Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism
Open accessAbstract
It is well established that acute administration of adrenocortical hormones enhances the consolidation of memories of emotional experiences and, concurrently, impairs working memory. These different glucocorticoid effects on these two memory functions have generally been considered to be independently regulated processes. Here we report that a glucocorticoid receptor agonist administered into the medial prefrontal cortex (mPFC) of male Sprague-Dawley rats both enhances memory consolidation and impairs working memory. Both memory effects are mediated by activation of a membrane-bound steroid receptor and depend on noradrenergic activity within the mPFC to increase levels of cAMP-dependent protein kinase. These findings provide direct evidence that glucocorticoid effects on both memory consolidation and working memory share a common neural influence within the mPFC.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Glucocorticoids have been shown to accentuate the effects of catecholamines in both the PFC and the amygdala, thus coordinating and exaggerating the switch from thoughtful to habitual responding during exposure to stress.
“Glucocorticoids have been shown to accentuate the effects of catecholamines in both the PFC and the amygdala69, thus coordinating and exaggerating the switch from thoughtful to habitual responding during exposure to stress (Fig. 1).”
From Stress weakens prefrontal networks: molecular insults to higher cognition (2015) · cites this paper as [69]
A highly responsive stress response system facilitates social learning, enhances mental activities in localized domains, focuses attention, and primes memory storage, improving cognitive processes for dealing with environmental opportunities and threats.
“a highly responsive system facilitates social learning, enhances mental activities in localized domains, focuses attention, and primes memory storage, thus improving cognitive processes for dealing with environmental opportunities and threats (Barsegyan et al., 2010; Flinn, 2006; Roozendaal, 2000; van Marle et al., 2009)”
From The Adaptive Calibration Model of stress responsivity (2011) · cites this paper as Barsegyan et al., 2010
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Stress signalling pathways that impair prefrontal cortex structure and function
Arnsten, A. F. T. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2648 · Cited by 3,299 · see citing works
THE AMYGDALA MODULATES THE CONSOLIDATION OF MEMORIES OF EMOTIONALLY AROUSING EXPERIENCES
McGaugh, J. L. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144157 · Cited by 2,296 · see citing works
Self-citationStress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
Self-citationStress and glucocorticoids impair retrieval of long-term spatial memory
de Quervain, D. J.-F., Roozendaal, B., & McGaugh, J. L. (1998) · Nature · doi:10.1038/29542 · Cited by 1,182 · see citing works
Self-citationAnxiety and affective style: role of prefrontal cortex and amygdala
Davidson, R. J. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01328-2 · Cited by 1,139 · 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
Karst, H., Berger, S., Turiault, M., Tronche, F., Schütz, G., & Joëls, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507572102 · Cited by 774 · 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
Schafe, G. E., & LeDoux, J. E. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-18-j0003.2000 · Cited by 611 · see citing works
The prefrontal cortex as a key target of the maladaptive response to stress
Cerqueira, J. J., Mailliet, F., Almeida, O. F. X., Jay, T. M., & Sousa, N. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4372-06.2007 · Cited by 599 · see citing works
Memory consolidation and the amygdala: a systems perspective
McGaugh, J. L. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02211-7 · Cited by 572 · see citing works
Self-citationLUPIEN, 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
Prefrontal regions involved in keeping information in and out of mind
Bunge, S. A. (2001) · Brain · doi:10.1093/brain/124.10.2074 · Cited by 528 · see citing works
A corticosteroid receptor in neuronal membranes
Orchinik, M., Murray, T. F., & Moore, F. L. (1991) · Science · doi:10.1126/science.2063198 · Cited by 523 · see citing works
Bernabeu, R., Bevilaqua, L. R., Ardenghi, P. G., Bromberg, E., Schmitz, P. K., Bianchin, M. M., Izquierdo, I., & Medina, J. H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.7041 · Cited by 499 · 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
Self-citationPsychosocial stress induces working memory impairments in an n-back paradigm.
Schoofs, D., Preuß, D., & Wolf, O. T. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.02.004 · Cited by 483 · see citing works
Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory
Yuen, E. Y., Liu, W., Karatsoreos, I. N., Feng, J., McEwen, B. S., & Yan, Z. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906791106 · Cited by 481 · see citing works
Sandi, C., Loscertales, M., & Guaza, C. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01412.x · Cited by 447 · see citing works
Rosenkranz, J. A., & Grace, A. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00324.2002 · Cited by 392 · 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
Self-citationPrefrontal Control of the Amygdala
Likhtik, E., Pelletier, J. G., Paz, R., & Paré, D. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2314-05.2005 · Cited by 361 · see citing works
The amygdala modulates prefrontal cortex activity relative to conditioned fear
Garcia, R., Vouimba, R.-M., Baudry, M., & Thompson, R. F. (1999) · Nature · doi:10.1038/46286 · Cited by 347 · see citing works
Roozendaal, B., McReynolds, J. R., & McGaugh, J. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4664-03.2004 · Cited by 327 · see citing works
Self-citationFunctional role of the prefrontal cortex in retrieval of memories: a PET study
Kapur, S., Craik, F. I. M., Jones, C., Brown, G. M., Houle, S., & Tulving, E. (1995) · Neuroreport · doi:10.1097/00001756-199510020-00014 · Cited by 295 · see citing works
Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory
Oitzl, M. S., Reichardt, H. M., Joëls, M., & de Kloet, E. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.231313998 · Cited by 286 · see citing works
Mueller, D., Porter, J. T., & Quirk, G. J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3248-07.2008 · Cited by 284 · see citing works
Glucocorticoid Release and Memory Consolidation in Men and Women
Andreano, J. M., & Cahill, L. (2006) · Psychological Science · doi:10.1111/j.1467-9280.2006.01729.x · Cited by 270 · 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
Self-citationA Role for Prefrontal Cortex in Memory Storage for Trace Fear Conditioning
Runyan, J. D., Moore, A. N., & Dash, P. K. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4880-03.2004 · Cited by 224 · see citing works
Dysregulation of Protein Kinase A Signaling in the Aged Prefrontal Cortex
Ramos, B. P., Birnbaum, S. G., Lindenmayer, I., Newton, S. S., Duman, R. S., & Arnsten, A. F. T. (2003) · Neuron · doi:10.1016/s0896-6273(03)00694-9 · Cited by 218 · see citing works
Haller, J., Mikics, É., & Makara, G. B. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.10.004 · Cited by 201 · see citing works
Ca2+-Stimulated Adenylyl Cyclases Regulate ERK-Dependent Activation of MSK1 during Fear Conditioning
Sindreu, C. B., Scheiner, Z. S., & Storm, D. R. (2007) · Neuron · doi:10.1016/j.neuron.2006.11.024 · Cited by 192 · see citing works
Roozendaal, B., McReynolds, J. R., van der Zee, E. A., Lee, S., McGaugh, J. D., & McIntyre, C. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3626-09.2009 · Cited by 182 · see citing works
Self-citationChapter 10 The prefrontal cortex and its relation to behavior
Fuster, J. M. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63053-8 · Cited by 180 · 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
Li, B. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00070-6 · Cited by 162 · 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
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-citationThe beta-1 adrenergic antagonist, betaxolol, improves working memory performance in rats and monkeys
Ramos, B. P., Colgan, L., Nou, E., Ovadia, S., Wilson, S. R., & Arnsten, A. F. T. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.05.022 · Cited by 147 · see citing works
Pérez-Jaranay, J. M., & Vives, F. (1991) · Brain Research · doi:10.1016/0006-8993(91)91357-7 · Cited by 122 · see citing works
Taylor, J. R., Birnbaum, S., Ubriani, R., & Arnsten, A. F. T. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-18-j0001.1999 · Cited by 120 · cited 2× · see citing works
“Because previous evidence indicates that an activation of PKA within the mPFC impairs working memory (17), whereas increased cAMP/PKA activity within the BLA and hippocampus seems necessary for A”
BackgroundEndocannabinoids: The silent partner of glucocorticoids in the synapse
Hill, M. N., & McEwen, B. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901519106 · Cited by 98 · see citing works
17α-Alkynyl-11β,17-dihydroxyandrostane derivatives : A new class of potent glucocorticoids.
Teutsch, G., COSTEROUSSE, G., Deraedt, R., Benzoni, J., Fortin, M., & Philibert, D. (1981) · Steroids · doi:10.1016/0039-128x(81)90084-2 · Cited by 94 · see citing works
Zheng, J., Ali, A. N. M., & RAMIREZ, V. D. (1996) · PubMed · Cited by 84 · see citing works
Zorawski, M. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4075 · Cited by 72 · see citing works
Slowing the progression of cognitive decline in alzheimer’s disease using mifepristone
Belanoff, J., Jurik, J., Schatzberg, L. D., DeBattista, C., & Schatzberg, A. (2002) · Journal of Molecular Neuroscience · doi:10.1007/s12031-002-0033-3 · Cited by 66 · see citing works
Micheau, J., Destrade, C., & Soumireu-Mourat, B. (1984) · European Journal of Pharmacology · doi:10.1016/0014-2999(84)90675-7 · Cited by 53 · see citing works
Izquierdo, L. A., Barros, D. M., da Costa, J. C., Furini, C. R. G., Zinn, C. G., Cammarota, M., Bevilaqua, L. R., & Izquierdo, I. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.04.014 · Cited by 52 · see citing works
Rasmussen, H. B., Rasmussen, T. N., Triller, A., & Vannier, C. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2001.1074 · Cited by 40 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course
McEwen, B. S., & Morrison, J. H. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.028 · Cited by 1,079 · see citing works
Dynamic adaptation of large-scale brain networks in response to acute stressors
Hermans, E. J., Henckens, M. J. A. G., Joëls, M., & Fernández, G. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.03.006 · Cited by 936 · see citing works
Stress weakens prefrontal networks: molecular insults to higher cognition
Arnsten, A. F. T. (2015) · Nature Neuroscience · doi:10.1038/nn.4087 · Cited by 752 · see citing works
Stress effects on memory: An update and integration
Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.002 · Cited by 714 · see citing works
Self-citationCatecholamine Influences on Dorsolateral Prefrontal Cortical Networks
Arnsten, A. F. T. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.01.027 · Cited by 493 · see citing works
Learning and memory under stress: implications for the classroom
Vogel, S., & Schwabe, L. (2016) · npj Science of Learning · doi:10.1038/npjscilearn.2016.11 · Cited by 515 · see citing works
Stress, glucocorticoids and memory: implications for treating fear-related disorders
de Quervain, D., Schwabe, L., & Roozendaal, B. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.155 · Cited by 484 · see citing works
Self-citationHigh Cortisol and the Risk of Dementia and Alzheimer’s Disease: A Review of the Literature
Ouanes, S., & Popp, J. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00043 · Cited by 481 · see citing works
Roozendaal, B., & McGaugh, J. L. (2011) · Behavioral Neuroscience · doi:10.1037/a0026187 · Cited by 445 · see citing works
Self-citationCrucian, B. E., Choukèr, A., Simpson, R. J., Mehta, S., Marshall, G., Smith, S. M., Zwart, S. R., Heer, M., Ponomarev, S., Whitmire, A., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01437 · Cited by 421 · see citing works
Arnsten, A. F. T., Raskind, M. A., Taylor, F. B., & Connor, D. F. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.002 · Cited by 381 · see citing works
Stress and emotional memory: a matter of timing
Joëls, M., Fernández, G., & Roozendaal, B. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.04.004 · Cited by 372 · see citing works
Self-citationStress and multiple memory systems: from ‘thinking’ to ‘doing’
Schwabe, L., & Wolf, O. T. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.12.001 · Cited by 355 · see citing works
Myers, B., McKlveen, J. M., & Herman, J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.003 · Cited by 318 · see citing works
Finsterwald, C., & Alberini, C. M. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.017 · Cited by 311 · see citing works
Groeneweg, F. L., Karst, H., de Kloet, E. R., & Joëls, M. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.06.020 · Cited by 289 · see citing works
McKlveen, J. M., Myers, B., & Herman, J. P. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12272 · Cited by 273 · see citing works
McGaugh, J. L. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-014954 · Cited by 271 · see citing works
Self-citationAdolescent Suicide as a Failure of Acute Stress-Response Systems.
Miller, A. B., & Prinstein, M. J. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095625 · Cited by 235 · see citing works
“Glucocorticoids (cortisol in humans) are the end point of the HPA axis system and are responsible for many of the adaptive acute stress responses, such as enhanced memory (Barsegyan et al. 2010) and regulation of inflammatory immune signaling (Slavich & Irwin 2014).”
BackgroundPlessow, F., Fischer, R., Kirschbaum, C., & Goschke, T. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00024 · Cited by 236 · see citing works
Acute stress and episodic memory retrieval: neurobiological mechanisms and behavioral consequences
Gagnon, S. A., & Wagner, A. D. (2016) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12996 · Cited by 233 · see citing works
Cognitive Adaptation under Stress: A Case for the Mineralocorticoid Receptor
Vogel, S., Fernández, G., Joëls, M., & Schwabe, L. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.12.003 · Cited by 204 · see citing works
Mechanisms of memory under stress
Schwabe, L., Hermans, E. J., Joëls, M., & Roozendaal, B. (2022) · Neuron · doi:10.1016/j.neuron.2022.02.020 · Cited by 188 · see citing works
Self-citationButts, K. A., Weinberg, J., Young, A. H., & Phillips, A. G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111746108 · Cited by 182 · see citing works
Prefrontal cortex executive processes affected by stress in health and disease
Girotti, M., Adler, S. M., Bulin, S. E., Fucich, E. A., Paredes, D., & Morilak, D. A. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.07.004 · Cited by 176 · see citing works
The Cognition-Enhancing Effects of Psychostimulants Involve Direct Action in the Prefrontal Cortex
Spencer, R. C., Devilbiss, D. M., & Berridge, C. W. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.09.013 · Cited by 164 · see citing works
Schwabe, L., Tegenthoff, M., Höffken, O., & Wolf, O. T. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.001 · Cited by 162 · see citing works
Glucocorticoids act on glutamatergic pathways to affect memory processes
Sandi, C. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.01.006 · Cited by 162 · see citing works
Chronic Stress Weakens Connectivity in the Prefrontal Cortex: Architectural and Molecular Changes.
Woo, E., Sansing, L. H., Arnsten, A. F. T., & Datta, D. (2021) · Chronic Stress · doi:10.1177/24705470211029254 · Cited by 159 · 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
Self-citationGutièrrez‐Mecinas, M., Trollope, A. F., Collins, A., Morfett, H., Hesketh, S. A., Kersanté, F., & Reul, J. M. H. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104383108 · Cited by 153 · see citing works
Dynamic Shifts in Large-Scale Brain Network Balance As a Function of Arousal
Young, C. B., Raz, G., Everaerd, D., Beckmann, C. F., Tendolkar, I., Hendler, T., Fernández, G., & Hermans, E. J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1759-16.2016 · Cited by 147 · see citing works
Bogdanov, M., & Schwabe, L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3687-15.2016 · Cited by 135 · 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
Andrade, C., & Rao, N. K. (2010) · Indian Journal of Psychiatry · doi:10.4103/0019-5545.74318 · Cited by 120 · see citing works
Action control is mediated by prefrontal BDNF and glucocorticoid receptor binding
Gourley, S. L., Swanson, A. M., Jacobs, A. M., Howell, J. L., Mo, M., Dileone, R., Koleske, A. J., & Taylor, J. R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208342109 · Cited by 118 · see citing works
Memory under stress: from single systems to network changes
Schwabe, L. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13478 · Cited by 114 · see citing works
Stress-induced enhancement of response inhibition depends on mineralocorticoid receptor activation
Schwabe, L., Höffken, O., Tegenthoff, M., & Wolf, O. T. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.05.001 · Cited by 107 · see citing works
HPA Axis Interactions with Behavioral Systems
Packard, A. E. B., Egan, A. E., & Ulrich‐Lai, Y. M. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150042 · Cited by 130 · see citing works
Atsak, P., Roozendaal, B., & Campolongo, P. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.047 · Cited by 98 · see citing works
Self-citationSchwabe, L., Höffken, O., Tegenthoff, M., & Wolf, O. T. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3304-11.2011 · Cited by 97 · see citing works
A behavioral neuroenergetics theory of ADHD
Killeen, P. R., Russell, V. A., & Sergeant, J. A. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.011 · Cited by 97 · see citing works
Corticotropin-Releasing Factor (CRF) circuit modulation of cognition and motivation
Hupalo, S., Bryce, C. A., Bangasser, D. A., Berridge, C. W., Valentino, R. J., & Floresco, S. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.010 · Cited by 90 · see citing works
Is AD a Stress-Related Disorder? Focus on the HPA Axis and Its Promising Therapeutic Targets
Canet, G., Hernandez, C., Zussy, C., Chevallier, N., Desrumaux, C. M., & Givalois, L. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00269 · Cited by 89 · see citing works
Hall, B. S., Moda, R. N., & Liston, C. M. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.008 · Cited by 90 · see citing works
Flak, J. N., Solomon, M. B., Jankord, R., Krause, E. G., & Herman, J. P. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08161.x · Cited by 87 · see citing works
Atsak, P., Hauer, D., Campolongo, P., Schelling, G., Fornari, R. V., & Roozendaal, B. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.334 · Cited by 85 · see citing works
Self-citationStress, working memory, and academic performance: a neuroscience perspective
Almarzouki, A. F. (2024) · Stress · doi:10.1080/10253890.2024.2364333 · Cited by 102 · see citing works
Localization of Mineralocorticoid Receptors at Mammalian Synapses
Prager, E. M., Brielmaier, J., Bergstrom, H. C., McGuire, J., & Johnson, L. R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014344 · Cited by 81 · see citing works
Glucocorticoid-induced enhancement of extinction—from animal models to clinical trials
de Quervain, D. J. ‐., Wolf, O. T., & Roozendaal, B. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5116-0 · Cited by 79 · see citing works
Self-citationDatta, D., & Arnsten, A. (2019) · Brain Sciences · doi:10.3390/brainsci9050113 · Cited by 78 · see citing works
Krugers, H. J., Karst, H., & Joëls, M. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00015 · Cited by 77 · see citing works
Blundell, J. J., Blaiss, C. A., Lagace, D. C., Eisch, A. J., & Powell, C. M. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.02.006 · Cited by 76 · see citing works
Zorzo, C., Méndez-López, M., Méndez, M., & Arias, J. L. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.011 · Cited by 75 · see citing works
Long-Term Continuous Corticosterone Treatment Decreases VEGF Receptor-2 Expression in Frontal Cortex
Howell, K. R., Kutiyanawalla, A., & Pillai, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020198 · Cited by 75 · see citing works
Bahtiyar, S., Karaca, K. G., Henckens, M. J. A. G., & Roozendaal, B. (2020) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2020.103537 · Cited by 75 · see citing works
Self-citationRussell, G., Kalafatakis, K., & Lightman, S. (2015) · Journal of neuroendocrinology · doi:10.1111/jne.12247 · Cited by 64 · see citing works
Bingham, B. C., Rani, C. S. S., Frazer, A., Strong, R., & Morilak, D. A. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.07.003 · Cited by 65 · see citing works
Neural mechanisms and computations underlying stress effects on learning and memory
Lukšys, G., & Sandi, C. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.03.003 · Cited by 64 · see citing works
Dismukes, 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
Glucocorticoid Receptors are Localized to Dendritic Spines and Influence Local Actin Signaling
Jafari, M., Seese, R. R., Babayan, A. H., Gall, C. M., & Lauterborn, J. C. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8288-3 · Cited by 61 · see citing works
Edelmann, M. N., Ogg, R. J., Scoggins, M., Brinkman, T. M., Sabin, N. D., Pui, C., Srivastava, D. K., Robison, L. L., Hudson, M. M., & Krull, K. R. (2013) · Pediatric Blood & Cancer · doi:10.1002/pbc.24644 · Cited by 59 · see citing works
Dorey, R., Piérard, C., Shinkaruk, S., Tronche, C., Chauveau, F., Baudonnat, M., & Béracochéa, D. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.152 · Cited by 59 · see citing works
Garrido, P., de Blas, M., Ronzoni, G., Cordero, I., Antón, M., Giné, E., Santos, Á., Arco, A. D., Segovia, G., & Mora, F. (2012) · Journal of Neural Transmission · doi:10.1007/s00702-012-0935-3 · Cited by 58 · see citing works
Compton, R. J., Hofheimer, J., & Kazinka, R. (2012) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-012-0126-6 · Cited by 59 · see citing works
Dong, J., Wang, Y., Cui, M., Wang, X.-J., Zheng, W.-S., Ma, M., Yang, F., He, D., Hu, Q.-X., Zhang, D., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.09.025 · Cited by 55 · see citing works
Anderson, R. M., Birnie, A. K., Koblesky, N. K., Romig‐Martin, S. A., & Radley, J. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1385-14.2014 · Cited by 51 · see citing works
Impact of Stress and Glucocorticoids on Schema-Based Learning
Kluen, L. M., Nixon, P., Agorastos, A., Wiedemann, K., & Schwabe, L. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.256 · Cited by 51 · see citing works
Barsegyan, A., Mirone, G., Ronzoni, G., Guo, C., Song, Q., van Kuppeveld, D., Schut, E. H. S., Atsak, P., Teurlings, S. M. W., McGaugh, J. L., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901513116 · Cited by 51 · see citing works
Self-citationThe effect of hydrocortisone administration on intertemporal choice
Riis-Vestergaard, M. I., van Ast, V. A., Cornelisse, S., Joëls, M., & Haushofer, J. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.10.002 · Cited by 50 · see citing works
Hauer, D., Kaufmann, I., Strewe, C., Briegel, I., Campolongo, P., & Schelling, G. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.10.003 · Cited by 49 · see citing works
Hippocampal spine changes across the sleep–wake cycle: corticosterone and kinases
Ikeda, M., Hojo, Y., Komatsuzaki, Y., Okamoto, M., Kato, A., Takeda, T., & Kawato, S. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0078 · Cited by 49 · see citing works
Hupalo, S., & Berridge, C. W. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.85 · Cited by 48 · see citing works
Cyrino, L. A. R., de Lima, D. D., Ullmann, O. M., & Maia, T. P. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.609487 · Cited by 48 · see citing works
Hood, A., Pulvers, K. M., Spady, T. J., Kliebenstein, A., & Bachand, J. (2014) · Anxiety Stress & Coping · doi:10.1080/10615806.2014.1000880 · Cited by 47 · see citing works
Aged rats are hypo-responsive to acute restraint: implications for psychosocial stress in aging
Buechel, H. M., Popović, J., Staggs, K. E., Anderson, K. L., Thibault, O., & Blalock, E. M. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00013 · Cited by 45 · see citing works
Vandesquille, M., Baudonnat, M., Decorte, L., Louis, C., Lestage, P. J., & Béracochéa, D. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.10.006 · Cited by 46 · see citing works
Kesler, S. R., Ogg, R. J., Reddick, W. E., Phillips, N. S., Scoggins, M., Glass, J. O., Cheung, Y. T., Pui, C., Robison, L. L., Hudson, M. M., et al. (2018) · Brain Connectivity · doi:10.1089/brain.2017.0574 · Cited by 47 · see citing works
Baicalein improves cognitive deficits and hippocampus impairments in temporal lobe epilepsy rats
Qian, X., Wang, Z.-R., Zheng, J.-J., Ding, J., Zhong, J.-G., Zhang, T., Li, W. S., & Zhang, M. (2019) · Brain Research · doi:10.1016/j.brainres.2019.02.028 · Cited by 46 · see citing works
Effect of Experience and Psychophysiological Modification by Combat Stress in Soldier’s Memory
Delgado-Moreno, R., Robles‐Pérez, J. J., Aznar, S., & Clemente‐Suárez, V. J. (2019) · Journal of Medical Systems · doi:10.1007/s10916-019-1261-1 · Cited by 46 · see citing works
Circadian regulation of hippocampal function is disrupted with corticosteroid treatment
Birnie, M. T., Claydon, M. D. B., Troy, O. R., Flynn, B. P., Yoshimura, M., Kershaw, Y. M., Zhao, Z., Demski-Allen, R. C. R., Barker, G. R. I., Warburton, E. C., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2211996120 · Cited by 45 · see citing works
Butts, K. A., & Phillips, A. G. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713000187 · Cited by 45 · see citing works
Murakami, G., Hojo, Y., Kato, A., Komatsuzaki, Y., Horie, S., Soma, M., Kim, J., & Kawato, S. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12561 · Cited by 45 · see citing works
Enhancing memory with stress: Progress, challenges, and opportunities
Goldfarb, E. V. (2018) · Brain and Cognition · doi:10.1016/j.bandc.2018.11.009 · Cited by 46 · see citing works
Making 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
Wichmann, R., Fornari, R. V., & Roozendaal, B. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.06.004 · Cited by 42 · see citing works
Self-citationTang, S. W., Helmeste, D. M., & Leonard, B. E. (2011) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.639800 · Cited by 42 · see citing works
Nongenomic glucocorticoid effects and their mechanisms of action in vertebrates
Johnstone, W. M., Mankiewicz, J. L., Deck, C. A., & Borski, R. J. (2019) · International review of cytology · doi:10.1016/bs.ircmb.2019.03.004 · Cited by 42 · see citing works
d-serine prevents cognitive deficits induced by acute stress
Guercio, G. D., Bevictori, L. E., Vargas-Lopes, C., Madeira, C., Oliveira, A. F., Carvalho, V. F., d’Avila, J. C., & Panizzutti, R. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.06.021 · Cited by 41 · see citing works
Stress affects the neural ensemble for integrating new information and prior knowledge
Vogel, S., Kluen, L. M., Fernández, G., & Schwabe, L. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.02.038 · Cited by 41 · see citing works
Dominguez, G., Henkous, N., Prévot, T. D., David, V., Guillou, J., Belzung, C., Mons, N. E., & Béracochéa, D. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100161 · 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
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
Acute stress selectively impairs learning to act
de Berker, A. O., Tirole, M., Rutledge, R. B., Cross, G. F., Dolan, R. J., & Bestmann, S. (2016) · Scientific Reports · doi:10.1038/srep29816 · Cited by 40 · see citing works
The impact of acute stress on cognitive functioning: a matter of cognitive demands?
Plieger, T., Felten, A., Diks, E., Tepel, J., Mies, M., & Reuter, M. (2016) · Cognitive Neuropsychiatry · doi:10.1080/13546805.2016.1261014 · Cited by 38 · see citing works
Phosphorylation of the AMPA receptor GluA1 subunit regulates memory load capacity
Olivito, L., Saccone, P., Perri, V., Bachman, J. L., Fragapane, P., Mele, A., Huganir, R. L., & Leonibus, E. D. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0927-1 · Cited by 36 · see citing works
New Perspectives in the Model of Stress Response
Tonhajzerová, I., & Mestanik, M. (2017) · Physiological Research · doi:10.33549/physiolres.933674 · Cited by 39 · see citing works
Arnsten, A. F. T., Woo, E., Yang, S., Wang, M., & Datta, D. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.02.003 · Cited by 35 · see citing works
Green, M. R., & McCormick, C. M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.08.011 · Cited by 36 · see citing works
- Authors
- Barsegyan, A., Mackenzie, S. M., Kurose, B. D., McGaugh, J. L., & Roozendaal, B.
- Affiliations
- University Medical Center Groningen (NL)
- University of California, Irvine (US)
- ORCID
- Roozendaal, Benno
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-09
- Volume
- 107
- Issue
- 38
- Pages
- 16655-16660
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2944727
- OpenAlex
- W2085425790
- Cited by
- 262
- References
- 52
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 9 · 2023: 17 · 2022: 13 · 2021: 14 · 2020: 11 · 2019: 24 · 2018: 17 · 2017: 13 · 2016: 27 · 2015: 15 · 2014: 22 · 2013: 26 · 2012: 14
- FWCI
- 13.36
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH012526, MH12526, R56MH012526)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- glucocorticoids, memory consolidation, working memory, medial prefrontal cortex, glucocorticoid receptor, noradrenergic activity, protein kinase A, emotional memory, adrenal cortex hormones
- MeSH terms
- Amygdala, Androstanols, Animals, Corticosterone, Glucocorticoids, Male, Memory, Memory, Short-Term, Models, Neurological, Receptors, Adrenergic, beta, Receptors, Glucocorticoid, Signal Transduction, Rats, Sprague-Dawley, Prefrontal Cortex, Cyclic AMP-Dependent Protein Kinases, Rats
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
