Behavioral testing-related changes in the expression of Synapsin I and glucocorticoid receptors in standard and enriched aged Wistar rats

Experimental Gerontology

Volumn 58, Issue , 2014, Pages 292-302

  Sampedro Piquero, P ^a,b   Arias, J L ^a,b   Begega, A ^a,b  

^a UNIVERSITY OF OVIEDO   (Spain)

^b INEUROPA Instituto de Neurociencias del Principado de Asturias   (Spain)

Author keywords

Aging; Glucocorticoid receptor; Hippocampus; Spatial memory; Synapsin I

Indexed keywords

GLUCOCORTICOID RECEPTOR; SYNAPSIN I; NR3C1 PROTEIN, RAT; SYNAPSIN;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; ELEVATED ZERO MAZE TEST; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; EXPERIMENTAL BEHAVIORAL TEST; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; MALE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RADIAL ARM WATER MAZE; RAT; SPATIAL MEMORY; WORKING MEMORY; AGE; ANIMAL; ANIMAL BEHAVIOR; ANIMAL HOUSING; HIPPOCAMPUS; MAZE TEST; METABOLISM; MOTOR ACTIVITY; PREVENTION AND CONTROL; PSYCHOLOGY; REACTION TIME; TIME; WISTAR RAT;

AGE FACTORS; AGING; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; HIPPOCAMPUS; HOUSING, ANIMAL; MALE; MAZE LEARNING; MOTOR ACTIVITY; RATS, WISTAR; REACTION TIME; RECEPTORS, GLUCOCORTICOID; SYNAPSINS; TIME FACTORS;

EID: 84907933782     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.09.004     Document Type: Article

References (73)

1. Aguilera G. HPA axis responsiveness to stress: implications for healthy aging. Exp. Gerontol. 2011, 46:90-95.
2. Alves J., Magalhaes R., Machado A., Gonçalves O.F., Sampaio A., Petrosyan A. Non-pharmacological cognitive intervention for aging and dementia: current perspectives. World J. Clin. Cases 2013, 1:233-241.
3. Artola A., von Frijtag J.C., Fermont P.C., Gispen W.H., Schrama L.H., Kamal A., Spruijt B.M. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur. J. Neurosci. 2006, 23:261-272.
4. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., Zhang W.N., Pothuizen H.H., Feldon J. Regional dissociations within the hippocampus-memory and stress. Neurosci. Biobehav. Rev. 2004, 28:273-283.
5. Baraldi T., Schöwe N., Balthazar J., Monteiro-Silva K.C., Albuquerque M.S., Buck H., Viel T. Cognitive stimulation during lifetime and in the aged phase improved spatial memory, and altered neuroplasticity and cholinergic markers of mice. Exp. Gerontol. 2013, 48:831-838.
6. Beer Z., Chwiesko C., Sauvage M. Processing of spatial and non-spatial information reveals functional homogeneity along the dorso-ventral axis of CA3, but not CA1. Neurobiol. Learn. Mem. 2014, 111:56-64.
7. Bizon J.L., Helm K.A., Han J.S., Chun H.J., Pucilowska J., Lund P.K., Gallagher M. Hypothalamic-pituitary-adrenal axis function and corticosterone receptor expression in behaviourally characterized young and aged Long-Evans rats. Eur. J. Neurosci. 2001, 14:1739-1751.
8. Burger C., Lopez M.C., Feller J.A., Baker H.V., Muzyczka N., Mandel R.J. Changes in transcription within the CA1 field of the hippocampus are associated with age-related spatial learning impairments. Neurobiol. Learn. Mem. 2007, 87:21-41.
9. Chen D.Y., Bambah-Mukku D., Pollonini G., Alberini C.M. Glucocorticoid receptors recruit the CaMKIIalpha-BDNF-CREB pathways to mediate memory consolidation. Nat. Neurosci. 2012, 15:1707-1714.
10. Cummins R.A., Walsh R.N., Budtz-Olsen O.E., Konstantinos T., Horsfall C.R. Environmentally- induced changes in the brains of elderly rats. Nature 1973, 243:516-518.
11. De Kloet E.R., Jöels M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
12. Diniz D.G., Foro C.A., Rego C.M., Gloria D.A., de Oliveira F.R., Paes J.M., de Sousa A.A., Tokuhashi T.P., Trindade L.S., Turiel M.C., Vasconcelos E.G., Torres J.B., Cunnigham C., Perry V.H., Vasconcelos P.F., Diniz C.W. Environmental impoverishment and aging alter object recognition, spatial learning, and dentate gyrus astrocytes. Eur. J. Neurosci. 2010, 32:509-519.
13. Donley M.P., Schulkin J., Rosen J.B. Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear. Behav. Brain Res. 2005, 164:197-205.
14. Duffy S.N., Craddock K.J., Nguyen P.V. Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learn. Mem. 2001, 8:26-34.
15. Eckles K.E., Dudek E.M., Bickford P.C., Browning M.D. Amelioration of age-related deficits in the stimulation of synapsin phosphorylation. Neurobiol. Aging 1997, 18:213-217.
16. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 2000, 1:41-50.
17. Fa M., Xia L., Anunu R., Kehat O., Kriebel M., Volkmer H., Richter-Levin G. Stress modulation of hippocampal activity-spotlight on the dentate gyrus. Neurobiol. Learn. Mem. 2014, 10.1016/j.nlm.2014.04.008.
18. Finsterwald C., Alberini C.M. Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: from adaptive responses to psychopathologies. Neurobiol. Learn. Mem. 2014, 112:17-29.
19. Foster T.C., Dumas T.C. Mechanism for increased hippocampal synaptic strength following differential experience. J. Neurophysiol. 2001, 85:1377-1383.
20. Foster T.C., Gagne J., Massicotte G. Mechanism of altered synaptic strength due to experience: relation to long-term potentiation. Brain Res. 1996, 736:243-250.
21. Fox C., Merali Z., Harrison C. Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav. Brain Res. 2006, 175:1-8.
22. Frick K.M., Benoit J.D. Use it or lose it: environmental enrichment as a means to promote successful cognitive aging. ScientificWorldJournal 2010, 10:1129-1141.
23. Frick K.M., Fernandez S.M. Enrichment enhances spatial memory and increases synaptophysin levels in aged female mice. Neurobiol. Aging 2003, 24:615-626.
24. Frick K.M., Stearns N., Pan J., Berger-Sweeney J. Effects of environmental enrichment on spatial memory and neurochemistry in middle-aged mice. Learn. Mem. 2003, 10:187-198.
25. Gabrieli J.D. Cognitive neuroscience of human memory. Annu. Rev. Psychol. 1998, 49:87-115.
26. Garrido P. Aging and stress: past hypotheses, present approaches and perspectives. Aging Dis. 2011, 2:80-99.
27. Gundersen H.J., Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 1992, 147:229-263.
28. Harati H., Majchrzak M., Cosquer B., Galani R., Kelche C., Cassel J.C., Barbelivien A. Attention and memory in aged rats: impact of lifelong environmental enrichment. Neurobiol. Aging 2011, 32:718-736.
29. Harris A.P., D'Eath R.B., Healy S.D. Environmental enrichment enhances spatial cognition in rats by reducing thigmotaxis (wall hugging) during the testing. Anim. Behav. 2009, 77:459-464.
30. Hawley D.F., Morch K., Christie B.R., Leasure J.L. Differential response of hippocampal subregions to stress and learning. PLoS One 2012, 7:e53126.
31. Hilfiker S., Pieribone V.A., Czernik A.J., Kao H.T., Augustine G.J., Greengard P. Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. B 1999, 354:269-279.
32. Issa A.M., Rowe W., Gauthier S., Meaney M.J. Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J. Neurosci. 1990, 10:3247-3254.
33. Jovanovic J.N., Czernik A.J., Fienberg A.A., Greengard P., Sihra T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci. 2000, 3:323-329.
34. Kheirbek M.A., Drew L.J., Burghardt N.S., Constantini D.O., Tannenholz L., Ahmari S.E., Zeng H., Fenton A.A., Hen R. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 2013, 77:955-968.
35. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 2002, 3:453-462.
36. Klencklen G., Després O., Dufour A. What do we know about aging and spatial cognition? Reviews and perspectives. Ageing Res. Rev. 2012, 11:123-135.
37. Larsson F., Winblad B., Mohammed A.H. Psychological stress and environmental adaptation in enriched vs. impoverished housed rats. Pharmacol. Biochem. Behav. 2002, 73:193-207.
38. Leal-Galicia P., Castañeda-Bueno M., Quiroz-Baez R., Arias C. Long-term exposure to environmental enrichment since youth prevents recognition memory decline and increases synaptic plasticity markers in aging. Neurobiol. Learn. Mem. 2008, 90:511-518.
39. Leggio M.G., Mandolesi L., Federico F., Spirito F., Ricci B., Gelfo F., Petrosini L. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav. Brain Res. 2005, 163:78-90.
40. Lupien S., Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without you. Behav. Brain Res. 2001, 127:137-158.
41. Lupien S., McEwen B., Gunnar M., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 2009, 10:434-445.
42. Mizoguchi K., Ikeda R., Shoji H., Tanaka Y., Maruyama W., Tabira T. Aging attenuated glucocorticoid negative feedback in the rat brain. Neuroscience 2009, 159:259-270.
43. Moffat S.D., Zonderman A.B., Resnick S.M. Age differences in spatial memory in a virtual environment navigation task. Neurobiol. Aging 2001, 22:787-796.
44. Nithianantharajah J., Hannan A. Enriched environments, experience dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 2006, 7:697-709.
45. O'Mara S., Commins S., Anderson M., Gigg J. The subiculum: a review of form, physiology and function. Prog. Neurobiol. 2001, 64:129-155.
46. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates-The New Coronal Set 2005, Elsevier Academic Press, London. 5th ed.
47. Pedersen W.A., Wan R., Mattson M.P. Impact of aging on stress-responsive neuroendocrine systems. Mech. Ageing Dev. 2001, 122:963-983.
48. Petralia R., Mattson M., Yao P. Communication breakdown: the impact of ageing on synapse structure. Ageing Res. Rev. 2014, 14:31-42.
49. Petrosini L., De Bartolo P., Foti F., Gelfo F., Cutuli D., Leggio M.G., Mandolesi L. On whether the environmental enrichment may provide cognitive and brain reserves. Brain Res. Rev. 2009, 61:221-239.
50. Pham T.M., Winblad B., Granholm A.C., Mohammed A.H. Environmental influences on brain neurotrophins in rats. Pharmacol. Biochem. Behav. 2002, 73:167-175.
51. Potvin O., Doré F.Y., Goulet S. Contributions of the dorsal hippocampus and the dorsal subiculum to processing of idiothetic information and spatial memory. Neurobiol. Learn. Mem. 2007, 87:669-678.
52. Revest J.M., Kaouane N., Mondin M., Le Roux A., Rougé-Pont F., Vallée M., Barik J., Tronche F., Desmedt A., Piazza P.V. The enhancement of stress-related memory by glucocorticoids depends on synapsin-Ia/Ib. Mol. Psychiatry 2010, 15:1140-1151.
53. Rizzuto D., Fratiglioni L. Lifestyle factors related to mortality and survival: a mini-review. Gerontology 2014, 60:1-9.
54. Rolls E.T. A quantitative theory of the functions of the hippocampal CA3 network in memory. Front. Cell. Neurosci. 2013, 7:1-24.
55. Roozendaal B. Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 2000, 25:213-238.
56. Sale A., Berardi N., Maffei L. Environment and brain plasticity: towards an endogenous pharmacotherapy. Physiol. Rev. 2014, 94:189-234.
57. Sampedro-Piquero P., Begega A., Zancada-Menendez C., Cuesta M., Arias J.L. Age-dependent effects of environmental enrichment on brain networks and spatial memory in Wistar rats. Neuroscience 2013, 248:43-53.
58. Sampedro-Piquero P., De Bartolo P., Petrosini L., Zancada-Menendez C., Arias J.L., Begega A. Astrocytic plasticity as a possible mediator of the cognitive improvements after environmental enrichment in aged rats. Neurobiol. Learn. Mem. 2014, 114:16-25.
59. Sandi C. Glucocorticoids act on glutamatergic pathways to affect memory processes. Trends Neurosci. 2011, 34:165-176.
60. Sandi C., Pinelo-Nava M.T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast. 2007, 10.1155/2007/78970.
61. Sapolsky R.M. Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp. Neurol. 1999, 34:721-732.
62. Scarmeas N., Stern Y. Cognitive reserve and lifestyle. J. Clin. Exp. Neuropsychol. 2003, 25:625-633.
63. Segovia G., Del Arco A., Garrido P., de Blas M., Mora F. Environmental enrichment reduces the response to stress of the cholinergic system in the prefrontal cortex during aging. Neurochem. Int. 2008, 52:1198-1203.
64. Simpson J., Kelly J. The impact of environmental enrichment in laboratory rats-behavioural and neurochemical aspects. Behav. Brain Res. 2011, 222:246-264.
65. Sindi S., Fiocco A., Juster R., Pruessner J., Lupien S. When we test, do we stress? Impact of the testing environment on cortisol secretion and memory performance in older adults. Psychoneuroendocrinology 2013, 38:1388-1396.
66. Slomianka L., West M. Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 2005, 136:757-767.
67. Soffié M., Hahn K., Terao E., Eclancher F. Behavioural and glial changes in old rats following environmental enrichment. Behav. Brain Res. 1999, 101:37-49.
68. Speisman R.B., Kumar A., Rani A., Pastoriza J.M., Severance J.E., Foster T.C., Ormerod B.K. Environmental enrichment restores neurogenesis and rapid acquisition in aged rats. Neurobiol. Aging 2013, 34:263-274.
69. Squire L.R. Memory systems of the brain: a brief history and current perspective. Neurobiol. Learn. Mem. 2004, 82:171-177.
70. Ulrich-Lai Y.M., Ryan K.K. PPARγ and stress: implications for aging. Exp. Gerontol. 2013, 48:671-676.
71. Warren J.M., Zerweck C., Anthony A. Effects of environmental enrichment on old mice. Dev. Psychobiol. 1982, 15:13-18.
72. Zahodne L.B., Nowinski C.J., Gershon R.C., Manly J.J. Which psychosocial factors best predict cognitive performance in older adults?. J. Int. Neuropsychol. Soc. 2014, 31:1-9.
73. Zimmerman A., Stauffacher M., Langhans W., Würbel H. Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behav. Brain Res. 2001, 121:11-20.