Short-term environmental enrichment enhances adult neurogenesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Beauquis, Juan ^a   Roig, Paulina ^a   de Nicola, Alejandro F ^a,b   Saravia, Flavia ^a,b  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; HIPPOCAMPUS; HUMIDITY; IMMUNOHISTOCHEMISTRY; INSULIN DEPENDENT DIABETES MELLITUS; LEARNING; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PYRAMIDAL NERVE CELL; TEMPERATURE; ANIMAL; ANIMAL HOUSING; C57BL MOUSE; DENDRITIC SPINE; HIPPOCAMPAL CA1 REGION; NERVE CELL; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; STANDARD; TIME; VASCULARIZATION;

ANIMALIA; MUS;

ANIMALS; ANIMALS, NEWBORN; CA1 REGION, HIPPOCAMPAL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DENDRITIC SPINES; DENTATE GYRUS; DIABETES MELLITUS, TYPE 1; HOUSING, ANIMAL; MALE; MICE; MICE, INBRED C57BL; NEUROGENESIS; NEURONS; PYRAMIDAL CELLS; TIME FACTORS;

EID: 78649725008     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013993     Document Type: Article

References (74)

1. Biessels GJ, Gispen WH (2005) The impact of diabetes on cognition: what can be learned from rodent models? Neurobiol Aging 26 Suppl 1: 36-41.
2. McCall A (1992) The impact of diabetes on the CNS. Diabetes 41: 557-570.
3. Kamal A, Biessels GJ, Urban I, Gispen WH (1999) Hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing. Neuroscience 90: 737-745.
4. Magariños A, McEwen B (2000) Experimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress. Proc Natl Acad Sci USA 97: 11056-11061.
5. Saravia F, Revsin Y, Gonzalez-Deniselle MS, Roig P, Lima A, et al. (2002) Increased astrocyte reactivity in the hippocampus of murine models of type 1 diabetes: the nonobese diabetic (NOD) and streptozotocin-treated mice. Brain Research 957: 345-353.
6. Biessels GJ, Kamal A, Urban IJ, Spruijt BM, Erkelens DW, et al. (1998) Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effects of insulin treatment. Brain Res 800: 125-135.
7. Beauquis J, Homo-Delarche F, Giroix MH, Ehses J, Coulaud J, et al. (2010) Hippocampal neurovascular and hypothalamic-pituitary-adrenal axis alterations in spontaneously type 2 diabetic GK rats. Exp Neurol 222: 125-134.
8. Biessels GJ, Kamal A, Ramakers GM, Urban IJ, Spruijt BM, et al. (1996) Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 45: 1259-1266.
9. Beauquis J, Saravia F, Coulaud J, Roig P, Dardenne M, et al. (2008) Prominently decreased hippocampal neurogenesis in a spontaneous modelof type 1 diabetes, the nonobese diabetic mouse. Exp Neurol 210: 359-367.
10. Jackson-Guilford J, Leander J, Nisenbaum L (2000) The effect of streptozotocininduced diabetes on cell proliferation in the rat dentate gyrus. Neurosc Letters 293: 91-94.
11. Zhang WJ, Tan YF, Yue JT, Vranic M, Wojtowicz JM (2008) Impairment ofhippocampal neurogenesis in streptozotocin-treated diabetic rats. Acta Neurol Scand 117: 205-210.
12. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033.
13. Gould E, McEwen B, Tanapat P, Galea E, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress andNMDA receptor activation. J of Neuroscience 17: 2492-2498.
14. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 100: 13632-13637.
15. Shors T, Townsend DA, Zhao M, Kozorovitskiy, Gould E (2002) Neurogenesismay relate to some but not all types of hippocampal-dependent learning. Hippocampus 12: 578-584.
16. Eriksson PS, Wallin L (2004) Functional consequences of stress-related suppression of adult hippocampal neurogenesis - a novel hypothesis on the neurobiology of burnout. Acta Neurol Scand 110: 275-280.
17. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425: 479-494.
18. Piatti VC, Esposito MS, Schinder AF (2006) The timing of neuronaldevelopment in adult hippocampal neurogenesis. Neuroscientist 12: 463-468.
19. Mankovsky BN, Metzger BE, Molitch ME, Biller J (1996) Cerebrovascular disorders in patients with diabetes mellitus. J Diabetes Complications 10: 228-242.
20. Brownlee M (2005) The pathobiology of diabetic complications: a unifyingmechanism. Diabetes 54: 1615-1625.
21. Beauquis J, Roig P, Homo-Delarche F, De Nicola A, Saravia F (2006) Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocininduced diabetic mice: reversion by antidepressant treatment. Eur J Neurosci 23: 1539-1546.
22. Saravia F, Revsin Y, Lux-Lantos V, Beauquis J, Homo-Delarche F, et al. (2004) Oestradiol restores cell proliferation in dentate gyrus and subventricular zone ofstreptozotocin-diabetic mice. Journal of Neuroendocrinology 16: 704-710.
23. Watanabe Y, Gould E, McEwen BS (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588: 341-345.
24. Lolova I (1989) Dendritic changes in the hippocampus of aged rats. Acta Morphol Hung 37: 3-10.
25. Martinez-Tellez R, Gomez-Villalobos MJ, Flores G (2005) Alteration in dendritic morphology of cortical neurons in rats with diabetes mellitus induced by streptozotocin. Brain Res 1048: 108-115.
26. Moser MB, Trommald M, Andersen P (1994) An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci U S A 91: 12673-12675.
27. Kolb B, Cioe J, Comeau W (2008) Contrasting effects of motor and visual spatial learning tasks on dendritic arborization and spine density in rats. Neurobiol Learn Mem.
28. Krech D, Rosenzweig MR, Bennett EL (1962) Relations between chemistry and problem-solving among rats raised in enriched and impoverished environments. J Comp Physiol Psychol 55: 801-807.
29. Hebb DO (1947) The effects of early experience on problem-solving at maturity. Am Psychol 2: 306-307.
30. Bindu B, Alladi PA, Mansooralikhan BM, Srikumar BN, Raju TR, et al. (2007) Short-term exposure to an enriched environment enhances dendritic branching but not brain-derived neurotrophic factor expression in the hippocampus of rats with ventral subicular lesions. Neuroscience 144: 412-423.
31. Wright RL, Conrad CD (2008) Enriched environment prevents chronic stressinduced spatial learning and memory deficits. Behav Brain Res 187: 41-47.
32. Faherty CJ, Kerley D, Smeyne RJ (2003) A Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment. Brain Res Dev BrainRes 141: 55-61.
33. Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52: 135-143.
34. Kempermann G, Kuhn H, Gage F (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495.
35. Lenzen S (2008) The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia 51: 216-226.
36. Gonzalez-Burgos I, Tapia-Arizmendi G, Feria-Velasco A (1992) Golgi method without osmium tetroxide for the study of the central nervous system. Biotech Histochem 67: 288-296.
37. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87: 387-406.
38. Fox C, Merali Z, Harrison C (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175: 1-8.
39. Lehmann A (1974) Atlas Stereotaxique du Cerveau de la Souris. Paris: Editions du Centre National de la Recherche Scientifique.
40. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
41. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, et al. (2010) Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J Neurosci 30: 6635-6645.
42. Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, et al. (2006) Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7: 77.
43. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, et al. (1988) The new stereological tools: disector, fractionator, nucleator and point sampledintercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
44. Gibb R, Kolb B (1998) A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 79: 1-4.
45. van Praag H, Lucero MJ, Yeo GW, Stecker K, Heivand N, et al. (2007) Plantderived flavanol (-) epicatechin enhances angiogenesis and retention of spatial memory in mice. J Neurosci 27: 5869-5878.
46. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, et al. (2008) Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 11: 309-317.
47. Alvarez EO, Beauquis J, Revsin Y, Banzan AM, Roig P, et al. (2009) Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes. Behav Brain Res 198: 224-230.
48. Nitta A, Murai R, Suzuki N, Ito H, Nomoto H, et al. (2002) Diabetic neuropathies in brain are induced by deficiency of BDNF. Neurotoxicol Teratol 24: 695-701.
49. Revsin Y, Rekers NV, Louwe MC, Saravia FE, De Nicola AF, et al. (2009) Glucocorticoid receptor blockade normalizes hippocampal alterations and cognitive impairment in streptozotocin-induced type 1 diabetes mice. Neuropsychopharmacology 34: 747-758.
50. Olson AK, Eadie BD, Ernst C, Christie BR (2006) Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16: 250-260.
51. Nithianantharajah J, Hannan AJ (2006) Enriched environments, experiencedependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7: 697-709.
52. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18: 3206-3212.
53. Jankowsky JL, Melnikova T, Fadale DJ, Xu GM, Slunt HH, et al. (2005) Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J Neurosci 25: 5217-5224.
54. Costa DA, Cracchiolo JR, Bachstetter AD, Hughes TF, Bales KR, et al. (2007) Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol Aging 28: 831-844.
55. Will BE, Rosenzweig MR, Bennett EL (1976) Effects of differential environments on recovery from neonatal brain lesions, measured by problem-solving scores and brain dimensions. Physiol Behav 16: 603-611.
56. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, et al. (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21: 1-14.
57. Llorens-Martin M, Torres-Aleman I, Trejo JL (2006) Pronounced individual variation in the response to the stimulatory action of exercise on immature hippocampal neurons. Hippocampus 16: 480-490.
58. Saravia F, Beauquis J, Pietranera L, De Nicola AF (2007) Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice. Psychoneuroendocrinology 32: 480-492.
59. Oomen CA, Mayer JL, de Kloet ER, Joels M, Lucassen PJ (2007) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci 26: 3395-3401.
60. Kuczewski N, Porcher C, Lessmann V, Medina I, Gaiarsa JL (2009) Activitydependent dendritic release of BDNF and biological consequences. Mol Neurobiol 39: 37-49.
61. Zacchigna S, Lambrechts D, Carmeliet P (2008) Neurovascular signalling defects in neurodegeneration. Nat Rev Neurosci 9: 169-181.
62. Hattiangady B, Shetty AK (2008) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol Aging 29: 129-147.
63. Sirevaag AM, Black JE, Shafron D, Greenough WT (1988) Direct evidence that complex experience increases capillary branching and surface area in visual cortex of young rats. Brain Res 471: 299-304.
64. Ekstrand J, Hellsten J, Tingstrom A (2008) Environmental enrichment, exercise and corticosterone affect endothelial cell proliferation in adult rat hippocampus and prefrontal cortex. Neurosci Lett 442: 203-207.
65. During MJ, Cao L (2006) VEGF, a mediator of the effect of experience on hippocampal neurogenesis. Curr Alzheimer Res 3: 29-33.
66. Liu LP, Hong H, Liao JM, Wang TS, Wu J, et al. (2009) Upregulation of RAGE at the blood-brain barrier in streptozotocin-induced diabetic mice. Synapse 63: 636-642.
67. Takeda S, Sato N, Uchio-Yamada K, Sawada K, Kunieda T, et al. (2010) Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc Natl Acad Sci U S A 107: 7036-7041.
68. Revsin Y, Saravia F, Roig P, Lima A, de Kloet ER, et al. (2005) Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes. Brain Research 1038: 22-31.
69. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96: 13427-13431.
70. Reisi P, Babri S, Alaei H, Sharifi MR, Mohaddes G, et al. (2008) Effects of treadmill running on short-term pre-synaptic plasticity at dentate gyrus of streptozotocin-induced diabetic rats. Brain Res 1211: 30-36.
71. De Nicola AF, Pietranera L, Beauquis J, Ferrini MG, Saravia FE (2008) Steroid protection in aging and age-associated diseases. Exp Gerontol 44: 34-40.
72. Kuhad A, Chopra K (2007) Curcumin attenuates diabetic encephalopathy in rats: behavioral and biochemical evidences. Eur J Pharmacol 576: 34-42.
73. Tuzcu M, Baydas G (2006) Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur J Pharmacol 537: 106-110.
74. Fernandez CI, Collazo J, Bauza Y, Castellanos MR, Lopez O (2004) Environmental enrichment-behavior-oxidative stress interactions in the aged rat: issues for a therapeutic approach in human aging. Ann N Y Acad Sci 1019:53-57.