Stress-induced out-of-context activation of memory

. 2010 Dec 21 ; 8 (12) : e1000570. [epub] 20101221

Jazyk angličtina Země Spojené státy americké Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid21203585

Inappropriate recollections and responses in stressful conditions are hallmarks of post-traumatic stress disorder and other anxiety and mood disorders, but how stress contributes to the disorders is unclear. Here we show that stress itself reactivates memories even if the memory is unrelated to the stressful experience. Forced-swim stress one day after learning enhanced memory recall. One-day post-learning amnestic treatments were ineffective unless administered soon after the swim, indicating that a stressful experience itself can reactivate unrelated consolidated memories. The swim also triggered inter-hemispheric transfer of a lateralized memory, confirming stress reactivates stable memories. These novel effects of stress on memory required the hippocampus although the memories themselves did not, indicating hippocampus-dependent modulation of extra-hippocampal memories. These findings that a stressful experience itself can activate memory suggest the novel hypothesis that traumatic stress reactivates pre-trauma memories, linking them to memory for the trauma and pathological facilitation of post-traumatic recall.

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Korte S. M, Koolhaas J. M, Wingfield J. C, McEwen B. S. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav Rev. 2005;29:3–38. PubMed

McEwen B. S. The neurobiology of stress: from serendipity to clinical relevance. Brain Res. 2000;886:172–189. PubMed

Rubin D. C, Berntsen D, Bohni M. K. A memory-based model of posttraumatic stress disorder: evaluating basic assumptions underlying the PTSD diagnosis. Psychol Rev. 2008;115:985–1011. PubMed PMC

Roozendaal B. 1999 Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology. 2000;25:213–238. PubMed

Misanin J. R, Miller R. R, Lewis D. J. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science. 1968;160:554–555. PubMed

Przybyslawski J, Roullet P, Sara S. J. Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors. J Neurosci. 1999;19:6623–6628. PubMed PMC

Izquierdo I, Quillfeldt J. A, Zanatta M. S, Quevedo J, Schaeffer E, et al. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur J Neurosci. 1997;9:786–793. PubMed

Alvarez P, Squire L. R. Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci U S A. 1994;91:7041–7045. PubMed PMC

Lewis D. J. Psychobiology of active and inactive memory. Psychol Bull. 1979;86:1054–1083. PubMed

Nader K, Schafe G. E, LeDoux J. E. The labile nature of consolidation theory. Nat Rev Neurosci. 2000;1:216–219. PubMed

Porsolt R. D, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature. 1977;266:730–732. PubMed

Korz V, Frey J. U. Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J Neurosci. 2005;25:7393–7400. PubMed PMC

Bures J. Reversible decortication and behavior. In: Brazier M. A. B, editor. The central nervous system and behavior. New York: Josiah Macy, Jr Foundation; 1959. pp. 207–248.

Nadel L, Buresova O. Monocular input and interhemispheric transfer in the reversible split-brain. Nature. 1968;220:914–915. PubMed

Fenton A. A, Bures J. Place navigation in rats with unilateral tetrodotoxin inactivation of the dorsal hippocampus: place but not procedural learning can be lateralized to one hippocampus. Behav Neurosci. 1993;107:552–564. PubMed

Fenton A. A, Bures J. Interhippocampal transfer of place navigation monocularly acquired by rats during unilateral functional ablation of the dorsal hippocampus and visual cortex with lidocaine. Neuroscience. 1994;58:481–491. PubMed

Russell I. S, Ochs S. One-trial interhemispheric transfer of a learning engram. Science. 1961;133:1077–1078. PubMed

Goldowitz D, Buresova O, Bures J. Time labelling of independently acquired lateralized engrams in rats. Physiol Behav. 1972;9:699–704. PubMed

Leão A. A. P. Spreading depression of activity in the cerebral cortex. Journal of Neurophysiology. 1944;7:359–390. PubMed

Klein S. B. Adrenal-pituitary influence in reactivation of avoidance-learning memory in the rat after intermediate intervals. J Comp Physiol Psychol. 1972;79:341–359. PubMed

Vargha-Khadem F, Gadian D. G, Watkins K. E, Connelly A, Van Paesschen W, et al. Differential effects of early hippocampal pathology on episodic and semantic memory. Science. 1997;277:376–380. PubMed

Tulving E. Episodic memory: from mind to brain. Annu Rev Psychol. 2002;53:1–25. PubMed

Squire L. R, Stark C. E, Clark R. E. The medial temporal lobe. Annu Rev Neurosci. 2004;27:279–306. PubMed

Olypher A. V, Klement D, Fenton A. A. Cognitive disorganization in hippocampus: a physiological model of the disorganization in psychosis. J Neurosci. 2006;26:158–168. PubMed PMC

Fenton A. A, Arolfo M. P, Nerad L, Bures J. Interhippocampal synthesis of lateralized place navigation engrams. Hippocampus. 1995;5:16–24. PubMed

Roozendaal B, McEwen B. S, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci. 2009;10:423–433. PubMed

Joels M, Pu Z, Wiegert O, Oitzl M. S, Krugers H. J. Learning under stress: how does it work? Trends Cogn Sci. 2006;10:152–158. PubMed

Roozendaal B, Hahn E. L, Nathan S. V, de Quervain D. J, McGaugh J. L. Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. J Neurosci. 2004;24:8161–8169. PubMed PMC

Ardenghi P, Barros D, Izquierdo L. A, Bevilaqua L, Schroder N, et al. Late and prolonged post-training memory modulation in entorhinal and parietal cortex by drugs acting on the cAMP/protein kinase A signalling pathway. Behav Pharmacol. 1997;8:745–751. PubMed

Blaisdell A. P, Sawa K, Leising K. J, Waldmann M. R. Causal reasoning in rats. Science. 2006;311:1020–1022. PubMed

Hardt O, Wang S. H, Nader K. Storage or retrieval deficit: the yin and yang of amnesia. Learn Mem. 2009;16:224–230. PubMed

Nader K, Schafe G. E, Le Doux J. E. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 2000;406:722–726. PubMed

Duvarci S, Nader K. Characterization of fear memory reconsolidation. J Neurosci. 2004;24:9269–9275. PubMed PMC

Nader K. Memory traces unbound. Trends Neurosci. 2003;26:65–72. PubMed

Alberini C. M. Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? Trends Neurosci. 2005;28:51–56. PubMed

Nader K, Hardt O. A single standard for memory: the case for reconsolidation. Nat Rev Neurosci. 2009;10:224–234. PubMed

Debiec J, Ledoux J. E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience. 2004;129:267–272. PubMed

Taubenfeld S. M, Milekic M. H, Monti B, Alberini C. M. The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci. 2001;4:813–818. PubMed

Debiec J, Doyere V, Nader K, Ledoux J. E. Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. Proc Natl Acad Sci U S A. 2006;103:3428–3433. PubMed PMC

Suzuki A, Josselyn S. A, Frankland P. W, Masushige S, Silva A. J, et al. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci. 2004;24:4787–4795. PubMed PMC

Serrano P, Friedman E. L, Kenney J, Taubenfeld S. M, Zimmerman J. M, et al. PKMzeta maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol. 2008;6:2698–2706. doi: 10.1371/journal.pbio.0060318. PubMed DOI PMC

Power A. E, Berlau D. J, McGaugh J. L, Steward O. Anisomycin infused into the hippocampus fails to block “reconsolidation” but impairs extinction: the role of re-exposure duration. Learn Mem. 2006;13:27–34. PubMed PMC

Kubik S, Fenton A. A. Behavioral evidence that segregation and representation are dissociable hippocampal functions. J Neurosci. 2005;25:9205–9212. PubMed PMC

Wesierska M, Dockery C, Fenton A. A. Beyond memory, navigation, and inhibition: behavioral evidence for hippocampus-dependent cognitive coordination in the rat. J Neurosci. 2005;25:2413–2419. PubMed PMC

Kubik S, Stuchlik A, Fenton A. A. Evidence for hippocampal role in place avoidance other than merely memory storage. Physiol Res. 2006;55:445–452. PubMed

Nadel L, Moscovitch M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol. 1997;7:217–227. PubMed

Fortin N. J, Wright S. P, Eichenbaum H. Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature. 2004;431:188–191. PubMed PMC

Wais P. E, Squire L. R, Wixted J. T. In search of recollection and familiarity signals in the hippocampus. J Cogn Neurosci. 2010;22:109–123. PubMed PMC

Hoffman K. L, McNaughton B. L. Coordinated reactivation of distributed memory traces in primate neocortex. Science. 2002;297:2070–2073. PubMed

Skaggs W. E, McNaughton B. L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271:1870–1873. PubMed

Louie K, Wilson M. A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001;29:145–156. PubMed

Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I. Internally generated reactivation of single neurons in human hippocampus during free recall. Science. 2008;322:96–101. PubMed PMC

Doyere V, Debiec J, Monfils M. H, Schafe G. E, LeDoux J. E. Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat Neurosci. 2007;10:414–416. PubMed

Moncada D, Viola H. PKMzeta inactivation induces spatial familiarity. Learn Mem. 2008;15:810–814. PubMed

Kemp A, Manahan-Vaughan D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci U S A. 2004;101:8192–8197. PubMed PMC

Kemp A, Manahan-Vaughan D. Hippocampal long-term depression: master or minion in declarative memory processes? Trends Neurosci. 2007;30:111–118. PubMed

Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton A. A, et al. Storage of spatial information by the maintenance mechanism of LTP. Science. 2006;313:1141–1144. PubMed

Suarez L. D, Smal L, Delorenzi A. Updating contextual information during consolidation as result of a new memory trace. Neurobiol Learn Mem. 2010;93:561–571. PubMed

Tronel S, Milekic M. H, Alberini C. M. Linking new information to a reactivated memory requires consolidation and not reconsolidation mechanisms. PLoS Biol. 2005;3:e293. doi: 10.1371/journal.pbio.0030293. PubMed DOI PMC

Klement D, Past'alkova E, Fenton A. A. Tetrodotoxin infusions into the dorsal hippocampus block non-locomotor place recognition. Hippocampus. 2005;15:460–471. PubMed

Buresova O. The influence of spreading cortical depression on unconditioned and conditioned alimentary reflexes. Physiol Bohemoslov. 1956;5:350–358. PubMed

Brooks M. C, Peck M. E. Effect of various cortical lesions on development of placing and hopping reactions in rats. Journal of Neurophysiology. 1940;3:66–73.

Izquierdo I, McGaugh J. L. Effect of a novel experience prior to training or testing on retention of an inhibitory avoidance response in mice: involvement of an opioid system. Behav Neural Biol. 1985;44:228–238. PubMed

Netto C. A, Oliveira C. B, Gianlupi A, Quillfeldt J. Effect of atropine and propranolol on retrieval enhancement by a novel experience or by injection of beta-endorphin prior to testing in rats. Braz J Med Biol Res. 1990;23:59–63. PubMed

McDonald R. J, White N. M. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci. 1993. 1993;107:3–22. PubMed

Paxinos G, Watson M. San Diego: Academic Press; 2007. The rat brain in stereotaxic coordinates.

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