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.
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Propranolol can reduce amygdala response to visual stimuli associated with negative emotions such as fear and anger.
“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
Propranolol leads to a reduction in amygdala responses to facial expressions and visual emotional stimuli.
“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
Cites
Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002) · NeuroImage · doi:10.1006/nimg.2002.1132 · Cited by 11,888 · see citing works
Fast robust automated brain extraction
Smith, S. M. (2002) · Human Brain Mapping · doi:10.1002/hbm.10062 · Cited by 10,496 · see citing works
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 6,806 · see citing works
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 · see citing works
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Goodman and Gilman's The Pharmacological Basis of Therapeutics
Hastings, R. C. (1996) · JAMA · doi:10.1001/jama.1996.03540120077042 · Cited by 2,386 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 1,335 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 913 · see citing works
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 905 · 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
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 · see citing works
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 · see citing works
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 · see citing works
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 742 · see citing works
Dolcos, F., LaBar, K. S., & Cabeza, R. (2004) · Neuron · doi:10.1016/s0896-6273(04)00289-2 · Cited by 714 · see citing works
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 · see citing works
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 674 · see citing works
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 · see citing works
Cahill, L., Gorski, L., & Le, K. (2003) · Learning & Memory · doi:10.1101/lm.62403 · Cited by 660 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Estrogen-related variations in human spatial and articulatory-motor skills
Hampson, E. (1990) · Psychoneuroendocrinology · doi:10.1016/0306-4530(90)90018-5 · Cited by 529 · see citing works
Lane, R. D., Chua, P. M.-L., & Dolan, R. J. (1999) · Neuropsychologia · doi:10.1016/s0028-3932(99)00017-2 · Cited by 479 · see citing works
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 471 · see citing works
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 · see citing works
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 385 · see citing works
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 · see citing works
Neuroimaging findings in post-traumatic stress disorder
Hull, A. M. (2002) · The British Journal of Psychiatry · doi:10.1017/s000712500016180x · Cited by 343 · see citing works
Roozendaal, B., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0001 · Cited by 317 · see citing works
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 · see citing works
Neuroimaging findings in post-traumatic stress disorder. Systematic review.
Hull, A. M. (2002) · PubMed · Cited by 307 · see citing works
Roozendaal, B., & McGaugh, J. L. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01355.x · Cited by 306 · see citing works
Kilpatrick, L. A. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.08.006 · Cited by 294 · see citing works
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 280 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Ferry, B., Roozendaal, B., & McGaugh, J. L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-12-05119.1999 · Cited by 243 · see citing works
van Stegeren, A. H., Everaerd, W., Cahill, L., McGaugh, J. L., & Gooren, L. J. G. (1998) · Psychopharmacology · doi:10.1007/s002130050675 · Cited by 230 · see citing works
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 · see citing works
The Neural Correlates of Aversive Auditory Stimulation
Zald, D. H., & Pardo, J. V. (2002) · NeuroImage · doi:10.1006/nimg.2002.1115 · Cited by 181 · see citing works
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 · see citing works
Maheu, F. S., Joober, R., Beaulieu, S., & LUPIEN, S. J. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.420 · Cited by 165 · see citing works
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 · see citing works
Ferry, B., & McGaugh, J. L. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3904 · Cited by 149 · see citing works
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 · see citing works
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 · see citing works
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 144 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 99 · see citing works
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 76 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationImaging gender differences in sexual arousal
Canli, T., & Gabrieli, J. D. E. (2004) · Nature Neuroscience · doi:10.1038/nn0404-325 · Cited by 29 · see citing works
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 · see citing works
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 · see citing works
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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 · see citing works
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 · see citing works
Ruffman, T., Henry, J., Livingstone, V., & Phillips, L. (2008) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.01.001 · Cited by 944 · see citing works
Sergerie, K., Chochol, C., & Armony, J. L. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.12.002 · Cited by 917 · see citing works
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 · see citing works
Impaired Memory Retrieval after Psychosocial Stress in Healthy Young Men
Kuhlmann, S., Piel, M., & Wolf, O. T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5139-04.2005 · Cited by 680 · see citing works
Glucocorticoids and the regulation of memory in health and disease
de Quervain, D. J. ‐., Aerni, A., Schelling, G., & Roozendaal, B. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.002 · Cited by 496 · see citing works
Roozendaal, B., Okuda, S., van der Zee, E. A., & McGaugh, J. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601874103 · Cited by 499 · see citing works
Roozendaal, B., & McGaugh, J. L. (2011) · Behavioral Neuroscience · doi:10.1037/a0026187 · Cited by 445 · see citing works
The genetics of sex differences in brain and behavior
Ngun, T. C., Ghahramani, N., Sánchez, F. J., Bocklandt, S., & Vilain, E. J. N. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.10.001 · Cited by 437 · see citing works
Salivary alpha amylase as marker for adrenergic activity during stress: Effect of betablockade
van Stegeren, A., Rohleder, N., Everaerd, W., & Wolf, O. T. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.05.012 · Cited by 419 · see citing works
Self-citationRoozendaal, B., Okuda, S., de Quervain, D. J.-F., & McGaugh, J. L. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.049 · Cited by 382 · see citing works
van Marle, H. J. F., Hermans, E. J., Qin, S., & Fernández, G. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.05.014 · Cited by 317 · see citing works
fMRI studies of successful emotional memory encoding: a quantitative meta-analysis
Murty, V. P., Ritchey, M., Adcock, R., & LaBar, K. S. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.07.030 · Cited by 313 · see citing works
Dissociating response systems: Erasing fear from memory
Soeter, M., & Kindt, M. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.03.004 · Cited by 290 · see citing works
Making lasting memories: Remembering the significant
McGaugh, J. D. (2013) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1301209110 · Cited by 291 · see citing works
Emotional enhancement of memory: how norepinephrine enables synaptic plasticity
Tully, K., & Bolshakov, V. Y. (2010) · Molecular Brain · doi:10.1186/1756-6606-3-15 · Cited by 278 · see citing works
Neuropsychological mechanism underlying antidepressant effect: a systematic meta-analysis
Ma, Y. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.24 · Cited by 270 · see citing works
McGaugh, J. L. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-014954 · Cited by 271 · see citing works
van Marle, H. J. F., Hermans, E. J., Qin, S., & Fernández, G. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.05.070 · Cited by 251 · see citing works
Salivary alpha amylase and cortisol responses to different stress tasks: Impact of sex
van Stegeren, A. H., Wolf, O. T., & Kindt, M. (2008) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2008.02.008 · Cited by 249 · see citing works
Lonergan, M. H., Olivera-Figueroa, L. A., Pitman, R. K., & Brunet, A. (2013) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.120111 · Cited by 237 · see citing works
The influence of stress hormones on emotional memory: Relevance for psychopathology
Wolf, O. T. (2007) · Acta Psychologica · doi:10.1016/j.actpsy.2007.08.002 · Cited by 233 · see citing works
Interacting Brain Systems Modulate Memory Consolidation
McIntyre, C. K., McGaugh, J. D., & Williams, C. (2011) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.11.001 · Cited by 233 · see citing works
Roozendaal, B., Castello, N. A., Vedana, G., Barsegyan, A., & McGaugh, J. L. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.06.010 · Cited by 216 · see citing works
Make mild moments memorable: add a little arousal
McGaugh, J. L. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.06.001 · Cited by 196 · see citing works
Arousal and cortisol interact in modulating memory consolidation in healthy young men.
Kuhlmann, S., & Wolf, O. T. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.217 · Cited by 194 · see citing works
The brainstem noradrenergic systems in stress, anxiety and depression
Itoi, K., & Sugimoto, N. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01988.x · Cited by 207 · see citing works
Noradrenergic modulation of cognition: Therapeutic implications
Chamberlain, S. R., & Robbins, T. W. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881113480988 · Cited by 193 · see citing works
Noradrenergic modulation of working memory and emotional memory in humans
Chamberlain, S. R., Müller, U., Blackwell, A. D., Robbins, T. W., & Sahakian, B. J. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0391-6 · Cited by 170 · see citing works
Endogenous cortisol level interacts with noradrenergic activation in the human amygdala
van Stegeren, A. H., Wolf, O. T., Everaerd, W. T. A. M., Scheltens, P., Barkhof, F., & Rombouts, S. A. R. B. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.05.008 · Cited by 170 · see citing works
Self-citationStark, R., Wolf, O. T., Tabbert, K., Kagerer, S., Zimmermann, M., Kirsch, P., Schienle, A., & Vaitl, D. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.05.046 · Cited by 167 · see citing works
Neurobiology of anxiety disorders and implications for treatment.
Garakani, A., Mathew, S. J., & Charney, D. S. (2006) · PubMed · Cited by 165 · see citing works
How the amygdala affects emotional memory by altering brain network properties
Hermans, E. J., Battaglia, F. P., Atsak, P., de Voogd, L. D., Fernández, G., & Roozendaal, B. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.02.005 · Cited by 162 · see citing works
Noradrenergic Modulation of Emotion-Induced Forgetting and Remembering
Hurlemann, R., Hawellek, B., Matusch, A., Kölsch, H., Wollersen, H., Madea, B., Vogeley, K., Maier, W., & Dolan, R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0228-05.2005 · Cited by 171 · see citing works
Henry, M., Fishman, J. R., & Youngner, S. J. (2007) · The American Journal of Bioethics · doi:10.1080/15265160701518474 · Cited by 156 · see citing works
Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences
Roozendaal, B., Barsegyan, A., & Lee, S. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67006-x · Cited by 154 · see citing works
Segal, S. K., Cotman, C. W., & Cahill, L. F. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-121078 · Cited by 153 · see citing works
Pharmacotherapy of PTSD: premises, principles, and priorities.
Ravindran, L. N., & Stein, M. B. (2009) · Brain Research · doi:10.1016/j.brainres.2009.03.037 · Cited by 153 · see citing works
Propranolol reduces implicit negative racial bias
Terbeck, S., Kahane, G., McTavish, S., Savulescu, J., Cowen, P. J., & Hewstone, M. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2657-5 · Cited by 149 · see citing works
The role of the noradrenergic system in emotional memory.
van Stegeren, A. V. (2008) · Acta Psychologica · doi:10.1016/j.actpsy.2007.10.004 · Cited by 102 · see citing works
Schwabe, L., & Schächinger, H. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.03.010 · Cited by 148 · see citing works
van Stegeren, A. V., Roozendaal, B., Kindt, M., Wolf, O. T., & Joëls, M. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.08.004 · Cited by 148 · see citing works
Cornelisse, S., van Stegeren, A. H., & Joëls, M. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.09.002 · Cited by 133 · see citing works
The Neural Correlates of Emotional Memory in Posttraumatic Stress Disorder
Brohawn, K. H., Offringa, R., Pfaff, D. L., Hughes, K. C., & Shin, L. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.07.018 · Cited by 127 · see citing works
Muehlhan, M., Lueken, U., Wïttchen, H., & Kirschbaum, C. (2010) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2010.09.009 · Cited by 124 · see citing works
Locus coeruleus activation by foot shock or electrical stimulation inhibits amygdala neurons
Chen, F.-J., & Sara, S. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.037 · Cited by 123 · see citing works
Roozendaal, B., Schelling, G., & McGaugh, J. L. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1336-08.2008 · Cited by 115 · see citing works
Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI
Merz, C. J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R. M., & Wolf, O. T. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.009 · Cited by 115 · see citing works
Human amygdala reactivity is diminished by the β-noradrenergic antagonist propranolol
Hurlemann, R., Walter, H., Rehme, A., Kukolja, J., Santoro, S. C., Schmidt, C., Schnell, K., Musshoff, F., Keysers, C., Maier, W., et al. (2010) · Psychological Medicine · doi:10.1017/s0033291709992376 · Cited by 122 · see citing works
Endogenous noradrenergic activation and memory for emotional material in men and women.
Segal, S., & Cahill, L. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.04.020 · Cited by 110 · see citing works
Henckens, M. J. A. G., Klumpers, F., Everaerd, D., Kooijman, S. C., van Wingen, G. A., & Fernández, G. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv149 · Cited by 104 · see citing works
Tollenaar, M. S., Elzinga, B. M., Spinhoven, P., & Everaerd, W. T. A. M. (2008) · Acta Psychologica · doi:10.1016/j.actpsy.2007.10.007 · Cited by 101 · see citing works
Self-citationCatecholamines and cognition after traumatic brain injury
Jenkins, P. O., Mehta, M. A., & Sharp, D. J. (2016) · Brain · doi:10.1093/brain/aww128 · Cited by 102 · see citing works
Modeling a Negative Response Bias in the Human Amygdala by Noradrenergic–Glucocorticoid Interactions
Kukolja, J., Schlaepfer, T. E., Keysers, C., Klingmüller, D., Maier, W., Fink, G. R., & Hurlemann, R. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3592-08.2008 · Cited by 96 · see citing works
Norepinephrine-mediated emotional arousal facilitates subsequent pattern separation
Segal, S. K., Stark, S. M., Kattan, D., Stark, C. E. L., & Yassa, M. A. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.03.010 · Cited by 97 · see citing works
Electrophysiological correlates of remembering emotional pictures
Schaefer, A., Pottage, C. L., & Rickart, A. J. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.030 · Cited by 87 · see citing works
Barsegyan, A., McGaugh, J. L., & Roozendaal, B. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00160 · Cited by 84 · see citing works
A single bout of resistance exercise can enhance episodic memory performance
Weinberg, L., Hasni, A., Shinohara, M., & Duarte, A. (2014) · Acta Psychologica · doi:10.1016/j.actpsy.2014.06.011 · Cited by 82 · see citing works
Neuropharmacological modulation of cognition
Chamberlain, S. R., Müller, U., Robbins, T. W., & Sahakian, B. J. (2006) · Current Opinion in Neurology · doi:10.1097/01.wco.0000247613.28859.77 · Cited by 79 · see citing works
Kuhlmann, S., & Wolf, O. T. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.02.007 · Cited by 78 · see citing works
Langley, A., & Pope, E. (2014) · British Journal of Dermatology · doi:10.1111/bjd.13379 · Cited by 78 · see citing works
Age differences in perception and awareness of emotion
Neiss, M. B., Leigland, L. A., Carlson, N. E., & Janowsky, J. S. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.11.007 · Cited by 77 · see citing works
Villain, H., Benkahoul, A., Drougard, A., Lafragette, M., Muzotte, E., Pech, S., Bui, É., Brunet, A., Birmes, P. J., & Roullet, P. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00049 · Cited by 76 · see citing works
Atucha, E., Vukojević, V., Fornari, R. V., Ronzoni, G., Demougin, P., Peter, F., Atsak, P., Coolen, M. W., Papassotiropoulos, A., McGaugh, J. L., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710819114 · Cited by 77 · see citing works
Zhao, L., Zhang, X., Shi, J., Epstein, D. H., & Lü, L. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1406-2 · Cited by 73 · see citing works
The cognitive neuroscience of true and false memories.
Johnson, M. K., Raye, C. L., Mitchell, K., & Ankudowich, E. (2012) · Nebraska Symposium on Motivation. Nebraska Symposium on Motivation · doi:10.1007/978-1-4614-1195-6_2 · Cited by 50 · see citing works
Amygdala control of emotion-induced forgetting and remembering: evidence from Urbach-Wiethe disease.
Hurlemann, R., Wagner, M., Hawellek, B., Reich, H., Pieperhoff, P., Amunts, K., Oros-Peusquens, A., Shah, N., Maier, W., & Dolan, R. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.08.027 · Cited by 74 · see citing works
Hormones, Stress, and Cognition: The Effects of Glucocorticoids and Oxytocin on Memory
Wirth, M. M. (2014) · Adaptive Human Behavior and Physiology · doi:10.1007/s40750-014-0010-4 · Cited by 72 · see citing works
Noradrenaline effects on social behaviour, intergroup relations, and moral decisions
Terbeck, S., Savulescu, J., Chesterman, L. P., & Cowen, P. J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.031 · Cited by 68 · see citing works
The effects of noradrenergic blockade on extinction in humans
Bos, M. G. N., Beckers, T., & Kindt, M. (2012) · Biological Psychology · doi:10.1016/j.biopsycho.2012.01.007 · Cited by 67 · see citing works
Neural long-term effects of emotion regulation on episodic memory processes.
Erk, S., von Kalckreuth, A., & Walter, H. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.11.022 · Cited by 64 · see citing works
Event-Related Nociceptive Arousal Enhances Memory Consolidation for Neutral Scenes
Schwarze, U., Bingel, U., & Sommer, T. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4497-11.2012 · Cited by 63 · see citing works
Hoscheidt, S. M., LaBar, K. S., Ryan, L., Jacobs, W. J., & Nadel, L. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.008 · Cited by 62 · see citing works
Anterior medial temporal lobe in human cognition: Memory for fear and the unexpected
Strange, B. A., & Dolan, R. J. (2006) · Cognitive Neuropsychiatry · doi:10.1080/13546800500305096 · Cited by 60 · see citing works
Human cerebellum and corticocerebellar connections involved in emotional memory enhancement
Fastenrath, M., Spalek, K., Coynel, D., Loos, E., Milnik, A., Egli, T., Schicktanz, N. S., Geissmann, L., Roozendaal, B., Papassotiropoulos, A., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204900119 · Cited by 56 · see citing works
Blurring of emotional and non-emotional memories by taxing working memory during recall
van den Hout, M., Eidhof, M. B., Verboom, J., Littel, M., & Engelhard, I. M. (2013) · Cognition & Emotion · doi:10.1080/02699931.2013.848785 · Cited by 59 · see citing works
Are You Morally Modified?: The Moral Effects of Widely Used Pharmaceuticals
Levy, N. L., Douglas, T., Kahane, G., Terbeck, S., Cowen, P. J., Hewstone, M., & Savulescu, J. (2014) · Philosophy, psychiatry & psychology · doi:10.1353/ppp.2014.0023 · Cited by 58 · see citing works
Imaging Stress Effects on Memory: A Review of Neuroimaging Studies
van Stegeren, A. H. (2009) · The Canadian Journal of Psychiatry · doi:10.1177/070674370905400105 · Cited by 56 · see citing works
Reprint of: fMRI studies of successful emotional memory encoding: A quantitative meta-analysis
Murty, V. P., Ritchey, M., Adcock, R., & LaBar, K. S. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.02.031 · Cited by 60 · see citing works
Ventura‐Bort, C., Wirkner, J., Wendt, J., Hamm, A. O., & Weymar, M. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2329-20.2021 · Cited by 50 · see citing works
The Roles of Noradrenergic and Glucocorticoid Activation in the Development of Intrusive Memories
Bryant, R. A., McGrath, C., & Felmingham, K. L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062675 · Cited by 51 · see citing works
Preventing Post Traumatic Stress Disorder: Are Drugs the Answer?
Fletcher, S. L., Creamer, M. C., & Forbes, D. (2010) · Australian & New Zealand Journal of Psychiatry · doi:10.3109/00048674.2010.509858 · Cited by 51 · see citing works
A Role for the Human Amygdala in Higher Cognition
Schaefer, A., & Gray, J. (2007) · Reviews in the Neurosciences · doi:10.1515/revneuro.2007.18.5.355 · Cited by 67 · see citing works
Bryant, R. A. (2021) · Clinical Psychology Review · doi:10.1016/j.cpr.2021.101981 · Cited by 53 · see citing works
Roozendaal, B., & Hermans, E. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.02.001 · Cited by 47 · see citing works
Opposite effects of noradrenergic arousal on amygdala processing of fearful faces in men and women
Schwabe, L., Höffken, O., Tegenthoff, M., & Wolf, O. T. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.01.057 · Cited by 46 · see citing works
Weymar, M., Löw, A., Modeß, C., Engel, G., Gründling, M., Petersmann, A., Siegmund, W., & Hamm, A. O. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.025 · Cited by 47 · see citing works
Own-sex effects in emotional memory for faces
Armony, J. L., & Sergerie, K. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.08.032 · Cited by 47 · see citing works
Interaction of endogenous cortisol and noradrenaline in the human amygdala
van Stegeren, A. H., Wolf, O. T., Everaerd, W. T. A. M., & Rombouts, S. A. R. B. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)67020-4 · Cited by 47 · see citing works
Self-citationAdrenal Stress Hormones and Enhanced Memory for Emotionally Arousing Experiences
McIntyre, C. K., & Roozendaal, B. (2007) · Frontiers in neuroscience · doi:10.1201/9781420008418.ch13 · Cited by 46 · see citing works
The Role of the Amygdala in Anxiety Disorders
Gina, L., Andrew, M., Jamie, L. A., & Michael, J. (2012) · InTech eBooks · doi:10.5772/50323 · Cited by 45 · see citing works
Smith, H. R., & Porrino, L. J. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0176-2 · Cited by 45 · see citing works
Oei, N. Y. L., Tollenaar, M. S., Elzinga, B. M., & Spinhoven, P. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.12.005 · Cited by 44 · see citing works
Kukolja, J., Thiel, C. M., Wolf, O. T., & Fink, G. R. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1275-8 · Cited by 44 · see citing works
Stress hormones are associated with the neuronal correlates of instructed fear conditioning
Merz, C. J., Stark, R. M., Vaitl, D., Tabbert, K., & Wolf, O. T. (2012) · Biological Psychology · doi:10.1016/j.biopsycho.2012.02.017 · Cited by 41 · see citing works
Examining the relationship between working memory consolidation and long-term consolidation
Cotton, K., & Ricker, T. J. (2022) · Psychonomic Bulletin & Review · doi:10.3758/s13423-022-02084-2 · Cited by 41 · see citing works
Krauseneck, T., Padberg, F., Roozendaal, B., Grathwohl, M., Weis, F. C., Hauer, D., Kaufmann, I., Schmoeckel, M., & Schelling, G. (2009) · Psychological Medicine · doi:10.1017/s0033291709990614 · Cited by 40 · see citing works
Pringle, A., McCabe, C., Cowen, P., & Harmer, C. (2013) · Journal of Psychopharmacology · doi:10.1177/0269881112474523 · Cited by 37 · see citing works
Noradrenergic-glucocorticoid modulation of emotional memory encoding in the human hippocampus
Kukolja, J., Klingmüller, D., Maier, W., Fink, G. R., & Hurlemann, R. (2011) · Psychological Medicine · doi:10.1017/s0033291711000183 · Cited by 38 · see citing works
- 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
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