Increased adult hippocampal neurogenesis is not necessary for wheel running to abolish conditioned place preference for cocaine in mice

European Journal of Neuroscience

Volumn 41, Issue 2, 2015, Pages 216-226

  Mustroph, M L ^a   Merritt, J R ^a   Holloway, A L ^a   Pinardo, H ^a   Miller, D S ^a   Kilby, C N ^a   Bucko, P ^a   Wyer, A ^a   Rhodes, J S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Conditioned place preference; Exercise; Nestin; Thymidine kinase; Valganciclovir

Indexed keywords

BROXURIDINE; COCAINE; VALGANCICLOVIR; AGENTS AFFECTING CELL DIVISION; DOPAMINE UPTAKE INHIBITOR; GANCICLOVIR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PLACE PREFERENCE; RUNNING; TRANSGENIC MOUSE; TREADMILL; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL FOOD; BODY WEIGHT; C57BL MOUSE; CONDITIONING; DRUG EFFECTS; DRUG SEEKING BEHAVIOR; IMMUNOHISTOCHEMISTRY; PHYSIOLOGY; REINFORCEMENT; SPATIAL LEARNING;

ANIMAL FEED; ANIMALS; APOPTOSIS; BODY WEIGHT; BROMODEOXYURIDINE; COCAINE; CONDITIONING (PSYCHOLOGY); DENTATE GYRUS; DOPAMINE UPTAKE INHIBITORS; DRUG-SEEKING BEHAVIOR; EXTINCTION, PSYCHOLOGICAL; GANCICLOVIR; IMMUNOHISTOCHEMISTRY; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOSIS MODULATORS; NEUROGENESIS; RUNNING; SPATIAL LEARNING;

EID: 84921061978     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12782     Document Type: Article

References (73)

1. Ames, S.L., Grenard, J.L., He, Q., Stacy, A.W., Wong, S.W., Xiao, L., Xue, G. & Bechara, A. (2013) Functional imaging of an alcohol-Implicit Association Test (IAT). Addict. Biol., 19, 467-481.
2. Blaiss, C.A., Yu, T.S., Zhang, G., Chen, J., Dimchev, G., Parada, L.F., Powell, C.M. & Kernie, S.G. (2011) Temporally specified genetic ablation of neurogenesis impairs cognitive recovery after traumatic brain injury. J. Neurosci., 31, 4906-4916.
3. Bothe, N., Zschucke, E., Dimeo, F., Heinz, A., Wustenberg, T. & Strohle, A. (2013) Acute exercise influences reward processing in highly trained and untrained men. Med. Sci. Sport. Exer., 45, 583-591.
4. Brown, R.A., Abrantes, A.M., Read, J.P., Marcus, B.H., Jakicic, J., Strong, D.R., Oakley, J.R., Ramsey, S.E., Kahler, C.W., Stuart, G.G., Dubreuil, M.E. & Gordon, A.A. (2010) A pilot study of aerobic exercise as an adjunctive treatment for drug dependence. Ment. Health Phys. Act, 3, 27-34.
5. Carro, E., Trejo, J.L., Busiguina, S. & Torres-Aleman, I. (2001) Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. J. Neurosci., 21, 5678-5684.
6. Chauvet, C., Lardeux, V., Jaber, M. & Solinas, M. (2011) Brain regions associated with the reversal of cocaine conditioned place preference by environmental enrichment. Neuroscience, 184, 88-96.
7. Cho, Y.H., Friedman, E. & Silva, A.J. (1999) Ibotenate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice. Behav. Brain Res., 98, 77-87.
8. Clark, P.J., Brzezinska, W.J., Thomas, M.W., Ryzhenko, N.A., Toshkov, S.A. & Rhodes, J.S. (2008) Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience, 155, 1048-1058.
9. Clark, P.J., Brzezinska, W.J., Puchalski, E.K., Krone, D.A. & Rhodes, J.S. (2009) Functional analysis of neurovascular adaptations to exercise in the dentate gyrus of young adult mice associated with cognitive gain. Hippocampus, 19, 937-950.
10. Clark, P.J., Bhattacharya, T.K., Miller, D.S. & Rhodes, J.S. (2011) Induction of c-Fos, Zif268, and Arc from acute bouts of voluntary wheel running in new and pre-existing adult mouse hippocampal granule neurons. Neuroscience, 184, 16-27.
11. Clelland, C.D., Choi, M., Romberg, C., Clemenson, G.D. Jr., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L.M., Barker, R.A., Gage, F.H. & Bussey, T.J. (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science, 325, 210-213.
12. Colcombe, S. & Kramer, A.F. (2003) Fitness effects on the cognitive function of older adults: a meta-analytic study. Psychol. Sci., 14, 125-130.
13. Creer, D.J., Romberg, C., Saksida, L.M., van Praag, H. & Bussey, T.J. (2010) Running enhances spatial pattern separation in mice. Proc. Natl. Acad. Sci. USA, 107, 2367-2372.
14. Cunningham, C.L., Gremel, C.M. & Groblewski, P.A. (2006) Drug-induced conditioned place preference and aversion in mice. Nat. Protoc., 1, 1662-1670.
15. De Chiara, V., Errico, F., Musella, A., Rossi, S., Mataluni, G., Sacchetti, L., Siracusano, A., Castelli, M., Cavasinni, F., Bernardi, G., Usiello, A. & Centonze, D. (2010) Voluntary exercise and sucrose consumption enhance cannabinoid CB1 receptor sensitivity in the striatum. Neuropsychopharmacology, 35, 374-387.
16. Dietrich, M.O., Andrews, Z.B. & Horvath, T.L. (2008) Exercise-induced synaptogenesis in the hippocampus is dependent on UCP2-regulated mitochondrial adaptation. J. Neurosci., 28, 10766-10771.
17. Doetsch, F., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. (1999) Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. USA, 96, 11619-11624.
18. Drew, M.R., Denny, C.A. & Hen, R. (2010) Arrest of adult hippocampal neurogenesis in mice impairs single- but not multiple-trial contextual fear conditioning. Behav. Neurosci., 124, 446-454.
19. Dupret, D., Revest, J.M., Koehl, M., Ichas, F., De Giorgi, F., Costet, P., Abrous, D.N. & Piazza, P.V. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS One, 3, e1959.
20. Eadie, B.D., Redila, V.A. & Christie, B.R. (2005) Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J. Comp. Neurol., 486, 39-47.
21. Everitt, B.J. & Robbins, T.W. (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci., 8, 1481-1489.
22. Evero, N., Hackett, L.C., Clark, R.D., Phelan, S. & Hagobian, T.A. (2012) Aerobic exercise reduces neuronal responses in food reward brain regions. J. Appl. Physiol., 112, 1612-1619.
23. Ferreira-Vieira, T.H., Bastos, C.P., Pereira, G.S., Moreira, F.A. & Massensini, A.R. (2014) A role for the endocannabinoid system in exercise-induced spatial memory enhancement in mice. Hippocampus, 24, 79-88.
24. Fontes-Ribeiro, C.A., Marques, E., Pereira, F.C., Silva, A.P. & Macedo, T.R. (2011) May exercise prevent addiction? Curr. Neuropharmacol., 9, 45-48.
25. Garthe, A., Behr, J. & Kempermann, G. (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One, 4, e5464.
26. Gomez-Pinilla, F., Vaynman, S. & Ying, Z. (2008) Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur. J. Neurosci., 28, 2278-2287.
27. Griffin, E.W., Bechara, R.G., Birch, A.M. & Kelly, A.M. (2009) Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus, 19, 973-980.
28. Groves, J.O., Leslie, I., Huang, G.J., McHugh, S.B., Taylor, A., Mott, R., Munafo, M., Bannerman, D.M. & Flint, J. (2013) Ablating adult neurogenesis in the rat has no effect on spatial processing: evidence from a novel pharmacogenetic model. PLoS Genet., 9, e1003718.
29. Hernandez-Rabaza, V., Hontecillas-Prieto, L., Velazquez-Sanchez, C., Ferragud, A., Perez-Villaba, A., Arcusa, A., Barcia, J.A., Trejo, J.L. & Canales, J.J. (2008) The hippocampal dentate gyrus is essential for generating contextual memories of fear and drug-induced reward. Neurobiol. Learn. Mem., 90, 553-559.
30. Hernández-Rabaza, V., Llorens-Martín, M., Velázquez-Sánchez, C., Ferragud, A., Arcusa, A., Gumus, H.G., Gómez-Pinedo, U., Pérez-Villalba, A., Roselló, J., Trejo, J.L., Barcia, J.A. & Canalesa, J.J. (2009) Inhibition of adult hippocampal neurogenesis disrupts contextual learning but spares spatial working memory, long-term conditional rule retention and spatial reversal. Neuroscience, 159, 59-68.
31. Heyman, E., Gamelin, F.X., Goekint, M., Piscitelli, F., Roelands, B., Leclair, E., Di Marzo, V. & Meeusen, R. (2012) Intense exercise increases circulating endocannabinoid and BDNF levels in humans - possible implications for reward and depression. Psychoneuroendocrinology, 37, 844-851.
32. Johnson, Z.V., Revis, A.A., Burdick, M.A. & Rhodes, J.S. (2010) A similar pattern of neuronal Fos activation in 10 brain regions following exposure to reward- or aversion-associated contextual cues in mice. Physiol. Behav., 99, 412-418.
33. Jung, D. & Dorr, A. (1999) Single-dose pharmacokinetics of valganciclovir in HIV- and CMV-seropositive subjects. J. Clin. Pharmacol., 39, 800-804.
34. Kim, J.J. & Fanselow, M.S. (1992) Modality-specific retrograde amnesia of fear. Science, 256, 675-677.
35. Koteja, P., Garland, T. Jr., Sax, J.K., Swallow, J.G. & Carter, P.A. (1999) Behaviour of house mice artificially selected for high levels of voluntary wheel running. Anim. Behav., 58, 1307-1318.
36. Lynch, W.J., Peterson, A.B., Sanchez, V., Abel, J. & Smith, M.A. (2013) Exercise as a novel treatment for drug addiction: a neurobiological and stage-dependent hypothesis. Neurosci. Biobehav. R., 37, 1622-1644.
37. Maren, S., Aharonov, G. & Fanselow, M.S. (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res., 88, 261-274.
38. Meyers, R.A., Zavala, A.R. & Neisewander, J.L. (2003) Dorsal, but not ventral, hippocampal lesions disrupt cocaine place conditioning. NeuroReport, 14, 2127-2131.
39. Michaelides, M., Thanos, P.K., Volkow, N.D. & Wang, G.J. (2012) Translational neuroimaging in drug addiction and obesity. ILAR J., 53, 59-68.
40. Mizumatsu, S., Monje, M.L., Morhardt, D.R., Rola, R., Palmer, T.D. & Fike, J.R. (2003) Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res., 63, 4021-4027.
41. Mustroph, M.L., Stobaugh, D.J., Miller, D.S., DeYoung, E.K. & Rhodes, J.S. (2011) Wheel running can accelerate or delay extinction of conditioned place preference for cocaine in male C57BL/6J mice, depending on timing of wheel access. Eur. J. Neurosci., 34, 1161-1169.
42. Nakashiba, T., Young, J.Z., McHugh, T.J., Buhl, D.L. & Tonegawa, S. (2008) Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science, 319, 1260-1264.
43. Neeper, S.A., Gómez-Pinilla, F., Choi, J. & Cotman, C. (1995) Exercise and brain neurotrophins. Nature, 373, 109.
44. Neeper, S.A., Gomez-Pinilla, F., Choi, J. & Cotman, C.W. (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res., 726, 49-56.
45. O'Brien, C.P., Childress, A.R., Ehrman, R. & Robbins, S.J. (1998) Conditioning factors in drug abuse: can they explain compulsion? J. Psychopharmacol., 12, 15-22.
46. O'Callaghan, R.M., Griffin, E.W. & Kelly, A.M. (2009) Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus, 19, 1019-1029.
47. Olsen, C.M. (2011) Natural rewards, neuroplasticity, and non-drug addictions. Neuropharmacology, 61, 1109-1122.
48. Ozburn, A.R., Harris, R.A. & Blednov, Y.A. (2008) Wheel running, voluntary ethanol consumption, and hedonic substitution. Alcohol, 42, 417-424.
49. Pescovitz, M.D., Rabkin, J., Merion, R.M., Paya, C.V., Pirsch, J., Freeman, R.B., O'Grady, J., Robinson, C., To, Z., Wren, K., Banken, L., Buhles, W. & Brown, F. (2000) Valganciclovir results in improved oral absorption of ganciclovir in liver transplant recipients. Antimicrob. Agents Ch., 44, 2811-2815.
50. van Praag, H., Christie, B.R., Sejnowski, T.J. & Gage, F.H. (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA, 96, 13427-13431.
51. Quirk, G.J. & Mueller, D. (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology, 33, 56-72.
52. Raichlen, D.A., Foster, A.D., Seillier, A., Giuffrida, A. & Gerdeman, G.L. (2013) Exercise-induced endocannabinoid signaling is modulated by intensity. Eur. J. Appl. Physiol., 113, 869-875.
53. Rhodes, J.S., Koteja, P., Swallow, J.G., Carter, P.A. & Garland, T. (2000) Body temperatures of house mice artificially selected for high voluntary wheel-running behavior: repeatability and effect of genetic selection. J. Therm. Biol., 25, 391-400.
54. Rhodes, J.S., Garland, T. Jr. & Gammie, S.C. (2003) Patterns of brain activity associated with variation in voluntary wheel-running behavior. Behav. Neurosci., 11, 1243-1256.
55. Rola, R., Raber, J., Rizk, A., Otsuka, S., VandenBerg, S.R., Morhardt, D.R. & Fike, J.R. (2004) Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol., 188, 316-330.
56. Saxe, M.D., Battaglia, F., Wang, J.W., Malleret, G., David, D.J., Monckton, J.E., Garcia, A.D., Sofroniew, M.V., Kandel, E.R., Santarelli, L., Hen, R. & Drew, M.R. (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. USA, 103, 17501-17506.
57. Schloesser, R.J., Manji, H.K. & Martinowich, K. (2009) Suppression of adult neurogenesis leads to an increased hypothalamo-pituitary-adrenal axis response. NeuroReport, 20, 553-557.
58. Scobie, K.N., Hall, B.J., Wilke, S.A., Klemenhagen, K.C., Fujii-Kuriyama, Y., Ghosh, A., Hen, R. & Sahay, A. (2009) Kruppel-like factor 9 is necessary for late-phase neuronal maturation in the developing dentate gyrus and during adult hippocampal neurogenesis. J. Neurosci., 29, 9875-9887.
59. Shapiro, A., Cheng, K.Y., Gao, Y., Seo, D.O., Anton, S., Carter, C.S., Zhang, Y., Tumer, N. & Scarpace, P.J. (2011) The act of voluntary wheel running reverses dietary hyperphagia and increases leptin signaling in ventral tegmental area of aged obese rats. Gerontology, 57, 335-342.
60. Shors, T.J., Townsend, D.A., Zhao, M., Kozorovitskiy, Y. & Gould, E. (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus, 12, 578-584.
61. Singer, B.H., Jutkiewicz, E.M., Fuller, C.L., Lichtenwalner, R.J., Zhang, H., Velander, A.J., Li, X., Gnegy, M.E., Burant, C.F. & Parent, J.M. (2009) Conditional ablation and recovery of forebrain neurogenesis in the mouse. J. Comp. Neurol., 514, 567-582.
62. Sparling, P.B., Giuffrida, A., Piomelli, D., Rosskopf, L. & Dietrich, A. (2003) Exercise activates the endocannabinoid system. NeuroReport, 14, 2209-2211.
63. Thanos, P.K., Tucci, A., Stamos, J., Robison, L., Wang, G.J., Anderson, B.J. & Volkow, N.D. (2010) Chronic forced exercise during adolescence decreases cocaine conditioned place preference in Lewis rats. Behav. Brain Res., 215, 77-82.
64. Tronel, S., Belnoue, L., Grosjean, N., Revest, J.M., Piazza, P.V., Koehl, M. & Abrous, D.N. (2012) Adult-born neurons are necessary for extended contextual discrimination. Hippocampus, 22, 292-298.
65. Volkow, N.D., Wang, G.J., Telang, F., Fowler, J.S., Logan, J., Childress, A.R., Jayne, M., Ma, Y. & Wong, C. (2006) Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J. Neurosci., 26, 6583-6588.
66. Werme, M., Thoren, P., Olson, L. & Brene, S. (2000) Running and cocaine both upregulate dynorphin mRNA in medial caudate putamen. Eur. J. Neurosci., 12, 2967-2974.
67. Wiltgen, B.J., Sanders, M.J., Anagnostaras, S.G., Sage, J.R. & Fanselow, M.S. (2006) Context fear learning in the absence of the hippocampus. J. Neurosci., 26, 5484-5491.
68. Winocur, G., Wojtowicz, J.M., Sekeres, M., Snyder, J.S. & Wang, S. (2006) Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus, 16, 296-304.
69. Wiskott, L., Rasch, M.J. & Kempermann, G. (2006) A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus, 16, 329-343.
70. Yu, T.S., Zhang, G., Liebl, D.J. & Kernie, S.G. (2008) Traumatic brain injury-induced hippocampal neurogenesis requires activation of early nestin-expressing progenitors. J. Neurosci., 28, 12901-12912.
71. Zhang, C.L., Zou, Y., He, W., Gage, F.H. & Evans, R.M. (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature, 451, 1004-1007.
72. Zlebnik, N.E., Hedges, V.L., Carroll, M.E. & Meisel, R.L. (2014) Chronic wheel running affects cocaine-induced c-Fos expression in brain reward areas in rats. Behav. Brain Res., 261, 71-78.
73. Zombeck, J.A., Chen, G.T., Johnson, Z.V., Rosenberg, D.M., Craig, A.B. & Rhodes, J.S. (2008) Neuroanatomical specificity of conditioned responses to cocaine versus food in mice. Physiol. Behav., 93, 637-650.