Cognitive and locomotor/exploratory behavior after chronic exercise in the olfactory bulbectomy animal model of depression

Behavioural Brain Research

Volumn 222, Issue 1, 2011, Pages 106-116

  Van Hoomissen, Jacqueline ^a   Kunrath, Julie ^a   Dentlinger, Renee ^a   Lafrenz, Andrew ^a   Krause, Mark ^a   Azar, Afaf ^a  

^a UNIVERSITY OF PORTLAND   (United States)

Author keywords

Corticosterone; Exercise; Exploratory behavior; Learning; Olfactory bulbectomy; Stress

Indexed keywords

CORTICOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONDITIONING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; EXERCISE; EXPLORATORY BEHAVIOR; FEAR; HYPERACTIVITY; LOCOMOTION; MALE; NONHUMAN; OLFACTORY BULBECTOMY; PRIORITY JOURNAL; RAT; RUNNING;

ANIMALS; BODY WEIGHT; COGNITION; CONDITIONING (PSYCHOLOGY); CORTICOSTERONE; DEPRESSION; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEAR; FREEZING REACTION, CATALEPTIC; LOCOMOTION; MALE; OLFACTORY BULB; PHYSICAL CONDITIONING, ANIMAL; PSYCHOMOTOR PERFORMANCE; RADIOIMMUNOASSAY; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 79953889198     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.03.017     Document Type: Article

References (73)

1. Barbour K.A., Edenfield T.M., Blumenthal J.A. Exercise as a treatment for depression and other psychiatric disorders: a review. J Cardiopulm Rehabil Prev 2007, 27:359-367.
2. Greer T.L., Trivedi M.H. Exercise in the treatment of depression. Curr Psychiatry Rep 2009, 11:466-472.
3. Rethorst C.D., Wipfli B.M., Landers D.M. The antidepressive effects of exercise: a meta-analysis of randomized trials. Sports Med 2009, 39:491-511.
4. Blumenthal J.A., Babyak M.A., Doraiswamy P.M., Watkins L., Hoffman B.M., Barbour K.A., et al. Exercise and pharmacotherapy in the treatment of major depressive disorder. Psychosom Med 2007, 69:587-596.
5. Blumenthal J.A., Babyak M.A., Moore K.A., Craighead W.E., Herman S., Khatri P., et al. Effects of exercise training on older patients with major depression. Arch Intern Med 1999, 159:2349-2356.
6. Dishman R.K., Berthoud H.R., Booth F.W., Cotman C.W., Edgerton V.R., Fleshner M.R., et al. Neurobiology of exercise. Obesity (Silver Spring) 2006, 14:345-356.
7. Kelly J.P., Wrynn A.S., Leonard B.E. The olfactory bulbectomized rat as a model of depression: an update. Pharmacol Ther 1997, 74:299-316.
8. Song C., Leonard B.E. The olfactory bulbectomised rat as a model of depression. Neurosci Biobehav Rev 2005, 29:627-647.
9. Chambliss H.O., Van Hoomissen J.D., Holmes P.V., Bunnell B.N., Dishman R.K. Effects of chronic activity wheel running and imipramine on masculine copulatory behavior after olfactory bulbectomy. Physiol Behav 2004, 82:593-600.
10. Hozumi S., Nakagawasai O., Tan-No K., Niijima F., Yamadera F., Murata A., et al. Characteristics of changes in cholinergic function and impairment of learning and memory-related behavior induced by olfactory bulbectomy. Behav Brain Res 2003, 138:9-15.
11. Jaako-Movits K., Zharkovsky A. Impaired fear memory and decreased hippocampal neurogenesis following olfactory bulbectomy in rats. Eur J Neurosci 2005, 22:2871-2878.
12. Hall R.D., Macrides F. Olfactory bulbectomy impairs the rat's radial-maze behavior. Physiol Behav 1983, 30:797-803.
13. Calcagnetti D.J., Quatrella L.A., Schechter M.D. Olfactory bulbectomy disrupts the expression of cocaine-induced conditioned place preference. Physiol Behav 1996, 59:597-604.
14. Amemori T., Ermakova I.V., Buresová O., Zigová T., Racekova E., Bures J. Brain transplants enhance rather than reduce the impairment of spatial memory and olfaction in bulbectomized rats. Behav Neurosci 1989, 103:61-70.
15. Aleksandrova I.Y., Kuvichkin V.V., Kashparov I.A., Medvinskaya N.I., Nesterova I.V., Lunin S.M., et al. Increased level of beta-amyloid in the brain of bulbectomized mice. Biochemistry (Moscow) 2004, 69:176-180.
16. Moriguchi S., Han F., Nakagawasai O., Tadano T., Fukunaga K. Decreased calcium/calmodulin-dependent protein kinase II and protein kinase C activities mediate impairment of hippocampal long-term potentiation in the olfactory bulbectomized mice. J Neurochem 2006, 97:22-29.
17. van Praag H., Christie B.C., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 1999, 96:13427-13431.
18. Molteni R., Wu A., Vaynman S., Ying Z., Barnard B.J., Gómez-Pinilla F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience 2004, 123:429-440.
19. Fordyce D.E., Wehner J.M. Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase C activity in C57BL/6 and DBA/2 mice. Brain Res 1993, 619:111-119.
20. Fordyce D.E., Farrar R.P. Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behav Brain Res 1991, 46:123-133.
21. Fordyce D.E., Farrar R.P. Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behav Brain Res 1991, 43:115-123.
22. Anderson B.J., Rapp D.N., Baek D.H., McCloskey D.P., Coburn-Litvak P.S., Robinson J.K. Exercise influences spatial learning in the radial arm maze. Physiol Behav 2000, 70:425-429.
23. Cheresharov L., Yonkov D., Toshkova S. Influence of increased motor activity on learning and memory in albino rats. Acta Physiol Pharmacol Bulg 1981, 7:41-46.
24. Radák Z., Kaneko T., Tahara S., Nakamoto H., Pucsok J., Sasvári M., et al. Regular exercise improves cognitive function and decreases oxidative damage in rat brain. Neurochem Int 2001, 38:17-23.
25. Huang F.L., Huang K.P., Wu J., Boucheron C. Environmental enrichment enhances neurogranin expression and hippocampal learning and memory but fails to rescue the impairments of neurogranin null mutant mice. J Neurosci 2006, 26:6230-6237.
26. Eisenstein S.A., Holmes P.V. Chronic and voluntary exercise enhances learning of conditioned place preference to morphine in rats. Pharmacol Biochem Behav 2007, 86:607-615.
27. Van der Borght K., Havekes R., Bos T., Eggen B.J., Van der Zee E.A. Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav Neurosci 2007, 121:324-334.
28. Pang T.Y.C., Stam N.C., Nithianantharajah J., Howard M.L., Hannan A.J. Differential effects of voluntary physical exercise on behavioral and brain-derived neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience 2006, 141:569-584.
29. Baruch D.E., Swain R.A., Helmstetter F.J. Effects of exercise on Pavlovian fear conditioning. Behav Neurosci 2004, 118:1123-1127.
30. Van Hoomissen J.D., Holmes P.V., Zellner A.S., Poudevigne A., Dishman R.K. Effects of beta-adrenoreceptor blockade during chronic exercise on contextual fear conditioning and mRNA for galanin and brain-derived neurotrophic factor. Behav Neurosci 2004, 118:1378-1390.
31. Burghardt P.R., Pasumarthi R.K., Wilson M.A., Fadel J. Alterations in fear conditioning and amygdalar activation following chronic wheel running in rats. Pharmacol Biochem Behav 2006, 84:306-312.
32. Fanselow M.S. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 2000, 110:73-81.
33. Vinkers C.H., Breuer M.E., Westphal K.G.C., Korte S.M., Oosting R.S., Olivier B., et al. Olfactory bulbectomy induces rapid and stable changes in basal and stress-induced locomotor activity, heart rate and body temperature responses in the home cage. Neuroscience 2009, 159:39-46.
34. Breuer M.E., van Gaalen M.M., Wernet W., Claessens S.E.F., Oosting R.S., Behl B., et al. SSR 149415, a non-peptide vasopressin V1b receptor antagonist, has long-lasting antidepressant effects in the olfactory bulbectomy-induced hyperactivity depression model. Naunyn Schmiedebergs Arch Pharmacol 2009, 379:101-106.
35. Breuer M.E., Groenink L., Oosting R.S., Westenberg H.G., Olivier B. Long-term behavioral changes after cessation of chronic antidepressant treatment in olfactory bulbectomized rats. Biol Psychiatry 2007, 61:990-995.
36. Binder E., Droste S.K., Ohl F., Reul J.M. Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice. Behav Brain Res 2004, 155:197-206.
37. 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, 1019:84-96.
38. Bucinskaite V., Theodorsson E., Crumpton K., Stenfors C., Ekblom A., Lundeberg T. Effects of repeated sensory stimulation (electro-acupuncture) and physical exercise (running) on open-field behaviour and concentrations of neuropeptides in the hippocampus in WKY and SHR rats. Eur J Neurosci 1996, 8:382-387.
39. Dishman R.K., Dunn A.L., Youngstedt S.D., Davis J.M., Burgess M.L., Wilson S.P., et al. Increased open field locomotion and decreased striatal GABAA binding after activity wheel running. Physiol Behav 1996, 60:699-705.
40. Hoffmann P., Thorén P., Ely D. Effect of voluntary exercise on open-field behavior and on aggression in the spontaneously hypertensive rat (SHR). Behav Neural Biol 1987, 47:346-355.
41. Schumacher H.E., Oehler J., Jaehkel M. Individual motor activity-relationships to dopaminergic responses. Pharmacol Biochem Behav 1994, 48:839-844.
42. Skalicky M., Viidik A. Comparison between continuous and intermittent physical exercise on aging rats: changes in patterns of spontaneous activity and connective tissue stability. Aging (Milano) 1999, 11:227-234.
43. Skalicky M., Bubna-Littitz H., Viidik A. Influence of physical exercise on aging rats: I. Life-long exercise preserves patterns of spontaneous activity. Mech Ageing Dev 1996, 87:127-139.
44. Tharp G.D., Carson W.H. Emotionality changes in rats following chronic exercise. Med Sci Sports 1975, 7:123-126.
45. Kariya F., Yamauchi H., Kobayashi K., Narusawa M., Nakahara Y. Effects of prolonged voluntary wheel-running on muscle structure and function in rat skeletal muscle. Eur J Appl Physiol 2004, 92:90-97.
46. Teychenne M., Ball K., Salmon J. Physical activity and likelihood of depression in adults: a review. Prev Med 2008, 46:397-411.
47. Roshanaei-Moghaddam B., Katon W.J., Russo J. The longitudinal effects of depression on physical activity. Gen Hosp Psychiatry 2009, 31:306-315.
48. Gillespie C.F., Nemeroff C.B. Hypercortisolemia and depression. Psychosom Med 2005, 67(Suppl. 1):S26-S28.
49. Pariante C.M. Glucocorticoid receptor function in vitro in patients with major depression. Stress 2004, 7:209-219.
50. Pariante C.P., Lightman S.L. The HPA axis in major depression: classical theories and new developments. Trends Neurosci 2008, 31:464-468.
51. Sothmann M.S., Buckworth J., Claytor R.P., Cox R.H., White-Welkley J.E., Dishman R.K. Exercise training and the cross-stressor adaptation hypothesis. Exerc Sport Sci Rev 1996, 24:267-287.
52. Dishman R.K., Bunnell B.N., Youngstedt S.D., Yoo H.S., Mougey E.H., Meyerhoff J.L. Activity wheel running blunts increased plasma adrenocorticotrophin (ACTH) after footshock and cage-switch stress. Physiol Behav 1998, 63:911-917.
53. Connor T.J., Harkin A., Kelly J.P., Leonard B.E. Olfactory bulbectomy provokes a suppression of interleukin-1beta and tumour necrosis factor-alpha production in response to an in vivo challenge with lipopolysaccharide: effect of chronic desipramine treatment. Neuroimmunomodulation 2000, 7:27-35.
54. Marcilhac A., Faudon M., Anglade G., Hery F., Siaud P. An investigation of serotonergic involvement in the regulation of ACTH and corticosterone in the olfactory bulbectomized rat. Pharmacol Biochem Behav 1999, 63:599-605.
55. Droste S.K., Chandramohan Y., Hill L.E., Linthorst A.C., Reul J.M. Voluntary exercise impacts on the rat hypothalamic-pituitary-adrenocortical axis mainly at the adrenal level. Neuroendocrinology 2007, 86:26-37.
56. Droste S.K., Schweizer M.C., Ulbricht S., Reul J.M. Long-term voluntary exercise and the mouse hypothalamic-pituitary-adrenocortical axis: impact of concurrent treatment with the antidepressant drug tianeptine. J Neuroendocrinol 2006, 18:915-925.
57. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006, 9:526-533.
58. Keppel G. Design and analysis. A researcher's handbook 1991, Prentice Hall, Upper Saddle, NJ. 3rd ed.
59. Daumas S., Halley H., Francés B., Lassalle J. Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learn Mem 2005, 12:375-382.
60. Hunsaker M.R., Kesner R.P. Dissociations across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear. Neurobiol Learn Mem 2008, 89:61-69.
61. Smith P.J., Blumenthal J.A., Hoffman B.M., Cooper H., Strauman T.A., Welsh-Bohmer K., et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom Med 2010, 72:239-252.
62. Molteni R., Wu A., Vaynman S., Ying Z., Barnard R.J., Gómez-Pinilla F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience 2004, 123:429-440.
63. Chen H., Lin L., Yu L., Liu Y., Kuo Y., Huang A., et al. Treadmill exercise enhances passive avoidance learning in rats: the role of down-regulated serotonin system in the limbic system. Neurobiol Learn Mem 2008, 89:489-496.
64. Clark P.J., Brzezinska W.J., Thomas M.W., Ryzhenko N.A., Toshkov S.A., Rhodes J.S. Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience 2008, 155:1048-1058.
65. Lamprecht R., Dracheva S., Assoun S., LeDoux J.E. Fear conditioning induces distinct patterns of gene expression in lateral amygdala. Genes Brain Behav 2009, 8:735-743.
66. Onishi B.K.A., Xavier G.F. Contextual, but not auditory, fear conditioning is disrupted by neurotoxic selective lesion of the basal nucleus of amygdala in rats. Neurobiol Learn Mem 2010, 93:165-174.
67. Lee I., Kesner R.P. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 2004, 14:301-310.
68. Lumia A.R., Teicher M.H., Salchli F., Ayers E., Possidente B. Olfactory bulbectomy as a model for agitated hyposerotonergic depression. Brain Res 1992, 587:181-185.
69. Primeaux S.D., Holmes P.V. Role of aversively motivated behavior in the olfactory bulbectomy syndrome. Physiol Behav 1999, 67:41-47.
70. Mar A., Spreekmeester E., Rochford J. Fluoxetine-induced increases in open-field habituation in the olfactory bulbectomized rat depend on test aversiveness but not on anxiety. Pharmacol Biochem Behav 2002, 73:703-712.
71. Cordero M.I., Venero C., Kruyt M.D., Sandi C. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm Behav 2003, 44:338-345.
72. Abrari K., Rashidy-Pour A., Semnanian S., Fathollahi Y., Jadid M. Post-training administration of corticosterone enhances consolidation of contextual fear memory and hippocampal long-term potentiation in rats. Neurobiol Learn Mem 2009, 91:260-265.
73. Fediuc S., Campbell J.E., Riddell M.C. Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague-Dawley rats. J Appl Physiol 2006, 100:1867-1875.