Low brain allopregnanolone levels mediate flattened circadian activity associated with memory impairments in aged rats

Biological Psychiatry

Volumn 68, Issue 10, 2010, Pages 956-963

  George, Olivier ^a,b,c   Valle, Monique ^a,b   Vitiello, Sergio ^a,b   Le Moal, Michel ^a,b   Piazza, Pier Vincenzo ^a,b   Mayo, Willy ^b  

^a INSERM   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Aging; anxiety; sleep; spatial; steroids; working memory

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; ELTANOLONE; INDOMETACIN; PRASTERONE; PREGNENOLONE; TESTOSTERONE;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN LEVEL; CIRCADIAN RHYTHM; CORPUS STRIATUM; GAS CHROMATOGRAPHY; GROUPS BY AGE; HORMONE ACTION; HORMONE BLOOD LEVEL; HYPOTHALAMUS; LOCOMOTION; LONG TERM MEMORY; MALE; MASS SPECTROMETRY; MAZE TEST; MEMORY DISORDER; NONHUMAN; OPEN FIELD TEST; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PRIORITY JOURNAL; RAT; SLEEP WAKING CYCLE; SPATIAL MEMORY;

AGING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; INDOMETHACIN; MALE; MEMORY DISORDERS; PREGNANOLONE; RATS; RATS, SPRAGUE-DAWLEY; SLEEP DISORDERS, CIRCADIAN RHYTHM; STEROIDS;

EID: 78049431667     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2010.03.022     Document Type: Article

References (65)

1. L. Marshall, and J. Born The contribution of sleep to hippocampus-dependent memory consolidation Trends Cogn Sci 11 2007 442 450
2. M.P. Walker, and R. Stickgold Sleep, memory, and plasticity Annu Rev Psychol 57 2006 139 166
3. O.P. Hornung, H. Danker-Hopfe, and I. Heuser Age-related changes in sleep and memory: Commonalities and interrelationships Exp Gerontol 40 2005 279 285
4. Y. Dagan Circadian rhythm sleep disorders (CRSD) Sleep Med Rev 6 2002 45 54
5. C. DeCarli Mild cognitive impairment: Prevalence, prognosis, aetiology, and treatment Lancet Neurol 2 2003 15 21
6. S. Ancoli-Israel, and L. Ayalon Diagnosis and treatment of sleep disorders in older adults Am J Geriatr Psychiatry 14 2006 95 103
7. J.A. Hobson, and E.F. Pace-Schott The cognitive neuroscience of sleep: Neuronal systems, consciousness and learning Nat Rev Neurosci 3 2002 679 693
8. N.F. Ruby, C.E. Hwang, C. Wessells, F. Fernandez, P. Zhang, R. Sapolsky, and H.C. Heller Hippocampal-dependent learning requires a functional circadian system Proc Natl Acad Sci U S A 105 2008 15593 15598
9. R. Stickgold, J.A. Hobson, R. Fosse, and M. Fosse Sleep, learning, and dreams: Off-line memory reprocessing Science 294 2001 1052 1057
10. S. Saha, and S. Datta Two-way active avoidance training-specific increases in phosphorylated cAMP response element-binding protein in the dorsal hippocampus, amygdala, and hypothalamus Eur J Neurosci 21 2005 3403 3414
11. W.E. Skaggs, and B.L. McNaughton Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience Science 271 1996 1870 1873
12. C.M. Pennartz, E. Lee, J. Verheul, P. Lipa, C.A. Barnes, and B.L. McNaughton The ventral striatum in off-line processing: Ensemble reactivation during sleep and modulation by hippocampal ripples J Neurosci 24 2004 6446 6456
13. S. Datta, V. Mavanji, J. Ulloor, and E.H. Patterson Activation of phasic pontine-wave generator prevents rapid eye movement sleep deprivation-induced learning impairment in the rat: A mechanism for sleep-dependent plasticity J Neurosci 24 2004 1416 1427
14. O. George, A. Parducz, D. Dupret, M. Kharouby, M. Le Moal, P.V. Piazza, and W. Mayo Smad-dependent alterations of PPT cholinergic neurons as a pathophysiological mechanism of age-related sleep-dependent memory impairments Neurobiol Aging 27 2006 1848 1858
15. E.E. Baulieu Neurosteroids: A novel function of the brain Psychoneuroendocrinology 23 1998 963 987
16. J.F. Flood, J.E. Morley, and E. Roberts Memory-enhancing effects in male mice of pregnenolone and steroids metabolically derived from it Proc Natl Acad Sci U S A 89 1992 1567 1571
17. C.A. Frye The neurosteroid 3 alpha, 5 apha-THP has antiseizure and possible neuroprotective effects in an animal model of epilepsy Brain Res 696 1995 113 120
18. I.M. Johansson, V. Birzniece, C. Lindblad, T. Olsson, and T. Backstrom Allopregnanolone inhibits learning in the Morris water maze Brain Res 934 2002 125 131
19. N. Ladurelle, B. Eychenne, D. Denton, J. Blair-West, M. Schumacher, and P. Robel Prolonged intracerebroventricular infusion of neurosteroids affects cognitive performances in the mouse Brain Res 858 2000 371 379
20. D.B. Matthews, A.L. Morrow, S. Tokunaga, and J.R. McDaniel Acute ethanol administration and acute allopregnanolone administration impair spatial memory in the Morris water task Alcohol Clin Exp Res 26 2002 1747 1751
21. S. Turkmen, P. Lundgren, V. Birzniece, E. Zingmark, T. Backstrom, and I.M. Johansson 3beta-20beta-dihydroxy-5alpha-pregnane (UC1011) antagonism of the GABA potentiation and the learning impairment induced in rats by allopregnanolone Eur J Neurosci 20 2004 1604 1612
22. M. Valle, W. Mayo, G.F. Koob, and M. Le Moal Neurosteroids in learning and memory processes Int Rev Neurobiol 46 2001 273 320
23. O. George, M. Valle, M. Le Moal, and W. Mayo Neurosteroids and cholinergic systems: Implications for sleep and cognitive processes and potential role of age-related changes Psychopharmacology (Berl) 186 2006 402 413
24. T. Maurice, A. Urani, V.L. Phan, and P. Romieu The interaction between neuroactive steroids and the sigma1 receptor function: Behavioral consequences and therapeutic opportunities Brain Res Brain Res Rev 37 2001 116 132
25. W. Mayo, O. George, S. Darbra, J.J. Bouyer, M. Valle, and M. Darnaudery Individual differences in cognitive aging: Implication of pregnenolone sulfate Prog Neurobiol 71 2003 43 48
26. M. Valle, W. Mayo, and M. Le Moal Role of pregnenolone, dehydroepiandrosterone and their sulfate esters on learning and memory in cognitive aging Brain Res Brain Res Rev 37 2001 301 312
27. M. Valle, O. George, S. Vitiello, M. Le Moal, and W. Mayo New insights into the role of neuroactive steroids in cognitive aging Exp Gerontol 39 2004 1695 1704
28. M. Valle, J.D. Rivera, G.F. Koob, R.H. Purdy, and R.L. Fitzgerald Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ionization gas chromatography/mass spectrometry Anal Biochem 287 2000 153 166
29. A.A. Alomary, R.L. Fitzgerald, and R.H. Purdy Neurosteroid analysis Int Rev Neurobiol 46 2001 97 115
30. M.J. Ebner, D.I. Corol, H. Havlikova, J.W. Honour, and J.P. Fry Identification of neuroactive steroids and their precursors and metabolites in adult male rat brain Endocrinology 147 2006 179 190
31. P. Liere, Y. Akwa, S. Weill-Engerer, B. Eychenne, A. Pianos, and P. Robel Validation of an analytical procedure to measure trace amounts of neurosteroids in brain tissue by gas chromatography-mass spectrometry J Chromatogr B Biomed Sci Appl 739 2000 301 312
32. S. Liu, J. Sjovall, and W.J. Griffiths Neurosteroids in rat brain: Extraction, isolation, and analysis by nanoscale liquid chromatography- electrospray mass spectrometry Anal Chem 75 2003 5835 5846
33. S. Jambhekar, R. Casella, and T. Maher The physicochemical characteristics and bioavailability of indomethacin from beta-cyclodextrin, hydroxyethyl-beta-cyclodextrin, and hydroxypropyl-beta-cyclodextrin complexes Int J Pharm 270 2004 149 166
34. D. Kozutsumi, A. Kawashima, T. Sugimoto, Y. Kotohda, S. Fujimori, and M. Takami Pharmacokinetics of 9alpha-fluoromedroxyprogesterone acetate in rats: Comparison with medroxyprogesterone acetate Biopharm Drug Dispos 20 1999 277 284
35. G. Saporta Description multidimentionelle de donnes numriques Analyse en composantes principales Probalits Analyse des donnes et statistique 1990 Technip Paris 159 185
36. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 1982 Academic Press New York
37. T.M. Penning, R.B. Sharp, and N.R. Krieger Purification and properties of 3 alpha-hydroxysteroid dehydrogenase from rat brain cytosol Inhibition by nonsteroidal anti-inflammatory drugs and progestins J Biol Chem 260 1985 15266 15272
38. C. Beyer, O. Gonzalez-Flores, J.M. Ramirez-Orduna, and G. Gonzalez-Mariscal Indomethacin inhibits lordosis induced by ring A-reduced progestins: Possible role of 3alpha-oxoreduction in progestin-facilitated lordosis Horm Behav 35 1999 1 8
39. A.I. Herrero, C. Sandi, and C. Venero Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors Neurobiol Learn Mem 86 2006 150 159
40. J.L.W. Yau, J. Noble, C. Hibberd, W.B. Rowe, M.J. Meaney, and R.G.M. Morris Chronic treatment with the antidepressant amitriptyline prevents impairments in water maze learning in aging rats J Neurosci 22 2002 1436 1442
41. American Academy of Sleep Medicine ICSD-International Classification of Sleep Disorders, Revised: Diagnostic and Coding Manual 2001 American Academy of Sleep Medicine Westchester, IL
42. S. Ancoli-Israel, R. Cole, C. Alessi, M. Chambers, W. Moorcroft, and C.P. Pollak The role of actigraphy in the study of sleep and circadian rhythms Sleep 26 2003 342 392
43. H.A. Middelkoop, B.J. Van Hilten, C.G. Kramer, and H.A. Kamphuisen Actigraphically recorded motor activity and immobility across sleep cycles and stages in healthy male subjects J Sleep Res 2 1993 28 33
44. B.L. Myers, and P. Badia Changes in circadian rhythms and sleep quality with aging: Mechanisms and interventions Neurosci Biobehav Rev 19 1995 553 571
45. H.S. Kudrimoti, C.A. Barnes, and B.L. McNaughton Reactivation of hippocampal cell assemblies: Effects of behavioral state, experience, and EEG dynamics J Neurosci 19 1999 4090 4101
46. A.K. Lee, and M.A. Wilson Memory of sequential experience in the hippocampus during slow wave sleep Neuron 36 2002 1183 1194
47. P. Maquet The role of sleep in learning and memory Science 294 2001 1048 1052
48. E.J. Van Someren Circadian and sleep disturbances in the elderly Exp Gerontol 35 2000 1229 1237
49. A.M. Costa, K.T. Spence, S.S. Smith, and J.M. ffrench-Mullen Withdrawal from the endogenous steroid progesterone results in GABAA currents insensitive to benzodiazepine modulation in rat CA1 hippocampus J Neurophysiol 74 1995 464 469
50. K. Damianisch, R. Rupprecht, and M. Lancel The influence of subchronic administration of the neurosteroid allopregnanolone on sleep in the rat Neuropsychopharmacology 25 2001 576 584
51. M. Lancel, J. Faulhaber, T. Schiffelholz, E. Romeo, F. Di Michele, F. Holsboer, and R. Rupprecht Allopregnanolone affects sleep in a benzodiazepine-like fashion J Pharmacol Exp Ther 282 1997 1213 1218
52. R.D. Brinton, and J.M. Wang Preclinical analyses of the therapeutic potential of allopregnanolone to promote neurogenesis in vitro and in vivo in transgenic mouse model of Alzheimer's disease Curr Alzheimer Res 3 2006 11 17
53. I. Ciriza, I. Azcoitia, and L.M. Garcia-Segura Reduced progesterone metabolites protect rat hippocampal neurones from kainic acid excitotoxicity in vivo J Neuroendocrinol 16 2004 58 63
54. M. Djebaili, S.W. Hoffman, and D.G. Stein Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex Neuroscience 123 2004 349 359
55. J. He, S.W. Hoffman, and D.G. Stein Allopregnanolone, a progesterone metabolite, enhances behavioral recovery and decreases neuronal loss after traumatic brain injury Restor Neurol Neurosci 22 2004 19 31
56. E.A. Keller, A. Zamparini, L.N. Borodinsky, M.C. Gravielle, and M.L. Fiszman Role of allopregnanolone on cerebellar granule cells neurogenesis Brain Res Dev Brain Res 153 2004 13 17
57. E. Leonelli, R. Bianchi, G. Cavaletti, D. Caruso, D. Crippa, and L.M. Garcia-Segura Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: A multimodal analysis Neuroscience 144 2007 1293 1304
58. R.J. Hemler, J.H. Hoogeveen, V. Kraaier, A.C. Van Huffelen, G.H. Wieneke, R. Hijman, and J.H. Glerum A pharmacological model of cerebral ischemia The effects of indomethacin on cerebral blood flow velocity, quantitative EEG and cognitive functions Methods Find Exp Clin Pharmacol 12 1990 641 643
59. T. Ishida, T. Sato, M. Irifune, K. Tanaka, K. Hirate, N. Nakamura, and T. Nishikawa Inhibitory effect of cyclooxygenase inhibitors on the step-through passive avoidance performance in mice treated with NC-1900, an arginine-vasopressin fragment analog Methods Find Exp Clin Pharmacol 29 2007 315 320
60. L.A. Teather, M.G. Packard, and N.G. Bazan Post-training cyclooxygenase-2 (COX-2) inhibition impairs memory consolidation Learn Mem 9 2002 41 47
61. W. Mayo, F. Dellu, P. Robel, J. Cherkaoui, M. Le Moal, E.E. Baulieu, and H. Simon Infusion of neurosteroids into the nucleus basalis magnocellularis affects cognitive processes in the rat Brain Res 607 1993 324 328
62. S. Turkmen, M. Lofgren, V. Birzniece, T. Backstrom, and I.M. Johansson Tolerance development to Morris water maze test impairments induced by acute allopregnanolone Neuroscience 139 2006 651 659
63. A.A. Walf, M.E. Rhodes, and C.A. Frye Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats Neurobiol Learn Mem 86 2006 35 46
64. C.A. Frye, and E.H. Lacey Progestins influence performance on cognitive task independent of changes of affective states Psychobiology 28 2000 550 563
65. C.A. Frye Neurosteroids' effects and mechanisms for social, cognitive, emotional, and physical functions Psychoneuroendocrinology 34 suppl 1 2009 S143 S161