Forebrain glucocorticoid receptor overexpression increases environmental reactivity and produces a stress-induced spatial discrimination deficit

Neuroscience

Volumn 169, Issue 2, 2010, Pages 645-653

  Hebda Bauer, E K ^a   Pletsch, A ^a   Darwish, H ^b   Fentress, H ^c   Simmons, T A ^a   Wei, Q ^a   Watson, S J ^a   Akil, H ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Object interaction; Restraint stress; Spatial and object novelty; Transgenic mice

Indexed keywords

GLUCOCORTICOID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; COPING BEHAVIOR; EMOTIONALITY; ENVIRONMENTAL STRESS; FOREBRAIN; GENE OVEREXPRESSION; HABITUATION; IMMOBILIZATION STRESS; LOCOMOTION; MALE; MOUSE; NONHUMAN; OBJECT RELATION; PRIORITY JOURNAL; PROTEIN FUNCTION; SPATIAL DISCRIMINATION; WILD TYPE;

ANIMALS; DISCRIMINATION (PSYCHOLOGY); ENVIRONMENT; EXPLORATORY BEHAVIOR; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; PROSENCEPHALON; RECEPTORS, GLUCOCORTICOID; RESTRAINT, PHYSICAL; SPACE PERCEPTION; STRESS, PSYCHOLOGICAL;

EID: 77954622756     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.05.033     Document Type: Article

References (49)

1. Akil H. Stressed and depressed. Nat Med 2005, 11:116-118.
2. Akil H., Morano M.I. The biology of stress: from periphery to brain. Biology of schizophrenia and affective disease (ARNMD) 1996, Raven Press, New York, NY. S.J. Watson (Ed.).
3. Bangasser D.A., Shors T.J. The hippocampus is necessary for enhancements and impairments of learning following stress. Nat Neurosci 2007, 10:1401-1403.
4. Bowman R.E., Beck K.D., Luine V.N. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm Behav 2003, 43:48-59.
5. Boyle M.P., Kolber B.J., Vogt S.K., Wozniak D.F., Muglia L.J. Forebrain glucocorticoid receptors modulate anxiety-associated locomotor activation and adrenal responsiveness. J Neurosci 2006, 26:1971-1978.
6. Caamano C.A., Morano M.I., Akil H. Corticosteroid receptors: a dynamic interplay between protein folding and homeostatic control. Possible implications in psychiatric disorders. Psychopharmacol Bull 2001, 35:6-23.
7. Caspi A., Moffitt T.E. Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat Rev Neurosci 2006, 7:583-590.
8. Clark R.E., Zola S.M., Squire L.R. Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 2000, 20:8853-8860.
9. Conrad C.D. The relationship between acute glucocorticoid levels and hippocampal function depends upon task aversiveness and memory processing stage. Nonlinearity Biol Toxicol Med 2005, 3:57-78.
10. Cullinan W.E., Herman J.P., Watson S.J. Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol 1993, 332:1-20.
11. de Kloet E.R., Oitzl M.S., Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci 1999, 22:422-426.
12. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev 1998, 19:269-301.
13. Diorio D., Viau V., Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 1993, 13:3839-3847.
14. File S.E., Gonzalez L.E. Anxiolytic effects in the plus-maze of 5-HT1A-receptor ligands in dorsal raphe and ventral hippocampus. Pharmacol Biochem Behav 1996, 54:123-128.
15. Frick K.M., Gresack J.E. Sex differences in the behavioral response to spatial and object novelty in adult C57BL/6 mice. Behav Neurosci 2003, 117:1283-1291.
16. Geyer M.A. Serotonergic functions in arousal and motor activity. Behav Brain Res 1996, 73:31-35.
17. Gilpin N.K., Koob G.F. Neurobiology of alcohol dependence: focus on motivational mechanisms. Alcohol Res Health 2008, 31:185-195.
18. Grailhe R., Waeber C., Dulawa S.C., Hornung J.P., Zhuang X., Brunner D., Geyer M.A., Hen R. Increased exploratory activity and altered response to LSD in mice lacking the 5-HT(5A) receptor. Neuron 1999, 22:581-591.
19. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997, 20:78-84.
20. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 2003, 24:151-180.
21. Herman J.P., Schafer M.K., Young E.A., Thompson R., Douglass J., Akil H., Watson S.J. Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. J Neurosci 1989, 9:3072-3082.
22. Kalueff A.V., Fox M.A., Gallagher P.S., Murphy D.L. Hypolocomotion, anxiety and serotonin syndrome-like behavior contribute to the complex phenotype of serotonin transporter knockout mice. Genes Brain Behav 2007, 6:389-400.
23. Kalueff A.V., Jensen C.L., Murphy D.L. Locomotory patterns, spatiotemporal organization of exploration and spatial memory in serotonin transporter knockout mice. Brain Res 2007, 1169:87-97.
24. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 2002, 3:453-462.
25. Lemaire V., Aurousseau C., Le Moal M., Abrous D.N. Behavioural trait of reactivity to novelty is related to hippocampal neurogenesis. Eur J Neurosci 1999, 11:4006-4014.
26. Lopez J.F., Akil H., Watson S.J. Neural circuits mediating stress. Biol Psychiatry 1999, 46:1461-1471.
27. Malleret G., Hen R., Guillou J.L., Segu L., Buhot M.C. 5-HT1B receptor knock-out mice exhibit increased exploratory activity and enhanced spatial memory performance in the Morris water maze. J Neurosci 1999, 19:6157-6168.
28. McEwen B.S. Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann N Y Acad Sci 2004, 1032:1-7.
29. Morimoto M., Morita N., Ozawa H., Yokoyama K., Kawata M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res 1996, 26:235-269.
30. Morris R.G. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 2006, 23:2829-2846.
31. Moses S.N., Cole C., Driscoll I., Ryan J.D. Differential contributions of hippocampus, amygdala and perirhinal cortex to recognition of novel objects, contextual stimuli and stimulus relationships. Brain Res Bull 2005, 67:62-76.
32. Moses S.N., Sutherland R.J., McDonald R.J. Differential involvement of amygdala and hippocampus in responding to novel objects and contexts. Brain Res Bull 2002, 58:517-527.
33. Mumby D.G., Gaskin S., Glenn M.J., Schramek T.E., Lehmann H. Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 2002, 9:49-57.
34. Oitzl M.S., Fluttert M., de Kloet E.R. The effect of corticosterone on reactivity to spatial novelty is mediated by central mineralocorticosteroid receptors. Eur J Neurosci 1994, 6:1072-1079.
35. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, Oxford University Press, Oxford.
36. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proc Natl Acad Sci U S A 2004, 101:853-858.
37. Ramboz S., Oosting R., Amara D.A., Kung H.F., Blier P., Mendelsohn M., Mann J.J., Brunner D., Hen R. Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc Natl Acad Sci U S A 1998, 95:14476-14481.
38. Roozendaal B., Okuda S., de Quervain D.J., McGaugh J.L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 2006, 138:901-910.
39. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 2006, 103:6741-6746.
40. Rossato J.I., Bevilaqua L.R., Myskiw J.C., Medina J.H., Izquierdo I., Cammarota M. On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learn Mem 2007, 14:36-46.
41. Save E., Poucet B., Foreman N., Buhot M.C. Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. Behav Neurosci 1992, 106:447-456.
42. Steckler T., Weis C., Sauvage M., Mederer A., Holsboer F. Disrupted allocentric but preserved egocentric spatial learning in transgenic mice with impaired glucocorticoid receptor function. Behav Brain Res 1999, 100:77-89.
43. Tackett J.L., Quilty L.C., Sellbom M., Rector N.A., Bagby R.M. Additional evidence for a quantitative hierarchical model of mood and anxiety disorders for DSM-V: the context of personality structure. J Abnorm Psychol 2008, 117:812-825.
44. Thinus-Blanc C., Save E., Rossi-Arnaud C., Tozzi A., Ammassari-Teule M. The differences shown by C57BL/6 and DBA/2 inbred mice in detecting spatial novelty are subserved by a different hippocampal and parietal cortex interplay. Behav Brain Res 1996, 80:33-40.
45. Wei Q., Hebda-Bauer E.K., Pletsch A., Luo J., Hoversten M.T., Osetek A.J., Evans S.J., Watson S.J., Seasholtz A.F., Akil H. Overexpressing the glucocorticoid receptor in forebrain causes an aging-like neuroendocrine phenotype and mild cognitive dysfunction. J Neurosci 2007, 27:8836-8844.
46. Wei Q., Lu X.Y., Liu L., Schafer G., Shieh K.R., Burke S., Robinson T.E., Watson S.J., Seasholtz A.F., Akil H. Glucocorticoid receptor overexpression in forebrain: a mouse model of increased emotional lability. Proc Natl Acad Sci U S A 2004, 101:11851-11856.
47. Winters B.D., Bussey T.J. Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. J Neurosci 2005, 25:4243-4251.
48. Winters B.D., Bussey T.J. Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J Neurosci 2005, 25:52-61.
49. Zola S.M., Squire L.R., Teng E., Stefanacci L., Buffalo E.A., Clark R.E. Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 2000, 20:451-463.