Neonatal stress affects vulnerability of cholinergic neurons and cognition in the rat: Involvement of the HPA axis

Psychoneuroendocrinology

Volumn 34, Issue 10, 2009, Pages 1495-1505

  Aisa, Bárbara ^a   Gil Bea, Francisco Javier ^a   Marcos, Beatriz ^a   Tordera, Rosa ^a   Lasheras, Berta ^a   Del Río, Joaquín ^a   Ramírez, Maria J ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

Author keywords

192 IgG saporin; Acetylcholine; Glucocorticoid receptor; Learning and memory; NGF

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINE ACETYLTRANSFERASE; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID RECEPTOR; IMMUNOTOXIN; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; SAPORIN;

ADULT ANIMAL; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FOREBRAIN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IN SITU HYBRIDIZATION; LEARNING DISORDER; MATERNAL DEPRIVATION; MAZE TEST; MEMORY DISORDER; NEONATAL STRESS; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, MONOCLONAL; CEREBRAL CORTEX; CHOLINERGIC FIBERS; COGNITION; CORTICOTROPIN-RELEASING HORMONE; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; HYPOTHALAMUS; IMMUNOTOXINS; MALE; MATERNAL DEPRIVATION; NERVE GROWTH FACTOR; PITUITARY-ADRENAL SYSTEM; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; RECEPTORS, NERVE GROWTH FACTOR; RIBOSOME INACTIVATING PROTEINS, TYPE 1; STRESS, PSYCHOLOGICAL;

EID: 70349835809     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2009.05.003     Document Type: Article

References (78)

1. Abrahám I., Harkany T., Horvath K.M., Veenema A.H., Penke B., Nyakas C., and Luiten P.G. Chronic corticosterone administration dose-dependently modulates Abeta(1-42)- and NMDA-induced neurodegeneration in rat magnocellular nucleus basalis. J. Neuroendocrinol. 12 (2000) 486-494
2. Abrahám I., Harkany T., Horvath K.M., and Luiten P.G. Action of glucocorticoids on survival of nerve cells: promoting neurodegeneration or neuroprotection?. J. Neuroendocrinol. 13 (2001) 749-760
3. Aisa B., Tordera R., Lasheras B., Del Río J., and Ramírez M.J. Cognitive impairment associated with HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32 (2007) 256-266
4. Amaral D.G., and Dent J.A. Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 195 (1981) 51-86
5. Anisman H., Zaharia M.D., Meaney M.J., and Merali Z. Do early-life events permanently alter behavioral and hormonal responses to stressors?. Int. J. Dev. Neurosci. 16 (1998) 149-164
6. Belanoff J.K., Jurik J., Schatzberg L.D., DeBattista C., and Schatzberg A.F. Slowing the progression of cognitive decline in Alzheimer's disease using mifepristone. J. Mol. Neurosci. 19 (2002) 201-206
7. Berton O., and Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7 (2006) 137-151
8. Bremner J.D., Vythilingam M., Vermetten E., Southwick S.M., McGlashan T., Staib L.H., Soufer R., and Charney D.S. Neural correlates of declarative memory for emotionally valenced words in women with posttraumatic stress disorder related to early childhood sexual abuse. Biol. Psychiatry 53 (2003) 879-889
9. Buresová O., Bolhuis J.J., and Bures J. Differential effects of cholinergic blockade on performance of rats in the water tank navigation task and in a radial water maze. Behav. Neurosci. 100 (1986) 476-482
10. Chen J.X., Tang Y.T., and Yang J.X. Changes of glucocorticoid receptor and levels of CRF mRNA, POMC mRNA in brain of chronic immobilization stress rats. Cell. Mol. Neurobiol. 28 (2007) 237-244
11. Cintra A., Bhatnagar M., Chadi G., Tinner B., Lindberg J., Gustafsson J.A., Agnati L.F., and Fuxe K. Glial and neuronal glucocorticoid receptor immunoreactive cell populations in developing, adult, and aging brain. Ann. N. Y. Acad. Sci. 746 (1994) 42-61
12. Cirulli F., Micera A., Alleva E., and Aloe L. Early maternal separation increases NGF expression in the developing rat hippocampus. Pharmacol. Biochem. Behav. 59 (1998) 853-858
13. Cirulli F., Alleva E., Antonelli A., and Aloe L. NGF expression in the developing rat brain: effects of maternal separation. Brain Res. Dev. Brain Res. 123 (2000) 129-134
14. Craig L.A., Hong N.S., Kopp J., and McDonald R.J. Emergence of spatial impairment in rats following specific cholinergic depletion of the medial septum combined with chronic stress. Eur. J. Neurosci. 27 (2008) 2262-2271
15. De Kloet E.R., Vreugdenhil E., Oitzl M.S., and Joëls M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19 (1998) 269-301
16. DeBattista C., and Belanoff J. C-1073 (mifepristone) in the adjunctive treatment of Alzheimer's disease. Curr. Alzheimer Res. 2 (2005) 125-129
17. Dhikav V., and Anand K.S. Glucocorticoids may initiate Alzheimer's disease: a potential therapeutic role for mifepristone (RU-486). Med. Hypotheses 68 (2007) 1088-1092
18. Diez-Ariza M., Redondo C., García-Alloza M., Lasheras B., Del Río J., and Ramírez M.J. Flumazenil and tacrine increase the effectiveness of ondansetron on scopolamine-induced impairment of spatial learning in rats. Psychopharmacology 169 (2003) 35-41
19. Diorio D., Viau V., and Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 13 (1993) 3839-3847
20. Elgh E., Lindqvist, Astot A., Fagerlund M., Eriksson S., Olsson T., and Näsman B. Cognitive dysfunction, hippocampal atrophy and glucocorticoid feedback in Alzheimer's disease. Biol. Psychiatry 59 (2006) 155-161
21. Emgard M., Paradisi M., Pirondi S., Fernández M., Giardino L., and Calzà L. Prenatal glucocorticoid exposure affects learning and vulnerability of cholinergic neurons. Neurobiol. Aging 28 (2007) 112-121
22. Finkelstein Y., Koffler B., Rabey J.M., and Gilad G.M. Dynamics of cholinergic synaptic mechanisms in rat hippocampus after stress. Brain Res. 343 (1985) 314-319
23. Fischer W., Wictorin K., Björklund A., Williams L.R., Varon S., and Gage F.H. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329 (1987) 65-68
24. García-Alloza M., Zaldua N., Diez-Ariza M., Marcos B., Lasheras B., Gil-Bea F.J., and Ramírez M.J. Effect of selective cholinergic denervation on the serotonergic system: implications for learning and memory. J. Neuropathol. Exp. Neurol. 65 (2006) 1074-1081
25. Geula C. Abnormalities of neural circuitry in Alzheimer's disease: hippocampus and cortical cholinergic innervation. Neurology 51 (1998) 18-29
26. Gilad G.M., Mahon B.D., Finkelstein Y., Koffler B., and Gilad V.H. Stress-induced activation of the hippocampal cholinergic system and the pituitary-adrenocortical axis. Brain Res. 347 (1985) 404-408
27. Gil-Bea F.J., Domínguez J., García-Alloza M., Marcos B., Lasheras B., and Ramírez M.J. Facilitation of cholinergic transmission by combined treatment of ondansetron with flumazenil after cortical cholinergic deafferentation. Neuropharmacology 47 (2004) 225-232
28. Han J.S., Bizon J.L., Chun H.J., Maus C.E., and Gallagher M. Decreased glucocorticoid receptor mRNA and dysfunction of HPA axis in rats after removal of the cholinergic innervation to hippocampus. Eur. J. Neurosci. 16 (2002) 1399-1404
29. Heckers S., Ohtake T., Wiley R.G., Lappi D.A., Geula C., and Mesulam M.M. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J. Neurosci. 14 (1994) 1271-1289
30. Helm K.A., Han J.S., and Gallagher M. Effects of cholinergic lesions produced by infusions of 192 IgG-saporin on glucocorticoid receptor mRNA expression in hippocampus and medial prefrontal cortex of the rat. Neuroscience 115 (2002) 765-774
31. Helm K.A., Ziegler D.R., and Gallagher M. Habituation to stress and dexamethasone suppression in rats with selective basal forebrain cholinergic lesions. Hippocampus 14 (2004) 628-635
32. Hörtnagl H., Berger M.L., Havelec L., and Hornykiewicz O. Role of glucocorticoids in the cholinergic degeneration in rat hippocampus induced by ethylcholine aziridinium (AF64A). J. Neurosci. 13 (1993) 2939-2945
33. Horvath K.M., Harkany T., Mulder J., Koolhaas J.M., Luiten P.G.M., and Meerlo P. Neonatal handling increases sensitivity to acute neurodegeneration in adult rats. J. Neurobiol. 60 (2004) 463-472
34. Huot R.L., Thrivikraman K.V., Meaney M.J., and Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology 158 (2001) 366-373
35. Imperato A., Puglisi-Allegra S., Casolini P., Zocchi A., and Angelucci L. Stress-induced enhancement of dopamine and acetylcholine release in limbic structures: role of corticosterone. Eur. J. Pharmacol. 165 (1989) 337-338
36. Jacobson L., and Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 12 (1991) 118-134
37. Joëls M., Krugers H., and Karst H. Stress-induced changes in hippocampal function. Prog. Brain Res. 167 (2008) 3-15
38. Kawano K., Morinobu S., Sawada T., Tsuji S., Erabi K., Fuchikami M., Kozuru T., Yamawaki S., Hisaoka K., and Takebayashi M. Prior neonatal isolation reduces induction of NGF mRNA and decreases GDNF mRNA in the hippocampus of juvenile and adult rodents subjected to immobilization stress. Synapse 62 (2008) 259-267
39. Knipper M., da Penha Berzaghi M., Blöchl A., Breer H., Thoenen H., and Lindholm D. Positive feedback between acetylcholine and the neurotrophins nerve growth factor and brain-derived neurotrophic factor in the rat hippocampus. Eur. J. Neurosci. 6 (1994) 668-671
40. Koh S., and Loy R. Localization and development of nerve growth factor-sensitive rat basal forebrain neurons and their afferent projections to hippocampus and neocortex. J. Neurosci. 9 (1989) 2999-3018
41. Koide T., Wieloch T.W., and Siesjö B.K. Circulating catecholamines modulate ischemic brain damage. J. Cereb. Blood Flow Metab. 6 (1986) 559-565
42. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Meaney M.J., and Plotsky P.M. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 122 (2000) 81-103
43. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., and Plotsky P.M. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol. Psychiatry 55 (2004) 367-375
44. Landfield P.W., Blalock E.M., Chen K.C., and Porter N.M. A new glucocorticoid hypothesis of brain aging: implications for Alzheimer's disease. Curr. Alzheimer Res. 4 (2007) 205-212
45. Leanza G., Nilsson O.G., Wiley R.G., and Björklund A. Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: behavioural, biochemical and stereological studies in the rat. Eur. J. Neurosci. 7 (1995) 329-343
46. Lehmann J., and Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?. Rev. Neurosci. 11 (2000) 383-408
47. Liu D., Diorio J., Day J.C., Francis D.D., and Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3 (2000) 799-806
48. Lupien S.J., Lecours A.R., Lussier I., Schwartz G., Nair N.P., and Meaney M.J. Basal cortisol levels and cognitive deficits in human aging. J. Neurosci. 14 (1994) 2893-2903
49. Lupien S.J., de Leon M., de Santi S., Convit A., Tarshish C., Nair N.P., Thakur M., McEwen B.S., Hauger R.L., and Meaney M.J. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1 (1998) 69-73
50. Lupien S.J., Maheu F., Tu M., Fiocco A., and Schramek T.E. The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain Cogn. 65 (2007) 209-237
51. Macrí S., Mason G.J., and Würbel H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. Eur. J. Neurosci. 20 (2004) 1017-1024
52. Marais L., Van Rensburg S.J., Van Zyl J.M., Stein D.J., and Daniels W.M. Maternal separation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus. Neurosci. Res. 61 (2008) 106-112
53. Matrone C., Di Lucio A., Meli G., D'Aguanno S., Severino C., Ciotti M.T., Cattaneo A., and Calissano P. Activation of the amyloidogenic route by NGF deprivation induces apoptotic death in PC12 cells. J. Alzheimers Dis. 13 (2008) 81-96
54. McGaughy J., Everitt B.J., Robbins T.W., and Sarter M. The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins. Behav. Brain Res. 115 (2000) 251-263
55. McGeer P.L., McGeer E.G., Suzuki J., Dolman C.E., and Nagai T. Aging, Alzheimer's disease, and the cholinergic system of the basal forebrain. Neurology 34 (1984) 741-745
56. Mobley W.C., Rutkowski J.L., Tennekoon G.I., Gemski J., Buchanan K., and Johnston M.V. Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Brain Res. 387 (1986) 53-62
57. Mocchetti I., Spiga G., Hayes V.Y., Isackson P.J., and Colangelo A. Glucocorticoids differentially increase nerve growth factor and basic fibroblast growth factor expression in the rat brain. J. Neurosci. 16 (1996) 2141-2148
58. Morris R. Developments of a water maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984) 47-60
59. Mufson E.J., Kroin J.S., Sendera T.J., and Sobreviela T. Distribution and retrograde transport of trophic factors in the central nervous system: functional implications for the treatment of neurodegenerative diseases. Prog. Neurobiol. 57 (1999) 451-484
60. Murphy E.K., Spencer R.L., Sipe K.J., and Herman J.P. Decrements in nuclear glucocorticoid receptor (GR) protein levels and DNA binding in aged rat hippocampus. Endocrinology 143 (2002) 1362-1370
61. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1982), Academic Press, San Diego
62. Pioro E.P., and Cuello A.C. Distribution of nerve growth factor receptor-like immunoreactivity in the adult rat central nervous system. Effect of colchicine and correlation with the cholinergic system. I. Forebrain. Neuroscience 34 (1990) 57-87
63. Ploj K., Roman E., and Nylander I. Long-term effects of maternal separation on ethanol intake and brain opioid and dopamine receptors in male Wistar rats. Neuroscience 121 (2003) 787-799
64. Pondiki S., Stamatakis A., Fragkouli A., Philippidis H., and Stylianopoulou F. Effects of neonatal handling on the basal forebrain cholinergic system of adult male and female rats. Neuroscience 142 (2006) 305-314
65. Sapolsky R.M., Krey L.C., and McEwen B.S. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci. 5 (1985) 1222-1227
66. Sapolsky R.M., and Pulsinelli W.A. Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications. Science 229 (1985) 1397-1400
67. Sapolsky R.M., Krey L.C., and McEwen B.S. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr. Rev. 7 (1986) 284-301
68. Sapolsky R.M., Armanini M., Packan D., and Tombaugh G. Stress and glucocorticoids in aging. Endocrinol. Metab. Clin. North Am. 16 (1987) 965-980
69. Sarter M., and Bruno J.P. Developmental origins of the age-related decline in cortical cholinergic function and associated cognitive abilities. Neurobiol. Aging 25 (2004) 1127-1139
70. Smith M.L., and Booze R.M. Cholinergic and GABAergic neurons in the nucleus basalis region of young and aged rats. Neuroscience 67 (1995) 679-688
71. Smith S.M., Vaughan J.M., Donaldson C.J., Rivier J., Li C., Chen A., and Vale W.W. Cocaine- and amphetamine-regulated transcript activates the hypothalamic-pituitary-adrenal axis through a corticotropin-releasing factor receptor-dependent mechanism. Endocrinology 145 (2004) 5202-5209
72. Sobreviela T., Clary D.O., Reichardt L.F., Brandabur M.M., Kordower J.H., and Mufson E.J. TrkA-immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. J. Comp. Neurol. 350 (1994) 587-611
73. Sotthibundhu A., Sykes A.M., Fox B., Underwood C.K., Thangnipon W., and Coulson E.J. Beta-amyloid (1-42) induces neuronal death through the p75 neurotrophin receptor. J. Neurosci. 28 (2008) 3941-3946
74. Spencer R.L., Kalman B.A., Cotter C.S., and Deak T. Discrimination between changes in glucocorticoid receptor expression and activation in rat brain using western blot analysis. Brain Res. 868 (2000) 275-286
75. Sutanto W., Rosenfeld P., de Kloet E.R., and Levine S. Long-term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors. Brain Res. Dev. Brain Res. 92 (1996) 156-163
76. Tizabi Y., Gilad V.H., and Gilad G.M. Effects of chronic stressors or corticosterone treatment on the septohippocampal cholinergic system of the rat. Neurosci. Lett. 105 (1989) 177-182
77. Wiley R.G., Oeltmann T.N., and Lappi D.A. Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res. 562 (1991) 149-153
78. Wrenn C.C., Lappi D.A., and Wiley R.G. Threshold relationship between lesion extent of the cholinergic basal forebrain in the rat and working memory impairment in the radial maze. Brain Res. 847 (1999) 284-298