Long-term behavioral and NMDA receptor effects of young-adult corticosterone treatment in BDNF heterozygous mice

Neurobiology of Disease

Volumn 46, Issue 3, 2012, Pages 722-731

  Klug, Maren ^a,b   Hill, Rachel A ^a   Choy, Kwok Ho Christopher ^a   Kyrios, Michael ^b   Hannan, Anthony J ^c   van den Buuse, Maarten ^a,c  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Anxiety; BDNF; Corticosterone; Hippocampus; NMDA receptor; Prepulse inhibition; Spatial memory; Startle

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CORTICOSTERONE; DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN LEVEL; CONTROLLED STUDY; FEMALE; HETEROZYGOTE; HIPPOCAMPUS; MALE; MAZE TEST; MOUSE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; SPATIAL MEMORY; STARTLE REFLEX; STRESS;

ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; DIZOCILPINE MALEATE; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HETEROZYGOTE; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; RECEPTORS, N-METHYL-D-ASPARTATE; SEX CHARACTERISTICS; STARTLE REACTION;

EID: 84860838938     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.03.015     Document Type: Article

References (76)

1. Amadoro G., et al. NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2892-2897.
2. Angelucci F., et al. BDNF in schizophrenia, depression and corresponding animal models. Mol. Psychiatry 2005, 10:345-352.
3. Bakshi V.P., Geyer M.A. Multiple limbic regions mediate the disruption of prepulse inhibition produced in rats by the noncompetitive NMDA antagonist dizocilpine. J. Neurosci. 1998, 18:8394-8401.
4. Bannerman D.M., et al. Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav. Neurosci. 2002, 116:884-901.
5. Bannerman D.M., et al. Regional dissociations within the hippocampus - memory and anxiety. Neurosci. Biobehav. Rev. 2004, 28:273-283.
6. Barkus C., et al. Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion. Eur. J. Pharmacol. 2010, 626:49-56.
7. Bast T., Feldon J. Hippocampal modulation of sensorimotor processes. Prog. Neurobiol. 2003, 70:319-345.
8. Bast T., et al. Effects of MK801 and neuroleptics on prepulse inhibition: re-examination in two strains of rats. Pharmacol. Biochem. Behav. 2000, 67:647-658.
9. Bayer T.A., et al. Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the "two hit hypothesis". J. Psychiatr. Res. 1999, 33:543-548.
10. Bowman R.E., et al. Chronic restraint stress enhances radial arm maze performance in female rats. Brain Res. 2001, 904:279-289.
11. Braff D.L., et al. Gating and habituation deficits in the schizophrenia disorders. Clin. Neurosci. 1995, 3:131-139.
12. Buckley P.F., et al. Neurotrophins and schizophrenia. Schizophr. Res. 2007, 94:1-11.
13. Caldeira M.V., et al. BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol. Cell. Neurosci. 2007, 35:208-219.
14. Carlsson A., et al. A glutamatergic deficiency model of schizophrenia. Br. J. Psychiatry 1999, 174:2-6.
15. Chen Y., et al. Environmental enrichment and chronic restraint stress in ICR mice: effects on prepulse inhibition of startle and Y-maze spatial recognition memory. Behav. Brain Res. 2010, 212:49-55.
16. Choy K.H., van den Buuse M. Attenuated disruption of prepulse inhibition by dopaminergic stimulation after maternal deprivation and adolescent corticosterone treatment in rats. Eur. Neuropsychopharmacol. 2008, 18:1-13.
17. Choy K.H., et al. Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 2008, 18:655-667.
18. Choy K.H.C., et al. The effect of 'two hit' neonatal and young-adult stress on dopaminergic modulation of prepulse inhibition and dopamine receptor density. Br. J. Pharmacol. 2009, 156:388-396.
19. Cirulli F., et al. Intrahippocampal administration of BDNF in adult rats affects short-term behavioral plasticity in the Morris water maze and performance in the elevated plus-maze. Hippocampus 2004, 14:802-807.
20. Conrad C.D., et al. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 1996, 110:1321-1334.
21. Conrad C.D., et al. Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol. Learn. Mem. 2003, 79:32-40.
22. Coyle J.T. Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell. Mol. Neurobiol. 2006, 26:365-384.
23. Dellu F., et al. A two-trial memory task with automated recording: study in young and aged rats. Brain Res. 1992, 588:132-139.
24. Dellu F., et al. Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiol. Learn. Mem. 2000, 73:31-48.
25. Durany N., et al. Brain-derived neurotrophic factor and neurotrophin 3 in schizophrenic psychoses. Schizophr. Res. 2001, 52:79-86.
26. Egan M.F., et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 2003, 112:257-269.
27. Ernfors P., et al. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 1994, 368:147-150.
28. Foy M.R. Ovarian hormones, aging and stress on hippocampal synaptic plasticity. Neurobiol. Learn. Mem. 2011, 95:134-144.
29. Geyer M.A., et al. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 2001, 156:117-154.
30. Gorski J.A., et al. Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice. Neuroscience 2003, 121:341-354.
31. Gourley S.L., et al. Acute hippocampal brain-derived neurotrophic factor restores motivational and forced swim performance after corticosterone. Biol. Psychiatry 2008, 64:884-890.
32. Gratacos M., et al. Brain-derived neurotrophic factor Val66Met and psychiatric disorders: meta-analysis of case-control studies confirm association to substance-related disorders, eating disorders, and schizophrenia. Biol. Psychiatry 2007, 61:911-922.
33. Hashimoto T., et al. Relationship of brain-derived neurotrophic factor and its receptor TrkB to altered inhibitory prefrontal circuitry in schizophrenia. J. Neurosci. 2005, 25:372-383.
34. Heldt S.A., et al. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol. Psychiatry 2007, 12:656-670.
35. Hill, R.A., et al., in press. Modulatory effects of sex steroid hormones on BDNF-TrkB expression during adolescent development in C57Bl/6 mice. J. Neuroendocrinol.
36. Hill R.A., van den Buuse M. Sex-dependent and region-specific changes in TrkB signaling in BDNF heterozygous mice. Brain Res. 2011, 1384:51-60.
37. Joels M., et al. Learning under stress: how does it work?. Trends Cogn. Sci. 2006, 10:152-158.
38. Karatsoreos I.N., et al. Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 2010, 151:2117-2127.
39. Laurie D.J., Seebrug P.H. Ligand affinities at recombinant N-methyl-d-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 1994, 268:335-345.
40. Lessmann V., Heumann R. Modulation of unitary glutamatergic synapses by neurotrophin-4/5 or brain-derived neurotrophic factor in hippocampal microcultures: presynaptic enhancement depends on pre-established paired-pulse facilitation. Neuroscience 1998, 86:399-413.
41. Lewis D.A., Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu. Rev. Neurosci. 2002, 25:409-432.
42. Lin S.Y., et al. BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res. 1998, 55:20-27.
43. Linnarsson S., et al. Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 1997, 9:2581-2587.
44. Liu Y., et al. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J. Neurosci. 2007, 27:2846-2857.
45. Luine V., et al. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 1994, 639:167-170.
46. Maynard T.M., et al. Neural development, cell-cell signaling, and the "two-hit" hypothesis of schizophrenia. Schizophr. Bull. 2001, 27:457-476.
47. McEwen B. Estrogen actions throughout the brain. Recent Prog. Horm. Res. 2002, 57:357-384.
48. Miller E.J., et al. Pathways from the ventral hippocampus and caudal amygdala to forebrain regions that regulate sensorimotor gating in the rat. Neuroscience 2010, 165:601-611.
49. Montkowski A., Holsboer F. Intact spatial learning and memory in transgenic mice with reduced BDNF. Neuroreport 1997, 8:779-782.
50. Motevasseli T., et al. Role of ventral hippocampal NMDA receptors in anxiolytic-like effect of morphine. Physiol. Behav. 2010, 101:608-613.
51. Mu J.S., et al. Deprivation of endogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats. Brain Res. 1999, 835:259-265.
52. Mueser K.T., McGurk S.R. Schizophrenia. Lancet 2004, 363:2063-2072.
53. Murray R.M., Fearon P. The developmental 'risk factor' model of schizophrenia. J. Psychiatr. Res. 1999, 33:497-499.
54. Nascimento Häckl L.P., Carobrez A.P. Distinct ventral and dorsal hippocampus AP5 anxiolytic effects revealed in the elevated plus-maze task in rats. Neurobiol. Learn. Mem. 2007, 88:177-185.
55. Newcomer J.W., Krystal J.H. NMDA receptor regulation of memory and behavior in humans. Hippocampus 2001, 11:529-542.
56. Nitta A., et al. Administration of corticosterone alters intracellular localization of brain-derived neurotrophic factor-like immunoreactivity in the rat brain. Neurosci. Lett. 1997, 226:115-118.
57. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 1992, 106:62-71.
58. Oitzl M.S., et al. Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12,790-12,795.
59. Schaaf M.J., et al. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res. 1998, 813:112-120.
60. Shoemaker J.M., et al. Prefrontal D1 and ventral hippocampal N-methyl-d-aspartate regulation of startle gating in rats. Neuroscience 2005, 135:385-394.
61. Smith M.A., et al. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci. 1995, 15:1768-1777.
62. Song L., et al. Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol. Biochem. Behav. 2006, 83:186-193.
63. Sterlemann V., et al. Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 2010, 20:540-549.
64. Stone E.A., et al. A final common pathway for depression? Progress toward a general conceptual framework. Neurosci. Biobehav. Rev. 2008, 32:508-524.
65. Suen P.C., et al. Brain-derived neurotrophic factor rapidly enhances phosphorylation of the postsynaptic N-methyl-d-aspartate receptor subunit 1. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:8191-8195.
66. Tang Y.P., et al. Genetic enhancement of learning and memory in mice. Nature 1999, 401:63-69.
67. van den Buuse M. Modeling the positive symptoms of schizophrenia in genetically modified mice: pharmacology and methodology aspects. Schizophr. Bull. 2010, 36:246-270.
68. 1A receptor stimulation, which are strongly dependent on the genetic background. Psychopharmacology (Berl) 2007, 195:273-283.
69. van den Buuse M., et al. Neuregulin 1 hypomorphic mutant mice: enhanced baseline locomotor activity but normal psychotropic drug-induced hyperlocomotion and prepulse inhibition regulation. Int. J. Neuropsychopharmacol. 2009, 12:1383-1393.
70. Wang J.H., et al. Improved spatial recognition memory in mice lacking adenosine A2A receptors. Exp. Neurol. 2006, 199:438-445.
71. Wang D., et al. Genetic enhancement of memory and long-term potentiation but not CA1 long-term depression in NR2B transgenic rats. PLoS One 2009, 4:e7486.
72. Weickert C.S., et al. Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 2003, 8:592-610.
73. Weiland N.G., et al. Chronic corticosterone treatment induces parallel changes in N-methyl-d-aspartate receptor subunit messenger RNA levels and antagonist binding sites in the hippocampus. Neuroscience 1997, 78:653-662.
74. Wright R.L., Conrad C.D. Chronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 2005, 8:151-154.
75. Yang Q., et al. Neuroprotective effects of hydroxysafflor yellow A against excitotoxic neuronal death partially through down-regulation of NR2B-containing NMDA receptors. Neurochem. Res. 2010, 35:1353-1360.
76. Zhang W.N., et al. Micro-infusion of the non-competitive N-methyl-d-aspartate receptor antagonist MK-801 (dizocilpine) into the dorsal hippocampus of wistar rats does not affect latent inhibition and prepulse inhibition, but increases startle reaction and locomotor activity. Neuroscience 2000, 101:589-599.