Influence of the stress hormone cortisol on fear conditioning in humans: evidence for sex differences in the response of the prefrontal cortex
Abstract
The stress hormone cortisol is known to influence declarative memory and associative learning. In animals, stress has often been reported to have opposing effects on memory and learning in males and females. In humans, the effects of cortisol have mainly been studied at the behavioral level. The aim of the present experiment was to characterize the effects of a single cortisol dose (30 mg) on the hemodynamic correlates of fear conditioning. In a double-blind group comparison study subjects (17 females and 17 males) received 30 mg cortisol or placebo orally before participating in a discriminative fear conditioning paradigm. Results revealed that cortisol impaired electrodermal signs of learning (the first interval response) in males, while no conditioned SCRs emerged for the females independent of treatment. fMRI results showed that cortisol reduced activity for the CS+ > CS- comparison in the anterior cingulate, the lateral orbitofrontal cortex and the medial prefrontal cortex in males. Opposite findings (increase in these regions under cortisol) were detected in females. In addition, cortisol reduced the habituation in the CS+ > CS- contrast in the dorsolateral prefrontal cortex independent of sex. Finally, cortisol also modified the response to the electric shock (the UCS) by enhancing the activity of the anterior as well as the posterior cingulate. In sum, these findings demonstrate that in humans cortisol mostly influences prefrontal brain activation during fear conditioning and that these effects appear to be modulated by sex.
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The stress response system modulates learning in several ways; HPA and autonomic profiles have been associated with individual differences in cognitive functioning, memory, and self-regulation or executive function.
“The SRS modulates learning in a number of different ways: HPA and autonomic profiles have been associated with individual differences in cognitive functioning (e.g., Staton et al., 2009), memory (e.g., Stark et al., 2006), and self-regulation/executive function (e.g., Blair et al., 2005; Shoal et al., 2003; Williams et al., 2009)”
From The Adaptive Calibration Model of stress responsivity (2011) · cites this paper as Stark et al., 2006
Cites
The assessment and analysis of handedness: The Edinburgh inventory
Oldfield, R. C. (1971) · Neuropsychologia · doi:10.1016/0028-3932(71)90067-4 · Cited by 35,900 · 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
Cognitive and emotional influences in anterior cingulate cortex
Bush, G., Luu, P., & Posner, M. I. (2000) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01483-2 · Cited by 6,259 · see citing works
Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI
Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002) · NeuroImage · doi:10.1006/nimg.2002.1087 · Cited by 3,502 · see citing works
The amygdala: vigilance and emotion
Davis, M., & Whalen, P. J. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000812 · Cited by 2,882 · see citing works
KRINGELBACH, M. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.03.006 · Cited by 1,977 · 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
Rolls, E. T. (1998) · doi:10.1093/oso/9780198524649.001.0001 · Cited by 1,314 · see citing works
Diorio, D., Viau, V, & Meaney, M. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03839.1993 · Cited by 1,151 · 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
Amat, J., Baratta, M. V., Paul, E., Bland, S. T., Watkins, L. R., & Maier, S. F. (2005) · Nature Neuroscience · doi:10.1038/nn1399 · Cited by 931 · 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
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
Enhanced memory for emotional material following stress-level cortisol treatment in humans
Buchanan, T. W., & Lovallo, W. R. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(00)00058-5 · Cited by 762 · see citing works
Critchley, H. D., Corfield, D. R., Chandler, M. P., Mathias, C. J., & Dolan, R. J. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-1-00259.x · Cited by 757 · see citing works
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.902 · Cited by 664 · see citing works
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.5.902 · Cited by 663 · see citing works
Cahill, L., Gorski, L., & Le, K. (2003) · Learning & Memory · doi:10.1101/lm.62403 · Cited by 660 · 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
LUPIEN, S. J., Gillin, C. J., & Hauger, R. L. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.3.420 · Cited by 561 · see citing works
Lupien, S. J., Gillin, C. J., & Hauger, R. L. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.3.420 · Cited by 561 · see citing works
Activation of the visual cortex in motivated attention
Bradley, M. M., Sabatinelli, D., Lang, P. J., Fitzsimmons, J. R., King, W., & Desai, P. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.2.369 · Cited by 528 · see citing works
Stress, memory, and the hippocampus: can't live with it, can't live without it
LUPIEN, S. J., & Lepage, M. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00361-8 · Cited by 515 · see citing works
Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress
Wang, J., Rao, H., Wetmore, G. S., Furlan, P. M., Korczykowski, M., Dinges, D. F., & Detre, J. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503082102 · Cited by 513 · see citing works
Stress and Plasticity in the Limbic System
Sapolsky, R. M. (2003) · Neurochemical Research · doi:10.1023/a:1026021307833 · Cited by 489 · see citing works
Drevets, W. C., Price, J. L., Bardgett, M. E., Reich, T., Todd, R. D., & Raichle, M. E. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00687-6 · Cited by 457 · see citing works
Decision-making and impulse control after frontal lobe injuries
Bechara, A., & der Linden, M. V. (2005) · Current Opinion in Neurology · doi:10.1097/01.wco.0000194141.56429.3c · Cited by 426 · see citing works
A meta-analytic review of the effects of acute cortisol administration on human memory
Het, S., Ramlow, G., & Wolf, O. T. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.005 · Cited by 414 · see citing works
Self-citationBüchel, 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
The relationship between stress induced cortisol levels and memory differs between men and women
Wolf, O. T., Schommer, N. C., Hellhammer, D. H., McEwen, B. S., & Kirschbaum, C. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00025-7 · Cited by 362 · see citing works
Self-citationPavlovian Conditioning: A Functional Perspective
Domjan, M. P. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.141409 · Cited by 359 · see citing works
De Quervain, D. J. ‐., Henke, K., Aerni, A., Treyer, V., McGaugh, J. L., Berthold, T., Nitsch, R. M., Buck, A., Roozendaal, B., & Hock, C. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02542.x · Cited by 342 · see citing works
Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses.
Strange, B., & Dolan, R. (2004) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0404282101 · Cited by 329 · see citing works
Cortisol-Induced Impairments of Working Memory Require Acute Sympathetic Activation.
Elzinga, B. M., & Karin Roelofs, A. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.98 · Cited by 287 · see citing works
Sex Differences in Chronic Stress Effects on Memory in Rats
Luine, V. (2002) · Stress · doi:10.1080/1025389021000010549 · Cited by 250 · 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
Learning During Stressful TimesPreprint
Shors, T. J. (2004) · Learning & Memory · doi:10.1101/lm.66604 · Cited by 245 · see citing works
Neural 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
Wolf, O. T. (2003) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/s1521-690x(02)00101-x · Cited by 225 · see citing works
Self-citationOrbitofrontal cortex activity related to emotional processing changes across the menstrual cycle
Protopopescu, X., Pan, H., Altemus, M. M., Tüscher, O., Polanecsky, M., McEwen, B. S., Silbersweig, D., & Stern, E. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502818102 · Cited by 221 · see citing works
Kuhlmann, S., Kirschbaum, C., & Wolf, O. T. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.09.001 · Cited by 217 · see citing works
Self-citationCortisol differentially affects memory in young and elderly men.
Wolf, O. T., Convit, A. J., McHugh, P. F., Kandil, E., Thorn, E. L., Santi, S. D., McEwen, B. S., & de Leon, M. J. (2001) · Behavioral Neuroscience · doi:10.1037//0735-7044.115.5.1002 · Cited by 213 · see citing works
Self-citationNoradrenaline mediates amygdala activation in men and women during encoding of emotional material
van Stegeren, A. H., Goekoop, R., Everaerd, W., Scheltens, P., Barkhof, F., Kuijer, J. P. A., & Rombouts, S. A. R. B. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.09.011 · Cited by 212 · see citing works
Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle
Conrad, C. D., Jackson, J. L., Wieczorek, L., Baran, S. E., Harman, J. S., Wright, R. L., & Korol, D. L. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.04.025 · Cited by 211 · see citing works
Fernández, G., Weis, S., Stoffel‐Wagner, B., Tendolkar, I., Reuber, M., Beyenburg, S., Klaver, P., Fell, J., de Greiff, A., Ruhlmann, J., et al. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-09-03790.2003 · Cited by 205 · see citing works
Memory facilitating and anti-amnesic effects of corticosteroids
Flood, J. F., Vidal, D., Bennett, E. L., Orme, A. E., Vasquez, S., & Jarvik, M. E. (1978) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(78)90127-2 · Cited by 200 · see citing works
Stress Differentially Modulates Fear Conditioning in Healthy Men and Women
Jackson, E. D., Payne, J. D., Nadel, L., & Jacobs, W. J. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.08.002 · Cited by 181 · see citing works
Cortisol Reduces Hippocampal Glucose Metabolism in Normal Elderly, but Not in Alzheimer's Disease
de Leon, M. J., McRae, T., Rusinek, H., Convit, A. J., Santi, S. D., Tarshish, C. Y., Golomb, J. B., Volkow, N. D., Daisley, K., Orentreich∥, N., et al. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.10.4305 · Cited by 176 · see citing works
Cortisol differentially affects memory in young and elderly men.
Wolf, O. T., Convit, A. J., McHugh, P. F., et al. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.5.1002 · Cited by 173 · see citing works
Self-citationGender differences in the processing of disgust- and fear-inducing pictures: an fMRI study
Schienle, A., fer, A. S., Stark, R. M., Walter, B., & Vaitl, D. (2005) · Neuroreport · doi:10.1097/00001756-200502280-00015 · Cited by 172 · see citing works
Self-citationPryce, C. R., Lehmann, J., & Feldon, J. (1999) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00147-1 · Cited by 169 · see citing works
Hui, G. K. (2003) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2003.09.002 · Cited by 168 · see citing works
The amygdala and individual differences in human fear conditioning
Furmark, T., Fischer, H., Wik, G., Larsson, M., & Fredrikson, M. (1997) · Neuroreport · doi:10.1097/00001756-199712220-00021 · Cited by 160 · 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
Three components of the classically conditioned GSR in human subjects.
Prokasy, W. F., & Ebel, H. C. (1967) · Journal of Experimental Psychology · doi:10.1037/h0024108 · Cited by 156 · see citing works
Brain activity during expectancy of emotional stimuli: an fMRI study
Ueda, K., Okamoto, Y., Okada, G., Yamashita, H., Hori, T., & Yamawaki, S. (2003) · Neuroreport · doi:10.1097/00001756-200301200-00010 · Cited by 145 · see citing works
Stress-level cortisol treatment impairs inhibitory control of behavior in monkeys
Lyons, D. M., Lopez, J. M., Yang, C., & Schatzberg, A. F. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-20-07816.2000 · Cited by 144 · see citing works
Cheng, D. T., Knight, D. C., Smith, C. N., et al. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.1.3 · Cited by 138 · see citing works
The effects of prefrontal lesions on working memory performance and theory
Curtis, C. E., & D’Esposito, M. (2004) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.4.4.528 · Cited by 125 · 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
Sex, stress, and fear: Individual differences in conditioned learning
Zorawski, M., Cook, C. A., Kuhn, C. M., & LaBar, K. S. (2005) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.5.2.191 · Cited by 108 · see citing works
Corticosterone Potentiation of Conditioned Fear in Ratsa
Corodimas, K. P., LeDoux, J. E., Gold, P. W., & Schulkin, J. A. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39264.x · Cited by 102 · see citing works
Adrenocortical hormones and avoidance behaviour of rats
Bohus, B., & Lissák, K. (1968) · International Journal of Neuropharmacology · doi:10.1016/0028-3908(68)90012-9 · Cited by 98 · see citing works
Wolf, O. T., Convit, A. J., de Leon, M. J., Caraos, C., & Qadri, S. F. (2002) · Neuroendocrinology · doi:10.1159/000054715 · Cited by 95 · see citing works
Self-citationWeike, A. I., Hamm, A. O., Schupp, H. T., Runge, U., Schroeder, H. W. S., & Kessler, C. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2032-05.2005 · Cited by 88 · see citing works
Functional MRI of human Pavlovian fear conditioning
Knight, D. C., Smith, C. N., Stein, E. A., & Helmstetter, F. J. (1999) · Neuroreport · doi:10.1097/00001756-199911260-00037 · Cited by 84 · see citing works
Croiset, G., Nijsen, M., & Kamphuis, P. J. G. H. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00556-2 · Cited by 84 · see citing works
Tabbert, K., Stark, R. M., Kirsch, P., & Vaitl, D. (2005) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.01.007 · Cited by 76 · see citing works
Self-citationZorawski, M. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4075 · Cited by 72 · see citing works
Fear conditioning and brain activity: A positron emission tomography study in humans.
Fischer, H., Andersson, J., Furmark, T., & Fredrikson, M. G. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.4.671 · Cited by 69 · see citing works
Fear conditioning and brain activity: A positron emission tomography study in humans.
Fischer, H., Andersson, J., Furmark, T., et al. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.4.671 · Cited by 57 · see citing works
Bromm, B. (2001) · Physiology · doi:10.1152/physiologyonline.2001.16.5.244 · Cited by 51 · see citing works
The involvement of the posterior cingulate gyrus in phasic pain processing of humans
Bromm, B. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.01.018 · Cited by 49 · see citing works
Glucocorticoids: effects on human cognition
LUPIEN, S. J., Maheul, F. S., & Weekes, N. Y. (2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80022-7 · Cited by 7 · see citing works
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Shin, L. M., & Liberzon, I. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.83 · Cited by 2,083 · see citing works
Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., & Schramek, T. E. (2007) · Brain and Cognition · doi:10.1016/j.bandc.2007.02.007 · Cited by 1,474 · see citing works
The Adaptive Calibration Model of stress responsivity
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.11.007 · Cited by 1,373 · see citing works
Lonsdorf, T. B., Menz, M. M., Andreatta, M., Fullana, M. A., Golkar, A., Haaker, J., Heitland, I., Hermann, A., Kuhn, M., Kruse, O., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.026 · Cited by 837 · 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
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Andreano, J. M., & Cahill, L. (2009) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.918309 · Cited by 672 · see citing works
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Mechias, M.-L., Etkin, A., & Kalisch, R. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.09.040 · Cited by 392 · see citing works
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Smeets, T., Otgaar, H., Candel, I., & Wolf, O. T. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.07.009 · Cited by 316 · see citing works
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Wolf, O. T. (2007) · Acta Psychologica · doi:10.1016/j.actpsy.2007.08.002 · Cited by 233 · see citing works
Self-citationLonsdorf, T. B., & Merz, C. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.07.007 · Cited by 236 · see citing works
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Giudice, M. D., Hinnant, J. B., Ellis, B. J., & El‐Sheikh, M. (2011) · Developmental Psychology · doi:10.1037/a0026519 · Cited by 168 · see citing works
Haaker, J., Gaburro, S., Sah, A., Gartmann, N., Lonsdorf, T. B., Meier, K., Singewald, N., Pape, H.-C., Morellini, F., & Kalisch, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303061110 · Cited by 166 · see citing works
Smeets, T., Dziobek, I., & Wolf, O. T. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.01.011 · Cited by 176 · see citing works
Self-citationNeuronal correlates of extinction learning are modulated by sex hormones
Merz, C. J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R. M., & Wolf, O. T. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr063 · Cited by 136 · see citing works
Self-citationvan 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
Self-citationSex differences in stress regulation of arousal and cognition
Bangasser, D. A., Eck, S. R., Telenson, A. M., & Salvatore, M. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.09.025 · Cited by 133 · see citing works
Henckens, M. J. A. G., van Wingen, G. A., Joëls, M., & Fernández, G. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00066 · Cited by 125 · see citing works
Sex differences in stress effects on emotional learning
Merz, C. J., & Wolf, O. T. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23811 · Cited by 122 · see citing works
Self-citationAcute effects of hydrocortisone on the human brain: An fMRI study
Lovallo, W. R., Robinson, J. L., Glahn, D. C., & Fox, P. T. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.09.010 · Cited by 121 · see citing works
Animal models in translational studies of PTSD
Daskalakis, N. P., Yehuda, R., & Diamond, D. M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.006 · Cited by 116 · 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
Self-citationDalla, C., Papachristos, E. B., Whetstone, A. S., & Shors, T. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809650106 · Cited by 111 · see citing works
Stress selectively and lastingly promotes learning of context-related high arousing information
Smeets, T., Wolf, O. T., Giesbrecht, T., Sijstermans, K., Telgen, S., & Joëls, M. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.03.001 · Cited by 104 · see citing works
Self-citationStress differentially affects fear conditioning in men and women
Merz, C. J., Wolf, O. T., Schweckendiek, J., Klucken, T., Vaitl, D., & Stark, R. M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.05.015 · Cited by 102 · see citing works
Self-citationOral contraceptive usage alters the effects of cortisol on implicit fear learning
Merz, C. J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R. M., & Wolf, O. T. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.09.001 · Cited by 101 · see citing works
Self-citationKlucken, T., Schweckendiek, J., Merz, C. J., Tabbert, K., Walter, B., Kagerer, S., Vaitl, D., & Stark, R. M. (2009) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2009.01405.x · Cited by 100 · see citing works
Self-citationThe Neurocircuitry of Fear, Stress, and Anxiety Disorders
Shin, L. M., & Liberzon, I. (2011) · FOCUS The Journal of Lifelong Learning in Psychiatry · doi:10.1176/foc.9.3.foc311 · Cited by 104 · see citing works
Stress reduces use of negative feedback in a feedback-based learning task.
Petzold, A., Plessow, F., Goschke, T., & Kirschbaum, C. (2010) · Behavioral Neuroscience · doi:10.1037/a0018930 · Cited by 97 · see citing works
Progesterone at encoding predicts subsequent emotional memoryPreprint
Ertman, N., Andreano, J. M., & Cahill, L. F. (2011) · Learning & Memory · doi:10.1101/lm.023267.111 · Cited by 94 · see citing works
Post-learning psychosocial stress enhances consolidation of neutral stimuli
Preuß, D., & Wolf, O. T. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.03.009 · Cited by 93 · see citing works
Self-citationAcute stress impairs the retrieval of extinction memory in humans
Raio, C. M., Brignoni-Perez, E., Goldman, R., & Phelps, E. A. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.015 · Cited by 90 · see citing works
Sleep and Cortisol Interact to Support Memory Consolidation
Bennion, K. A., Steinmetz, K. R. M., Kensinger, E. A., & Payne, J. D. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht255 · Cited by 88 · see citing works
Modulation of Fear Extinction by Stress, Stress Hormones and Estradiol: A Review
Stockhorst, U., & Antov, M. I. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00359 · Cited by 86 · see citing works
Fear as a translational mechanism in the psychopathology of anorexia nervosa
Murray, S. B., Strober, M., Craske, M. G., Griffiths, S., Levinson, C. A., & Strigo, I. A. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.10.013 · Cited by 75 · see citing works
Cortisol administration induces global down-regulation of the brain's reward circuitry
Montoya, E. R., Bos, P. A., Terburg, D., Rosenberger, L. A., & van Honk, J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.04.022 · Cited by 80 · see citing works
Corticosteroid Induced Decoupling of the Amygdala in Men
Henckens, M. J. A. G., van Wingen, G. A., Joëls, M., & Fernández, G. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr313 · Cited by 80 · see citing works
Dynamically changing effects of corticosteroids on human hippocampal and prefrontal processing
Henckens, M. J. A. G., Pu, Z., Hermans, E. J., van Wingen, G. A., Joëls, M., & Fernández, G. (2012) · Human Brain Mapping · doi:10.1002/hbm.21409 · Cited by 80 · see citing works
Apter-Levy, Y., Pratt, M., Vakart, A., Feldman, M., Zagoory‐Sharon, O., & Feldman, R. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.11.006 · Cited by 79 · see citing works
Sex differences in the generalization of fear as a function of retention intervalsPreprint
Lynch, J. F., Cullen, P. K., Jasnow, A. M., & Riccio, D. C. (2013) · Learning & Memory · doi:10.1101/lm.032011.113 · Cited by 77 · see citing works
Neural correlates of disgust- and fear-conditioned responses
Klucken, T., Schweckendiek, J., Koppe, G., Merz, C. J., Kagerer, S., Walter, B., Sammer, G., Vaitl, D., & Stark, R. M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.007 · Cited by 77 · see citing works
Self-citationBentz, D., Michael, T., Wilhelm, F. H., Hartmann, F., Kunz, S., von Rohr, I. R. R., & de Quervain, D. J. ‐. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.12.018 · Cited by 77 · see citing works
Goldstein, J. M., Handa, R. J., & Tobet, S. A. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.001 · Cited by 77 · see citing works
Li, C.-S. R., Chao, H. H., & Lee, T.-W. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn132 · Cited by 75 · see citing works
Associations between brain activity and endogenous and exogenous cortisol – A systematic review
Harrewijn, A., Vidal‐Ribas, P., Clore-Gronenborn, K., Jackson, S. M., Pisano, S., Pine, D. S., & Stringaris, A. K. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104775 · Cited by 66 · see citing works
Stress and memory retrieval in women: No strong impairing effect during the luteal phase.
Schoofs, D., & Wolf, O. T. (2009) · Behavioral Neuroscience · doi:10.1037/a0015625 · Cited by 68 · see citing works
Self-citationPsycho-physiological response in an automatic parachute jump
Clemente‐Suárez, V. J., Robles‐Pérez, J. J., & Fernández‐Lucas, J. (2016) · Journal of Sports Sciences · doi:10.1080/02640414.2016.1240878 · Cited by 68 · see citing works
Cortisol modifies extinction learning of recently acquired fear in men
Merz, C. J., Hermann, A., Stark, R. M., & Wolf, O. T. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst137 · Cited by 67 · see citing works
Self-citationWeckesser, L. J., Plessow, F., Pilhatsch, M., Muehlhan, M., Kirschbaum, C., & Miller, R. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.04.012 · Cited by 72 · see citing works
Let's talk about sex … differences in human fear conditioning
Merz, C. J., Jentsch, V. L., & Wolf, O. T. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.01.021 · Cited by 65 · see citing works
Self-citationDismukes, A. R., Johnson, M. M., Vitacco, M. J., Iturri, F., & Shirtcliff, E. A. (2014) · Developmental Psychobiology · doi:10.1002/dev.21231 · Cited by 63 · see citing works
Social modulation of decision-making: a cross-species review
van den Bos, R., Jolles, J. W., & Homberg, J. R. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00301 · Cited by 64 · see citing works
Goldstein, J. M., Holsen, L. M., Handa, R. J., & Tobet, S. A. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00247 · Cited by 63 · see citing works
Sex Differences in the Central Nervous System
(2016) · Elsevier eBooks · doi:10.1016/c2014-0-01274-9 · Cited by 61 · see citing works
Jentsch, V. L., Merz, C. J., & Wolf, O. T. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.049 · Cited by 59 · see citing works
Self-citationContingency learning in human fear conditioning involves the ventral striatum
Klucken, T., Tabbert, K., Schweckendiek, J., Merz, C. J., Kagerer, S., Vaitl, D., & Stark, R. M. (2009) · Human Brain Mapping · doi:10.1002/hbm.20791 · Cited by 60 · see citing works
Self-citationKlucken, T., Alexander, N., Schweckendiek, J., Merz, C. J., Kagerer, S., Osinsky, R., Walter, B., Vaitl, D., Hennig, J., & Stark, R. M. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss005 · Cited by 56 · see citing works
Self-citationBiggs, E. E., Timmers, I., Meulders, A., Vlaeyen, J. W. S., Goebel, R., & Kaas, A. L. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.016 · Cited by 56 · see citing works
Genetic, epigenetic and environmental impact on sex differences in social behavior
Shepard, K. N., Michopoulos, V., Toufexis, D. J., & Wilson, M. E. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.016 · Cited by 57 · see citing works
Graham, L. K., Yoon, T., Lee, H. J., & Kim, J. J. (2009) · Psychology & Neuroscience · doi:10.3922/j.psns.2009.2.015 · Cited by 55 · see citing works
Antov, M. I., & Stockhorst, U. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.06.022 · Cited by 55 · see citing works
Metyrapone Administration Reduces the Strength of an Emotional Memory Trace in a Long-Lasting Manner
Marin, M., Hupbach, A., Maheu, F. S., Nader, K., & LUPIEN, S. J. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0226 · Cited by 55 · see citing works
How stress and glucocorticoids timing-dependently affect extinction and relapse
Drexler, S. M., Merz, C. J., Jentsch, V. L., & Wolf, O. T. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.12.029 · Cited by 56 · see citing works
Self-citationDifferential chronic social stress models in male and female mice
Furman, O., Tsoory, M., & Chen, A. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15481 · Cited by 57 · see citing works
Cortisol alters reward processing in the human brain
Jentsch, V. L., Wolf, O. T., & Merz, C. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.05.005 · Cited by 52 · see citing works
Self-citationOlsson, A., Kopsida, E., Sorjonen, K., & Savic, I. (2016) · Emotion · doi:10.1037/a0039765 · Cited by 49 · see citing works
Frontolimbic function and cortisol reactivity in response to emotional stimuli
Root, J. C., Tüscher, O., Cunningham‐Bussel, A., Pan, H., Epstein, J., Altemus, M. M., Cloître, M., Goldstein, M., Silverman, M. E., Furman, D. J., et al. (2009) · Neuroreport · doi:10.1097/wnr.0b013e328326a031 · Cited by 51 · see citing works
Sheikh, H. I., Joanisse, M. F., Mackrell, S. V. M., Kryski, K. R., Smith, H. J., Singh, S. M., & Hayden, E. P. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.08.013 · Cited by 47 · see citing works
Koot, S., Baars, A., Hesseling, P., van den Bos, R., & Joëls, M. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.02.008 · Cited by 46 · see citing works
Exposure to stress attenuates fear retrieval in healthy men
Merz, C. J., Hamacher‐Dang, T. C., & Wolf, O. T. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.12.009 · Cited by 47 · see citing works
Self-citationHormonal contraceptive usage influences stress hormone effects on cognition and emotion
Jentsch, V. L., Pötzl, L., Wolf, O. T., & Merz, C. J. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101012 · Cited by 46 · see citing works
Self-citationTabbert, K., Merz, C. J., Klucken, T., Schweckendiek, J., Vaitl, D., Wolf, O. T., & Stark, R. M. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.08.006 · Cited by 44 · see citing works
Self-citationMaking Sense of Stress: An Evolutionary—Developmental Framework
Giudice, M. D., Ellis, B. J., & Shirtcliff, E. A. (2012) · Springer eBooks · doi:10.1007/978-1-4614-5605-6_2 · Cited by 44 · see citing works
Battaglia, S., Fazio, C. D., Mazzà, M., Tamietto, M., & Avenanti, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25020864 · Cited by 45 · see citing works
Cortisol, stress, and attentional bias toward threat
McHugh, R. K., Behar, E., Gutner, C. A., Geem, D., & Otto, M. W. (2010) · Anxiety Stress & Coping · doi:10.1080/10615801003596969 · Cited by 43 · 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
Self-citationGarcía-Contreras, C., Vázquez-Gómez, M., Barbero-Fernández, A., Pacheco, J. L. P., Zinellu, A., Berlinguer, F., Gonzalez-Añover, P., Gonzalez, J., Encinas, T., Torres-Rovira, L., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20051187 · Cited by 41 · see citing works
Grillon, C., Heller, R., Hirschhorn, E., Kling, M. A., Pine, D. S., Schulkin, J. A., & Vythilingam, M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.12.013 · Cited by 41 · see citing works
Regulation of excitatory synapses and fearful memories by stress hormones
Krugers, H. J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00062 · Cited by 40 · see citing works
Contribution of stress and sex hormones to memory encoding
Merz, C. J. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.05.002 · Cited by 39 · see citing works
Endocrine Regulations in Human–Dog Coexistence through Domestication
Kikusui, T., Nagasawa, M., Nomoto, K., Kuse-Arata, S., & Mogi, K. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.09.002 · Cited by 39 · see citing works
Peyrot, C., Brouillard, A., Morand‐Beaulieu, S., & Marin, M. (2020) · Behaviour Research and Therapy · doi:10.1016/j.brat.2020.103615 · Cited by 38 · see citing works
Glucocorticoids, metabolism and brain activity
Jaszczyk, A., & Juszczak, G. R. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.007 · Cited by 41 · see citing works
Biological embedding of perinatal social relationships in infant stress reactivity
Thomas, J. C., Letourneau, N., Bryce, C. I., Campbell, T. S., Giesbrecht, G. F., & The APrON Study Team (2017) · Developmental Psychobiology · doi:10.1002/dev.21505 · Cited by 38 · see citing works
Contextual control over expression of fear is affected by cortisol
van Ast, V. A., Vervliet, B., & Kindt, M. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00067 · Cited by 38 · see citing works
Stress impairs acquisition of delay eyeblink conditioning in men and women
Wolf, O. T., Minnebusch, D. A., & Daum, I. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.11.002 · Cited by 38 · see citing works
Self-citation
- Authors
- Stark, R., Wolf, O. T., Tabbert, K., Kagerer, S., Zimmermann, M., Kirsch, P., Schienle, A., & Vaitl, D.
- Affiliations
- Justus-Liebig-Universität Gießen (DE)
- Bielefeld University (DE)
- Corresponding author
- Stark, Rudolf
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2006-09
- Volume
- 32
- Issue
- 3
- Pages
- 1290-1298
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W1971752570
- Cited by
- 167
- References
- 70
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 3 · 2019: 6 · 2018: 7 · 2017: 7 · 2016: 13 · 2015: 7 · 2014: 14 · 2013: 17 · 2012: 13
- FWCI
- 4.83
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- cortisol, fear conditioning, sex differences, prefrontal cortex, stress hormones, electrodermal activity, anterior cingulate cortex, orbitofrontal cortex, dorsolateral prefrontal cortex, habituation, learning and memory
- MeSH terms
- Adult, Conditioning, Psychological, Double-Blind Method, Fear, Female, Galvanic Skin Response, Hemodynamics, Humans, Hydrocortisone, Magnetic Resonance Imaging, Male, Photic Stimulation, Sex Characteristics, Prefrontal Cortex
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