Environmental enrichment increases doublecortin-associated new neurons and decreases neuronal death without modifying anxiety-like behavior in mice chronically exposed to toluene

Behavioural Brain Research

Volumn 256, Issue , 2013, Pages 432-440

  Paez Martinez, Nayeli ^a,b   Flores Serrano, Zoraida ^a   Ortiz Lopez, Leonardo ^b   Ramirez Rodriguez, Gerardo ^b  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b INSTITUTO NACIONAL DE PSIQUIATRÍA RAMÓN DE LA FUENTE MUÑIZ   (Mexico)

Author keywords

Anxiety; Doublecortin; Environmental enrichment; Neurogenesis; Neuronal death; Toluene

Indexed keywords

CASPASE 3; DOUBLECORTIN; TOLUENE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ENVIRONMENTAL ENRICHMENT; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LONG TERM EXPOSURE; MALE; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL;

ANXIETY; DOUBLECORTIN; ENVIRONMENTAL ENRICHMENT; NEUROGENESIS; NEURONAL DEATH; TOLUENE;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CELL DEATH; ENVIRONMENT; HIPPOCAMPUS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; TOLUENE;

EID: 84884234615     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.09.007     Document Type: Article

References (51)

1. Balster R.L., Cruz S.L., Howard M.O., Dell C.A., Cottler L.B. Classification of abused inhalants. Addiction 2009, 104(6):878-882.
2. Cruz S.L. The latest evidence in the neuroscience of solvent misuse: an article written for service providers. Subst Use Misuse 2011, 46(Suppl. 1):62-67.
3. Dell C.A., Gust S.W., MacLean S. Global issues in volatile substance misuse. Subst Use Misuse 2011, 46(Suppl. 1):1-7.
4. Hefner K., Holmes A. Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav Brain Res 2007, 176(2):210-215.
5. Howard M.O., Perron B.E., Sacco P., Ilgen M., Vaughn M.G., Garland E., et al. Suicide ideation and attempts among inhalant users: results from the national epidemiologic survey on alcohol and related conditions. Suicide Life Threat Behav 2010, 40(3):276-286.
6. Perron B.E., Vaughn M.G., Howard M.O. Reasons for using inhalants: evidence for discrete classes in a sample of incarcerated adolescents. J Subst Abuse Treat 2008, 34(4):450-455.
7. Wu L.T., Howard M.O. Psychiatric disorders in inhalant users: results from the National Epidemiologic Survey on alcohol and related conditions. Drug Alcohol Depend 2007, 88(2-3):146-155.
8. Gospe S.M., Zhou S.S. Prenatal exposure to toluene results in abnormal neurogenesis and migration in rat somatosensory cortex. Pediatr Res 2000, 47(3):362-368.
9. Seo H.S., Yang M., Song M.S., Kim J.S., Kim S.H., Kim J.C., et al. Toluene inhibits hippocampal neurogenesis in adult mice. Pharmacol Biochem Behav 2010, 94(4):588-594.
10. Dalgaard M., Hossaini A., Hougaard K.S., Hass U., Ladefoged O. Developmental toxicity of toluene in male rats: effects on semen quality, testis morphology, and apoptotic neurodegeneration. Arch Toxicol 2001, 75(2):103-109.
11. El-Nabi Kamel M.A., Shehata M. Effect of toluene exposure on the antioxidant status and apoptotic pathway in organs of the rat. Br J Biomed Sci 2008, 65(2):75-79.
12. Korbo L., Ladefoged O., Lam H.R., Ostergaard G., West M.J., Arlien-Soborg P. Neuronal loss in hippocampus in rats exposed to toluene. Neurotoxicology 1996, 17(2):359-366.
13. Howard M.O., Bowen S.E., Garland E.L., Perron B.E., Vaughn M.G. Inhalant use and inhalant use disorders in the United States. Addict Sci Clin Pract 2011, 6(1):18-31.
14. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386(6624):493-495.
15. Nithianantharajah J., Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 2006, 7(9):697-709.
16. van P.H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000, 1(3):191-198.
17. Benaroya-Milshtein N., Hollander N., Apter A., Kukulansky T., Raz N., Wilf A., et al. Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur J Neurosci 2004, 20(5):1341-1347.
18. Fox C., Merali Z., Harrison C. Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 2006, 175(1):1-8.
19. Leal-Galicia P., Saldivar-Gonzalez A., Morimoto S., Arias C. Exposure to environmental enrichment elicits differential hippocampal cell proliferation: role of individual responsiveness to anxiety. Dev Neurobiol 2007, 67(4):395-405.
20. Sztainberg Y., Kuperman Y., Tsoory M., Lebow M., Chen A. The anxiolytic effect of environmental enrichment is mediated via amygdalar CRF receptor type 1. Mol Psychiatry 2010, 15(9):905-917.
21. Faherty C.J., Raviie S.K., Herasimtschuk A., Smeyne R.J. Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res 2005, 134(1):170-179.
22. Young D., Lawlor P.A., Leone P., Dragunow M., During M.J. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med 1999, 5(4):448-453.
23. Nelson G. Controlled Test Atmospheres: Principles and Techniques 1971, Ann Arbor Science Publishers.
24. Cruz S.L., Gauthereau M.Y., Camacho-Munoz C., Lopez-Rubalcava C., Balster R.L. Effects of inhaled toluene and 1,1,1-trichloroethane on seizures and death produced by N-methyl-d-aspartic acid in mice. Behav Brain Res 2003, 140(1-2):195-202.
25. Bowen S.E., Batis J.C., Paez-Martinez N., Cruz S.L. The last decade of solvent research in animal models of abuse: mechanistic and behavioral studies. Neurotoxicol Teratol 2006, 28(6):636-647.
26. Treit D., Pinel J.P., Fibiger H.C. Conditioned defensive burying: a new paradigm for the study of anxiolytic agents. Pharmacol Biochem Behav 1981, 15(4):619-626.
27. Ramirez-Rodriguez G., Klempin F., Babu H., Benitez-King G., Kempermann G. Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 2009, 34(9):2180-2191.
28. Ramirez-Rodriguez G., Ortiz-Lopez L., Dominguez-Alonso A., Benitez-King G.A., Kempermann G. Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J Pineal Res 2011, 50(1):29-37.
29. Kempermann G., Gast D., Kronenberg G., Yamaguchi M., Gage F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003, 130(2):391-399.
30. Plumpe T., Ehninger D., Steiner B., Klempin F., Jessberger S., Brandt M., et al. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 2006, 7:77.
31. Bamat N.A., Brunelli S.A., Kron M.M., Schulte A.R., Zimmerberg B. Behavioral effects of toluene in rats selectively bred for infantile vocalization rate. Neurotoxicol Teratol 2005, 27(6):883-890.
32. Bowen S.E., Wiley J.L., Balster R.L. The effects of abused inhalants on mouse behavior in an elevated plus-maze. Eur J Pharmacol 1996, 312(2):131-136.
33. Paez-Martinez N., Cruz S.L., Lopez-Rubalcava C. Comparative study of the effects of toluene, benzene, 1,1,1-trichloroethane, diethyl ether, and flurothyl on anxiety and nociception in mice. Toxicol Appl Pharmacol 2003, 193(1):9-16.
34. Batis J.C., Hannigan J.H., Bowen S.E. Differential effects of inhaled toluene on locomotor activity in adolescent and adult rats. Pharmacol Biochem Behav 2010, 96(4):438-448.
35. O'Leary-Moore S.K., Galloway M.P., McMechan A.P., Irtenkauf S., Hannigan J.H., Bowen S.E. Neurochemical changes after acute binge toluene inhalation in adolescent and adult rats: a high-resolution magnetic resonance spectroscopy study. Neurotoxicol Teratol 2009, 31(6):382-389.
36. Wilking J.A., Hesterberg K.G., Nguyen V.H., Cyboron A.P., Hua A.Y., Stitzel J.A. Comparison of nicotine oral consumption and baseline anxiety measures in adolescent and adult C57BL/6J and C3H/Ibg mice. Behav Brain Res 2012, 233(2):280-287.
37. Beasley T.E., Evansky P.A., Bushnell P.J. Behavioral effects of sub-acute inhalation of toluene in adult rats. Neurotoxicol Teratol 2012, 34(1):83-89.
38. Bale A.S., Tu Y., Carpenter-Hyland E.P., Chandler L.J., Woodward J.J. Alterations in glutamatergic and gabaergic ion channel activity in hippocampal neurons following exposure to the abused inhalant toluene. Neuroscience 2005, 130(1):197-206.
39. Hsieh G.C., Sharma R.P., Parker R.D. Hypothalamic-pituitary-adrenocortical axis activity and immune function after oral exposure to benzene and toluene. Immunopharmacology 1991, 21(1):23-31.
40. Fuss J., Ben Abdallah N.M., Vogt M.A., Touma C., Pacifici P.G., Palme R., et al. Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 2010, 20(3):364-376.
41. Green T.A., Alibhai I.N., Roybal C.N., Winstanley C.A., Theobald D.E., Birnbaum S.G., et al. Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biol Psychiatry 2010, 67(1):28-35.
42. Pritchard L.M., Van Kempen T.A., Zimmerberg B. Behavioral effects of repeated handling differ in rats reared in social isolation and environmental enrichment. Neurosci Lett 2013, 536:47-51.
43. van de Weerd H.A., Baumans V., Koolhaas J.M., van Zutphen L.F. Strain specific behavioural response to environmental enrichment in the mouse. J Exp Anim Sci 1994, 36(4-5):117-127.
44. Burghardt P.R., Fulk L.J., Hand G.A., Wilson M.A. The effects of chronic treadmill and wheel running on behavior in rats. Brain Res 2004, 1019(1-2):84-96.
45. Revest J.M., Dupret D., Koehl M., Funk-Reiter C., Grosjean N., Piazza P.V., et al. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 2009, 14(10):959-967.
46. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., et al. Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 2004, 28(3):273-283.
47. Moser E.I. Learning-related changes in hippocampal field potentials. Behav Brain Res 1995, 71(1-2):11-18.
48. Piatti V.C., Davies-Sala M.G., Esposito M.S., Mongiat L.A., Trinchero M.F., Schinder A.F. The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci 2011, 31(21):7715-7728.
49. Filley C.M., Halliday W., Kleinschmidt-DeMasters B.K. The effects of toluene on the central nervous system. J Neuropathol Exp Neurol 2004, 63(1):1-12.
50. Solinas M., Thiriet N., Chauvet C., Jaber M. Prevention and treatment of drug addiction by environmental enrichment. Prog Neurobiol 2010, 92(4):572-592.
51. Simpson J., Kelly J.P. The impact of environmental enrichment in laboratory rats-behavioural and neurochemical aspects. Behav Brain Res 2011, 222(1):246-264.