Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man

Neurobiology of Learning and Memory

Volumn 90, Issue 3, 2008, Pages 495-503

  Schwabe, Lars ^a,b   Dalm, Sergiu ^b   Schächinger, Hartmut ^a   Oitzl, Melly S ^b  

^a UNIVERSITY OF TRIER   (Germany)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Chronic stress; Multiple memory systems; Spatial learning; Stimulus response learning

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; EMOTION; FEMALE; HUMAN; LEARNING; MALE; MEMORY; MOTIVATION; MOUSE; NONHUMAN; QUESTIONNAIRE; SPATIAL ORIENTATION; STIMULUS RESPONSE; TASK PERFORMANCE;

ADAPTATION, PSYCHOLOGICAL; ADULT; ANALYSIS OF VARIANCE; ANIMALS; ASSOCIATION LEARNING; CAUDATE NUCLEUS; CHI-SQUARE DISTRIBUTION; CHRONIC DISEASE; DISCRIMINATION LEARNING; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, INBRED C57BL; RATS; REACTION TIME; REFERENCE VALUES; RETENTION (PSYCHOLOGY); SELF ASSESSMENT (PSYCHOLOGY); SPATIAL BEHAVIOR; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 51349111149     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2008.07.015     Document Type: Article

References (46)

1. Armony J.L., Corbo V., Clement M.H., and Brunet A. Amygdala response in patients with acute PTSD to masked and unmasked emotional facial expressions. American Journal of Psychiatry 162 (2005) 1961-1963
2. Blackburn-Munro G., and Blackburn-Munro R.E. Chronic pain, chronic stress and depression: Coincidence or consequence?. Journal of Neuroendocrinology 13 (2001) 1009-1023
3. Bodnoff S.R., Humphreys A.G., Lehman J.C., Diamond D.M., Rose G.M., and Meaney M.J. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuroatrophy in young and mid-aged rats. The Journal of Neuroscience 15 (1995) 61-69
4. Brinks V., De Kloet E.R., and Oitzl M.S. Emotion and cognition in high and low stress sensitive mouse strains: A combined neuroendocrine and behavioral study in BALB/c and C57BL/6j mice. Frontiers in Behavioural Neuroscience 1 (2007) doi: 10.3389/neuro.3308/3008.2007
5. Conrad C.D. What is the functional significance of chronic stress-induced CA3 dendritic retraction within the hippocampus?. Behavioral and Cognitive Neuroscience Reviews 5 (2006) 41-60
6. Conrad C.D., Magarinos A.M., LeDoux J.E., and McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behavioral Neuroscience 113 (1999) 902-913
7. De Quervain D.J., Roozendaal B., and McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394 (1998) 787-790
8. Dickerson S.S., and Kemeny M.E. Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin 130 (2004) 355-391
9. Düzel E., Habib R., Rotte M., Guderian S., Tulving E., and Heinze H.J. Human hippocampal and parahippocampal activity during visual associative recognition memory for spatial and nonspatial stimulus-configurations. The Journal of Neuroscience 23 (2003) 9439-9444
10. Eichenbaum H. Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 44 (2004) 109-120
11. Fuchs E., Flugge G., and Czeh B. Remodeling of neural networks by stress. Frontiers in Biosciences 11 (2006) 2746-2758
12. Gabrieli J.D. Cognitive neuroscience of human memory. Annual Review in Psychology 49 (1998) 87-115
13. Gronli J., Murison R., Fiske E., Bjorvatn B., Sorensen E., Portas C.M., et al. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiology & Behavior 84 (2005) 571-577
14. Grootendorst J., de Kloet E.R., Dalm S., and Oitzl M.S. Reversal of cognitive deficit of apolipoprotein E knockout mice after repeated exposure to a common environmental experience. Neuroscience 108 (2001) 137-247
15. Grootendorst J., de Kloet E.R., Vossen C., Dalm S., and Oitzl M.S. Repeated exposure to rats has persistent genotype-dependent effects on learning and locomotor activity of apolipoprotein E knockout and C57BL/6 mice. Behavioral Brain Research 125 (2001) 249-259
16. Harvey P.O., Le Bastard G., Pochon J.B., Levy R., Allilaire J.F., Dubois B., et al. Executive functions and updating of the contents of working memory in unipolar depression. Journal of Psychiatric Research 38 (2004) 567-576
17. Iaria G., Petrides M., Dagher A., Pike B., and Bohbot V. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. Journal of Neuroscience 23 (2003) 5945-5952
18. Jog M.S., Kubota Y., Connolly C.I., Hillegaart V., and Graybiel A.M. Building neural representations of habits. Science 286 (1999) 1745-1749
19. Kim J., Lee H., Han J., and Packard M. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. Journal of Neuroscience 21 (2001) 5222-5228
20. Kleen J.K., Sitomer M.T., Killeen P.R., and Conrad C.D. Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behavioral Neuroscience 120 (2006) 842-851
21. Knowlton B.J., Mangels J.A., and Squire L.R. A neostriatal habit learning system in humans. Science 273 (1996) 1399-1402
22. Konkle A.T., Baker S.L., Kentner A.C., Barbagallo L.S., Merali Z., and Bielajew C. Evaluation of the effects of chronic mild stressors on hedonic and physiological responses: Sex and strain compared. Brain Research 992 (2003) 227-238
23. Linthorst A.C., Flachskamm C., Barden N., Holsboer F., and Reul J.M. Glucocorticoid receptor impairment alters CNS responses to a psychological stressor: An in vivo microdialysis study in transgenic mice. European Journal of Neuroscience 12 (2000) 283-291
24. Luine V. Sex differences in chronic stress effects on memory in rats. Stress 5 (2002) 205-216
25. McEwen B.S. Stress and hippocampal plasticity. Annual Reviews of Neuroscience 22 (1999) 105-122
26. McKittrick C.R., Magarinos A.M., Blanchard D.C., Blanchard R.J., McEwen B.S., and Sakai R.R. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36 (2000) 85-94
27. Meaney M.J., Szyf M., and Seckl J.R. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Molecular Medicine 13 (2007) 269-277
28. Mitra R., Jadhav S., McEwen B.S., Vyas A., and Chattarji S. Stress duration modulates spatiotemporal patterns of spine formation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 102 (2005) 9371-9376
29. Mizumori S.J.Y., Yeshenko O., Gill K.M., and Davis D.M. Parallel processing across neural systems: Implications for a multiple memory system hypothesis. Neurobiology of Learning and Memory 82 (2004) 278-298
30. Packard M., and McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially effects expression of place and response learning. Neurobiology of Learning and Memory 65 (1996) 65-72
31. Packard M., and Wingard J.C. Amygdala and "emotional" modulation of the relative use of multiple memory systems. Neurobiology of Learning and Memory 82 (2004) 243-252
32. Poldrack R.A., and Packard M. Competition among multiple memory systems: Converging evidence from animal and human brain studies. Neuropsychologia 41 (2003) 245-251
33. Purcell R., Maruff P., Kyrios M., and Pantelis C. Neuropsychological function in young patients with unipolar major depression. Psychological Medicine 27 (1997) 1277-1285
34. Roozendaal B. Stress and memory: Opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory 78 (2002) 578-595
35. Schulz P., and Schlotz P. Trierer Inventar zur Erfassung von chronischem Stress (TICS): Skalenkonstruktion teststatistische Uberprufung und Validierung der Skala Arbeitsüberlastung. Diagnostica 45 (1999) 8-19
36. Schulz P., Schlotz W., and Becker P. Das Trierer Inventar zum Chronischen Stress (2004), Hogrefe Verlag, Göttingen
37. Schwabe L., Oitzl M., Philippsen C., Richter S., Bohringer A., Wippich W., et al. Stress modulates the use of spatial and stimulus-response learning strategies in humans. Learning and Memory 14 (2007) 109-116
38. Scoville W.B., and Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry 20 (1957) 11-12
39. Squire L.R. Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory 82 (2004) 171-177
40. Tejani-Butt S.M., Pare W.P., and Yang J. Effect of repeated novel stressors on depressive behavior and brain norepinephrine receptor system in Sprague-Dawley and Wistar Kyoto (WKY) rats. Brain Research 649 (1994) 27-35
41. Voermans N.C., Petersson K.M., Daudey L., Weber B., van Spaendonck K.P., Kremer H.P.H., et al. Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 43 (2004) 427-435
42. Vyas A., Mitra R., Rao B.S., and Chattarji S. Chronic stress induces contrasting patterns of dendritic remodelling in hippocampal and amygdaloid neurons. Journal of Neuroscience 22 (2002) 6810-6818
43. Willner P. Validity, reliability and utility of the chronic mild stress model of depression: A 10-year review and evaluation. Psychopharmacology 134 (1997) 314-329
44. Winocur G., Moscovitch M., Fogel S., Rosenbaum R.S., and Sekeres M. Preserved spatial memory after hippocampal lesions: Effects of extensive experience in a complex environment. Nature Neuroscience 8 (2005) 273-275
45. Wood G.E., Norris E.H., Waters E., Stoldt J.T., and McEwen B.S. Chronic immobilization stress alters aspects of emotionality and associative learning in the rat. Behavioral Neuroscience 122 (2008) 282-292
46. Wright R.L., and Conrad C.D. Chronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 8 (2005) 151-154