Please cite this article in press as: Schwabe, L., et al., Stress effects on memory: An update and integration. Neurosci. Biobehav. Rev. (2011), doi:10.1016/j.neubiorev.2011.07.002 ARTICLE IN PRESS G Model NBR-1487; No. of Pages 10 Neuroscience and Biobehavioral Reviews xxx (2011) xxx–xxx Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews jou rnal h omepa ge: www.elsevier.com/locate/neubiorev Review Stress effects on memory: An update and integration Lars Schwabe a,∗ , Marian Joëls b , Benno Roozendaal c , Oliver T. Wolf a , Melly S. Oitzl d a Department of Cognitive Psychology, Ruhr-University Bochum, Universitaetsstrasse 150, 44780 Bochum, Germany b Department of Neuroscience and Pharmacology, Division of Neuroscience, UMC Utrecht, Rudolf Magnus Institute, Universiteitsweg 100, 3584 CG Utrecht, The Netherlands c Department of Neuroscience, Section Anatomy, University Medical Center Groningen, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands d Division of Medical Pharmacology, Leiden/Amsterdam Center for Drug Research and Leiden University Medical Center, University of Leiden, Einsteinweg 55, 2333 CC Leiden, The Netherlands a r t i c l e i n f o Article history: Received 2 May 2011 Received in revised form 30 June 2011 Accepted 3 July 2011 Keywords: Stress Glucocorticoids Noradrenaline Memory Encoding Consolidation Retrieval Multiple memory systems a b s t r a c t It is well known that stressful experiences may affect learning and memory processes. Less clear is the exact nature of these stress effects on memory: both enhancing and impairing effects have been reported. These opposite effects may be explained if the different time courses of stress hormone, in particular catecholamine and glucocorticoid, actions are taken into account. Integrating two popular models, we argue here that rapid catecholamine and non-genomic glucocorticoid actions interact in the basolat- eral amygdala to shift the organism into a ‘memory formation mode’ that facilitates the consolidation of stressful experiences into long-term memory. The undisturbed consolidation of these experiences is then promoted by genomic glucocorticoid actions that induce a ‘memory storage mode’, which sup- presses competing cognitive processes and thus reduces interference by unrelated material. Highlighting some current trends in the field, we further argue that stress affects learning and memory processes beyond the basolateral amygdala and hippocampus and that stress may pre-program subsequent memory performance when it is experienced during critical periods of brain development. © 2011 Elsevier Ltd. All rights reserved. Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 2. Stress effects on memory: timing matters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 3. Explaining stress effects on memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 3.1. The ‘vertical’ perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 3.2. The ‘horizontal’ perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 3.3. An integrative model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 4. Stress effects on memory: current trends . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 4.1. Stress effects on striatum-dependent learning and memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 4.2. Stress and the quality of memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 4.3. Effects of early life and prenatal stress on memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 5. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 1. Introduction Everyone is familiar with stress. We experience it in varying forms and degrees every day. When we are exposed to potential threats (stressors), our brain initiates a course of action that releases numerous transmitters, peptides, and hormones throughout our body (Joëls and Baram, 2009), all of which is directed at coping with ∗ Corresponding author. Tel.: +49 234 3229324; fax: +49 234 3214308. E-mail address: Lars.Schwabe@rub.de (L. Schwabe). the stressful situation and bringing our organism back into balance (i.e., homeostasis). In particular, two systems are mobilized under stress: (i) the fast acting sympathetic nervous system and (ii) the slow hypothalamus-pituitary-adrenal (HPA) axis. Sympathetic ner- vous system responses include the release of the catecholamines adrenaline and noradrenaline from the adrenal medulla, which cause, for example, increases in heart rate or enhanced blood flow to skeletal muscles and thus prepare the organism for a ‘fight-or- flight’ response. Activation of the HPA-axis leads, via intermediate steps, to the release of glucocorticoids (mainly cortisol in humans, corticosterone in rodents) from the adrenal cortex. Glucocorticoids 0149-7634/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2011.07.002