Caudate nucleus-dependent response strategies in a virtual navigation task are associated with lower basal cortisol and impaired episodic memory

Neurobiology of Learning and Memory

Volumn 96, Issue 2, 2011, Pages 173-180

  Bohbot, Véronique D ^a   Gupta, Melini ^a   Banner, Harrison ^a   Dahmani, Louisa ^a  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

Cortisol; Navigational strategies; Spatial memory; Stress; Virtual radial maze

Indexed keywords

HYDROCORTISONE;

ADULT; ARTICLE; BRAIN REGION; CAUDATE NUCLEUS; CIRCADIAN RHYTHM; CONTROLLED STUDY; EPISODIC MEMORY; FEMALE; HIPPOCAMPUS; HORMONE RESPONSE; HUMAN; HUMAN EXPERIMENT; LEARNING TEST; MALE; MAZE TEST; MENTAL TASK; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; QUESTIONNAIRE; RATING SCALE; SALIVA LEVEL; SPATIAL MEMORY; STIMULUS RESPONSE; TASK PERFORMANCE; VIRTUAL NAVIGATION TASK;

CAUDATE NUCLEUS; FEMALE; HUMANS; HYDROCORTISONE; MALE; MAZE LEARNING; MEMORY, EPISODIC; NEUROPSYCHOLOGICAL TESTS; QUESTIONNAIRES; SALIVA; SPACE PERCEPTION; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 79960840665     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2011.04.007     Document Type: Article

References (70)

1. Abercrombie H., Kalin N., Thurow M., Rosenkranz M., Davidson R. Cortisol variation in humans affects memory for emotionally laden and neutral information. Behavioral Neuroscience 2003, 117(3):505-516.
2. Alvarez P., Zola-Morgan S., Squire L.R. Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. Journal of Neuroscience 1995, 15(5 Pt 2):3796-3807.
3. Barnes C.A., Nadel L., Honig W.K. Spatial memory deficit in senescent rats. Canadian Journal of Psychology 1980, 34(1):29-39.
4. Bennett M.C., Diamond D.M., Fleshner M., Rose G.M. Serum corticosterone level predicts the magnitude of hippocampal primed burst potentiation and depression in urethane-anesthetized rats. Psychobiology 1991, 19:301-307.
5. Bohbot V.D., Iaria G., Petrides M. Hippocampal function and spatial memory: Evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 2004, 18(3):418-425.
6. Bohbot V.D., Kalina M., Stepankova K., Spackova N., Petrides M., Nadel L. Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 1998, 36(11):1217-1238.
7. Bohbot V.D., Lerch J., Thorndycraft B., Iaria G., Zijdenbos A. Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. Journal of Neuroscience 2007, 27:10078-10083.
8. Bremner J.D., Vythilingam M., Vermetten E., Adil J., Khan S., Nazeer A., et al. Cortisol response to a cognitive stress challenge in posttraumatic stress disorder (PTSD) related to childhood abuse. Psychoneuroendocrinology 2003, 28(6):733-750.
9. Cohen S., Kamarck T., Mermelstein R. A global measure of perceived stress. Journal of Health and Social Behavior 1983, 24(4):385-396.
10. Conrad C., Galea L., Kuroda Y., McEwen B. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behavioral Neuroscience 1996, 110(6):1321-1334.
11. de Kloet E.R. Brain corticosteroid receptor balance and homeostatic control. Frontiers in Neuroendocrinology 1991, 12:95-164.
12. de Kloet E., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nature Reviews Neuroscience 2005, 6(6):463-475.
13. de Kloet E., Oitzl M., Joëls M. Stress and cognition: Are corticosteroids good or bad guys?. Trends in Neurosciences 1999, 22(10):422-426.
14. Diamond D., Bennett M., Fleshner M., Rose G. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 1992, 2(4):421-430.
15. Dubrovsky B., Liquornik M., Noble P., Gijsbers K. Effects of 5 alpha-dihydrocorticosterone on evoked responses and long-term potentiation. Brain Research Bulletin 1987, 19(6):635-638.
16. Edwards S., Evans P., Hucklebridge F., Clow A. Association between time of awakening and diurnal cortisol secretory activity. Psychoneuroendocrinology 2001, 26(6):613-622.
17. Etchamendy N., Bohbot V.D. Spontaneous navigational strategies and performance in the virtual town. Hippocampus 2007, 17(8):595-599.
18. Ferguson D., Sapolsky R. Mineralocorticoid receptor overexpression differentially modulates specific phases of spatial and nonspatial memory. Journal of Neuroscience 2007, 27(30):8046-8052.
19. Filipini D., Gijsbers K., Birmingham M., Dubrovsky B. Effects of adrenal steroids and their reduced metabolites on hippocampal long-term potentiation. Journal of Steroid Biochemistry and Molecular Biology 1991, 40(1-3):87-92.
20. Gilbertson M.W., Shenton M.E., Ciszewski A., Kasai K., Lasko N.B., Orr S.P., et al. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nature Neuroscience 2002, 5(11):1242-1247.
21. Hartley T., Maguire E.A., Spiers H.J., Burgess N. The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37(5):877-888.
22. Hassan A., Patchev V., von Rosenstiel P., Holsboer F., Almeida O. Plasticity of hippocampal corticosteroid receptors during aging in the rat. FASEB Journal 1999, 13(1):115-122.
23. Head D., Isom M. Age effects on wayfinding and route learning skills. Behavioural Brain Research 2010, 209(1):49-58.
24. Herbert J., Goodyer I., Grossman A., Hastings M., de Kloet E., Lightman S., et al. Do corticosteroids damage the brain?. Journal of Neuroendocrinology 2006, 18(6):393-411.
25. Iaria G., Petrides M., Dagher A., Pike B., Bohbot V.D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. Journal of Neuroscience 2003, 23(13):5945-5952.
26. Joels M. Steroid hormones and excitability in the mammalian brain. Frontiers in Neuroendocrinology 1997, 18(1):2-48.
27. Kim J., Lee H., Welday A., Song E., Cho J., Sharp P., et al. Stress-induced alterations in hippocampal plasticity, place cells, and spatial memory. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(46):18297-18302.
28. Kleen J., Sitomer M., Killeen P., Conrad C. Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behavioral Neuroscience 2006, 120(4):842-851.
29. Lerch J.P., Yiu A.P., Martinez-Canabal A., Pekar T., Bohbot V.D., Frankland P.W., et al. Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning. Neuroimage 2011, 54(3):2086-2095.
30. Lezak M.D. Neuropsychological assessment 1995, Oxford University Press, New York. 3rd ed.
31. López J., Chalmers D., Little K., Watson S. A.E. Bennett Research Award. Regulation of serotonin1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biological Psychiatry 1998, 43(8):547-573.
32. Lupien S.J., Buss C., Schramek T.E., Maheu F., Pruessner J. Hormetic influence of glucocorticoids on human memory. Nonlinearity in Biology, Toxicology and Medicine 2005, 3(1):23-56.
33. Lupien S.J., McEwen B.S. The acute effects of corticosteroids on cognition: Integration of animal and human model studies. Brain Research. Brain Research Reviews 1997, 24(1):1-27.
34. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S., Frith C.D., O'Keefe J. Knowing where and getting there: A human navigation network. Science 1998, 280(5365):921-924.
35. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S., et al. Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(8):4398-4403.
36. Maheu F., Joober R., Beaulieu S., Lupien S. Differential effects of adrenergic and corticosteroid hormonal systems on human short- and long-term declarative memory for emotionally arousing material. Behavioral Neuroscience 2004, 118(2):420-428.
37. Marshall R.D., Blanco C., Printz D., Liebowitz M.R., Klein D.F., Coplan J. A pilot study of noradrenergic and HPA axis functioning in PTSD vs. panic disorder. Psychiatry Research 2002, 110(3):219-230.
38. McDonald R.J., White N.M. A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience 1993, 107(1):3-22.
39. McDonald R.J., White N.M. Parallel information processing in the water maze: Evidence for independent memory systems involving dorsal striatum and hippocampus. Behavioral and Neural Biology 1994, 61(3):260-270.
40. McEwen B., Sapolsky R. Stress and cognitive function. Current Opinion in Neurobiology 1995, 5(2):205-216.
41. McKittrick C., Magariños A., Blanchard D., Blanchard R., McEwen B., Sakai R. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 2000, 36(2):85-94.
42. Milner B. The medial temporal-lobe amnesic syndrome. Psychiatric Clinics of North America 2005, 28(3):599-611.
43. Mizumori S., Yeshenko O., Gill K., Davis D. Parallel processing across neural systems: Implications for a multiple memory system hypothesis. Neurobiology of Learning and Memory 2004, 82(3):278-298.
44. Nadel L., Hardt O. The spatial brain. Neuropsychology 2004, 18(3):473-476.
45. Newcomer J., Selke G., Melson A., Hershey T., Craft S., Richards K., et al. Decreased memory performance in healthy humans induced by stress-level cortisol treatment. Archives of General Psychiatry 1999, 56(6):527-533.
46. Nicolle M., Prescott S., Bizon J. Emergence of a cue strategy preference on the water maze task in aged C57B6 × SJL F1 hybrid mice. Learn Memory 2003, 10(6):520-524.
47. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Clarendon, Oxford.
48. Olton D.S., Samuelson R.J. Remembrance of places passed: Spatial memory in rats. Journal of Experimental Psychology: Animal Behavior Processes 1976, 2:97-116.
49. Oquendo M.A., Echavarria G., Galfalvy H.C., Grunebaum M.F., Burke A., Barrera A., et al. Lower cortisol levels in depressed patients with comorbid post-traumatic stress disorder. Neuropsychopharmacology 2003, 28(3):591-598.
50. Packard M.G., Hirsh R., White N.M. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. Journal of Neuroscience 1989, 9(5):1465-1472.
51. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65(1):65-72.
52. Pavlides C., Watanabe Y., McEwen B. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 1993, 3(2):183-192.
53. Pruessner J.C., Dedovic K., Pruessner M., Lord C., Buss C., Collins L., et al. Stress regulation in the central nervous system: Evidence from structural and functional neuroimaging studies in human populations - 2008 Curt Richter Award Winner. Psychoneuroendocrinology 2010, 35(1):179-191.
54. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology 1985, 117(6):2505-2511.
55. Roozendaal B., McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiology of Learning and Memory 1997, 67(2):176-179.
56. Sapolsky R. The physiological relevance of glucocorticoid endangerment of the hippocampus. Annals New York Academy of Sciences 1994, 746:294-304. (discussion 304-297).
57. Sapolsky R., Uno H., Rebert C., Finch C. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. Journal of Neuroscience 1990, 10(9):2897-2902.
58. Schwabe L., Dalm S., Schachinger H., Oitzl M.S. Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiology of Learning and Memory 2008, 90:495-503.
59. Schwabe L., Oitzl M.S., Philippsen C., Richter S., Bohringer A., Wippich W., et al. Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learn Memory 2007, 14(1):109-116.
60. Schwabe L., Oitzl M.S., Richter S., Schachinger H. Modulation of spatial and stimulus-response learning strategies by exogenous cortisol in healthy young women. Psychoneuroendocrinology 2009, 34(3):358-366.
61. Schwabe L., Schachinger H., de Kloet E.R., Oitzl M.S. Corticosteroids operate as a switch between memory systems. Journal of Cognitive Neuroscience 2010, 22(7):1362-1372.
62. Schwabe L., Wolf O.T., Oitzl M.S. Memory formation under stress: Quantity and quality. Neuroscience and Biobehavioral Reviews 2010, 34(4):584-591.
63. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry 1957, 20:11-21.
64. Sloviter R.S., Valiquette G., Abrams G.M., Ronk E.C., Sollas A.L., Paul L.A., et al. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 1989, 243(4890):535-538.
65. Squire L.R., Zola-Morgan S. The medial temporal lobe memory system. Science 1991, 253(5026):1380-1386.
66. Tulving E. Episodic and semantic memory. Organization of memory 1972, 381-403. Academic Press, New York. E. Tulving, W. Donaldson (Eds.).
67. 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 2004, 43(3):427-435.
68. Wright R., Conrad C. Chronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 2005, 8(2):151-154.
69. Yehuda R., Teicher M.H., Trestman R.L., Levengood R.A., Siever L.J. Cortisol regulation in posttraumatic stress disorder and major depression: A chronobiological analysis. Biological Psychiatry 1996, 40(2):79-88.
70. Zachary, R. A. (1991). Shipley institute of living scale. Los Angeles.