depends on amygdala and hippocampus and their interactions
Richardson, M., Strange, B., & Dolan, R. (2004) · Nature Neuroscience · doi:10.1038/nn1190 · Cited by 591
Variations in sex-related cognitive abilities across the menstrual cycle
Hampson, E. (1990) · Brain and Cognition · doi:10.1016/0278-2626(90)90058-v · Cited by 571
Estrogen-related variations in human spatial and articulatory-motor skills
Hampson, E. (1990) · Psychoneuroendocrinology · doi:10.1016/0306-4530(90)90018-5 · Cited by 534
Individual differences in emotion processing
Hamann, S. B., & Canli, T. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.010 · Cited by 489
Lane, R. D., Chua, P. M.-L., & Dolan, R. J. (1999) · Neuropsychologia · doi:10.1016/s0028-3932(99)00017-2 · Cited by 479
Sex-related difference in amygdala activity during emotionally influenced memory storage
Cahill, L., Haier, R. J., White, N. S., Fallon, J., Kilpatrick, L., Lawrence, C., Potkin, S. G., & Alkire, M. T. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2000.3999 · Cited by 413
Quirarte, G. L., Roozendaal, B., & McGaugh, J. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.14048 · Cited by 386
Cahill, L. F., Uncapher, M. R., Kilpatrick, L. A., Alkire, M. T., & Turner, J. A. (2004) · Learning & Memory · doi:10.1101/lm.70504 · Cited by 362
Neuroimaging findings in post-traumatic stress disorder
Hull, A. M. (2002) · The British Journal of Psychiatry · doi:10.1017/s000712500016180x · Cited by 351
Roozendaal, B., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0001 · Cited by 317
Amygdala response to both positively and negatively valenced stimuli
Garavan, H., Pendergrass, J. C., Ross, T. J., Stein, E. A., & Risinger, R. C. (2001) · Neuroreport · doi:10.1097/00001756-200108280-00036 · Cited by 312
Neuroimaging findings in post-traumatic stress disorder. Systematic review.
Hull, A. M. (2002) · PubMed · Cited by 307
Roozendaal, B., & McGaugh, J. L. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01355.x · Cited by 307
Kilpatrick, L. A. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.08.006 · Cited by 294
Emotional context modulates subsequent memory effect
Erk, S., Kiefer, M., Grothe, J., Wunderlich, A. P., Spitzer, M., & Walter, H. (2003) · NeuroImage · doi:10.1016/s1053-8119(02)00015-0 · Cited by 278
An emotion-induced retrograde amnesia in humans is amygdala- and β-adrenergic-dependent
Strange, B. A., Hurlemann, R., & Dolan, R. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1635116100 · Cited by 273
Roozendaal, B., Quirarte, G. L., & McGaugh, J. L. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01876.x · Cited by 260
Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study
Fischer, H., Wright, C. I., Whalen, P. J., McInerney, S. C., Shin, L. M., & Rauch, S. L. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00940-1 · Cited by 250
Ferry, B., Roozendaal, B., & McGaugh, J. L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-12-05119.1999 · Cited by 243
van Stegeren, A. H., Everaerd, W., Cahill, L., McGaugh, J. L., & Gooren, L. J. G. (1998) · Psychopharmacology · doi:10.1007/s002130050675 · Cited by 230
Self-citationPhan, K. L., Taylor, S. F., Welsh, R. C., Decker, L. R., Noll, D. C., Nichols, T. E., Britton, J. C., & Liberzon, I. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01485-3 · Cited by 207
The Neural Correlates of Aversive Auditory Stimulation
Zald, D. H., & Pardo, J. V. (2002) · NeuroImage · doi:10.1006/nimg.2002.1115 · Cited by 190
O’Carroll, R. E., Drysdale, E. E., Cahill, L. F., Shajahan, P. M., & Ebmeier, K. P. (1999) · Psychological Medicine · doi:10.1017/s0033291799008703 · Cited by 166
Maheu, F. S., Joober, R., Beaulieu, S., & LUPIEN, S. J. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.420 · Cited by 165
Southwick, S. M., Davis, M. E., Horner, B., Cahill, L. F., Morgan, C. A., Gold, P. E., Bremner, J. D., & Charney, D. C. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.8.1420 · Cited by 156
Ferry, B., & McGaugh, J. L. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3904 · Cited by 149
Role of the Basolateral Amygdala in Memory Consolidation
McINTYRE, C. K., POWER, A. E., ROOZENDAAL, B., & McGAUGH, J. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07088.x · Cited by 147
Sex-related impairment of memory for emotional events with β-adrenergic blockade
Cahill, L., & van Stegeren, A. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(02)00019-9 · Cited by 145
Involvement of α1-adrenoceptors in the basolateral amygdala in modulation of memory storage
Ferry, B., Roozendaal, B., & McGaugh, J. L. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00169-7 · Cited by 142
Roozendaal, B., de Quervain, D. J.-F., Ferry, B., Setlow, B., & McGaugh, J. L. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-07-02518.2001 · Cited by 128
Impaired Emotional Declarative Memory Following Unilateral Amygdala DamagePreprint
Adolphs, R., Tranel, D., & Denburg, N. L. (2000) · Learning & Memory · doi:10.1101/lm.7.3.180 · Cited by 126
Sex‐Related Influences on the Neurobiology of Emotionally Influenced Memory
Cahill, L. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07080.x · Cited by 113
Hemodynamic responses to fear and disgust-inducing pictures: an fMRI study
Stark, R. M. (2003) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(03)00169-7 · Cited by 101
Time course of the subjective emotional response to aversive pictures: relevance to fMRI studies
Garrett, A. S., & Maddock, R. J. (2001) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(01)00110-x · Cited by 77
The amygdala and sexual drive: Insights from temporal lobe epilepsy surgery
Baird, A., Wilson, S. J., Bladin, P., Saling, M., & Reutens, D. (2004) · Annals of Neurology · doi:10.1002/ana.10997 · Cited by 74
Nonlinear Coupling between Evoked rCBF and BOLD Signals: A Simulation Study of Hemodynamic Responses
Mechelli, A., Price, C. J., & Friston, K. J. (2001) · NeuroImage · doi:10.1006/nimg.2001.0876 · Cited by 69
Oestrogen Modulation of Noradrenaline Neurotransmission
Herbison, A. E., Simonian, S. X., Thanky, N. R., & Bicknell, R. J. (2000) · Novartis Foundation symposium · doi:10.1002/0470870818.ch7 · Cited by 62
Real-time fMRI of cortico-limbic brain activity during emotional processing
Phan, K. L., Fitzgerald, D. A., Gao, K., Moore, G. J., Tancer, M. E., & Posse, S. (2004) · Neuroreport · doi:10.1097/00001756-200403010-00029 · Cited by 52
Ethnicity, gender, and age effects on adrenoceptors and physiological responses to emotional stress
Suarez, E. C., Saab, P. G., Llabre, M. M., Kuhn, C. M., & Zimmerman, E. A. (2004) · Psychophysiology · doi:10.1111/j.1469-8986.00161.x · Cited by 43
The effect of beta-adrenergic blockade after encoding on memory of an emotional event
van Stegeren, A. V., Everaerd, W., & Gooren, L. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1163-6 · Cited by 40
Self-citationImaging gender differences in sexual arousal
Canli, T., & Gabrieli, J. D. E. (2004) · Nature Neuroscience · doi:10.1038/nn0404-325 · Cited by 29
La mémoire aux prises avec les émotions et le stress : un impact nécessairement dommageable?
Maheu, F. S., & Lupienn, S. J. (2003) · médecine/sciences · doi:10.1051/medsci/2003191118 · Cited by 27
Beta‐adrenoceptor blocker pharmacokinetics and the oral contraceptive pill.
Kendall, M. J., Jack, D. B., Quarterman, C., Smith, S., & Zaman, R. (1984) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.1984.tb02435.x · Cited by 24
Research works printed but not linked: 1
- Suarez, 2004, Ethnicity, gender, and age effects on adrenoceptors and physiological responses to emotional stress, Null, 41, 450
Cited by
Sorted by citations
Cognitive neuroscience of emotional memory
LaBar, K. S., & Cabeza, R. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1825 · Cited by 1,834
Gender differences in posttraumatic stress disorder.
Olff, M., Langeland, W., Draijer, N., & Gersons, B. P. R. (2007) · Psychological Bulletin · doi:10.1037/0033-2909.133.2.183 · Cited by 1,058
Ruffman, T., Henry, J. D., Livingstone, V., & Phillips, L. H. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.01.001 · Cited by 984
Sergerie, K., Chochol, C., & Armony, J. L. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.12.002 · Cited by 917
Beyond extinction: erasing human fear responses and preventing the return of fear
Kindt, M., Soeter, M., & Vervliet, B. (2009) · Nature Neuroscience · doi:10.1038/nn.2271 · Cited by 826
Metadata
- Authors
- van Stegeren, A. H., Goekoop, R., Everaerd, W., Scheltens, P., Barkhof, F., Kuijer, J. P. A., & Rombouts, S. A. R. B.
- Affiliations
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- University of Amsterdam (NL)
- ORCID
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2005-02
- Volume
- 24
- Issue
- 3
- Pages
- 898-909
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2020947884
- Cited by
- 212
- References
- 73
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 5 · 2022: 4 · 2021: 4 · 2020: 6 · 2019: 1 · 2018: 14 · 2017: 7 · 2016: 10 · 2015: 9 · 2014: 17 · 2013: 13 · 2012: 18
- FWCI
- 6.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- 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 › Memory Processes and Influences
- Keywords
- norepinephrine, amygdala activation, propranolol, beta-adrenergic blockade, emotional intensity, sex differences, emotional arousal
- MeSH terms
- Adolescent, Adrenergic beta-Antagonists, Adult, Amygdala, Double-Blind Method, Emotions, Female, Humans, Image Interpretation, Computer-Assisted, Functional Laterality, Magnetic Resonance Imaging, Male, Memory, Norepinephrine, Propranolol, Sex Characteristics
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