Physical exercise during adolescence versus adulthood: Differential effects on object recognition memory and brain-derived neurotrophic factor levels

Neuroscience

Volumn 194, Issue , 2011, Pages 84-94

  Hopkins, M E ^a   Nitecki, R ^a   Bucci, D J ^a  

^a Dartmouth College   (United States)

Author keywords

Familiarity; Hippocampus; Perirhinal cortex; Recollection; Wheel running

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ADOLESCENCE; ADULT ANIMAL; ADULTHOOD; AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; COGNITION; CONTROLLED STUDY; EXERCISE; HIPPOCAMPUS; JUVENILE ANIMAL; LOCOMOTION; MALE; MENTAL PERFORMANCE; NONHUMAN; OBJECT RECOGNITION; PERIRHINAL CORTEX; PRIORITY JOURNAL; RAT; RECALL; RECOGNITION; RUNNING;

AGING; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; EXERCISE THERAPY; HIPPOCAMPUS; MALE; MEMORY; PATTERN RECOGNITION, VISUAL; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, LONG-EVANS; RECOGNITION (PSYCHOLOGY); SEXUAL MATURATION; TEMPORAL LOBE;

EID: 80053093795     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.07.071     Document Type: Article

References (57)

1. Adlard P.A., Perreau V.M., Engesser-Cesar C., Cotman C.W. The time course of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci Lett 2004, 363(1):43-48.
2. Aggleton J.P., Sanderson D.J., Pearce J.M. Structural learning and the hippocampus. Hippocampus 2007, 17(9):723-734.
3. Alaei H., Moloudi R., Sarkaki A.R., Azizi-Malekabadi H., Hanninen O. Daily running promotes spatial learning and memory in rats. Pathophysiology 2007, 14(2):105-108.
4. Albeck D.S., Sano K., Prewitt G.E., Dalton L. Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res 2006, 168:345-348.
5. Andersen S.L. Trajectories of brain development: point of vulnerability or window of opportunity?. Neurosci Biobehav Rev 2003, 27:3-18.
6. Baruch D.E., Swain R.A., Helmstetter F.J. Effects of exercise on Pavlovian fear conditioning. Behav Neurosci 2004, 118(5):1123-1127.
7. Berchtold N.C., Chinn G., Chou M., Kesslak J.P., Cotman C.W. Exercise primes a molecular memory for brain-derived neurotrophic factor protein induction in the rat hippocampus. Neuroscience 2005, 133:853-861.
8. Bevins R.A., Besheer J. Object recognition in rats and mice: A one-trial non-matching-to-sample learning task to study "recognition memory. Nat Protoc 2006, 1(3):1306-1311.
9. Binder E., Droste S.K., Ohl F., Reul J.M. Regular voluntary exercise reduces anxiety-related behaviour and impulsiveness in mice. Behav Brain 2004, 155(2):197-206.
10. Bjørnebekk A., Mathé A.A., Brené S. The antidepressant effect of running is associated with increased hippocampal cell proliferation. Int J Neuropsychopharmacol 2005, 8:357-368.
11. Brown M.W., Aggleton J.P. Recognition memory: what are the roles of the perirhinal cortex and hippocampus?. Nat Rev 2001, 2:51-61.
12. Bussey T.J., Muir J.L., Aggleton J.P. Functionally dissociating aspects of event memory: the effects of combined perirhinal and postrhinal cortex lesions on object and place memory in the rat. J Neurosci 1999, 19(1):495-502.
13. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29(8):1193-1205.
14. Chen J., Kitanishi T., Ikeda T., Matsuki N., Yamada M.K. Contextual learning induces an increase in the number of hippocampal CA1 neurons expressing high levels of BDNF. Neurobiol Learn Mem 2007, 88(4):409-415.
15. Counotte D.S., Li K.W., Wortel J., Gouwenberg Y., Van Der Schors R.C., Smit A.B., Spijker S. Changes in molecular composition of rat medial prefrontal cortex synapses during adolescent development. Eur J Neurosci 2010, 32(9):1452-1460.
16. Cressman V.L., Balaban J., Steinfeld S., Shemyakin A., Graham P., Parisot N., Moore H. Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat. J Comp Neurol 2010, 518(14):2693-2709.
17. Dere E., Huston J.P., De Souza Silva M.A. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 2007, 31(5):673-704.
18. Ding Q., Vaynman S., Akhavan M., Ying Z., Gomez-Pinilla F. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 2006, 140(3):823-833.
19. Dishman R.K., Berthoud H.R., Booth F.W., Cotman C.W., Edgerton V.R., Fleshner M.R., Zigmond M.J. Neurobiology of exercise. Obesity (Silver Spring) 2006, 14(3):345-356.
20. Douglas L.A., Varlinskaya E.I., Spear L.P. Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation. Physiol Behav 2003, 80(2-3):317-325.
21. 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(1):26-37.
22. Fabel K., Kempermann G. Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromol Med 2008, 10(2):59-66.
23. Fahey B., Barlow S., Day J.S., O'Mara S.M. Interferon-alpha-induced deficits in novel object recognition are rescued by chronic exercise. Physiol Behav 2008, 95(1-2):125-129.
24. Forwood S.E., Winters B.D., Bussey T.J. Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 2005, 15(3):347-355.
25. Fox K.M., Sterling R.C., Van Bockstaele E.J. Cannabinoids and novelty investigation: influence of age and duration of exposure. Behav Brain Res 2009, 196(2):248-253.
26. Fulk L.J., Stock H.S., Lynn A., Marshall J., Wilson M.A., Hand G.A. Chronic physical exercise reduces anxiety-like behavior in rats. Int J Sports Med 2004, 25(1):78-82.
27. García-Capdevila S., Portell-Cortés I., Torras-Garcia M., Coll-Andreu M., Costa-Miserachs D. Effects of long-term voluntary exercise on learning and memory processes: dependency of the task and level of exercise. Behav Brain Res 2009, 202(2):162-170.
28. Gomes da Silva S, Unsain N, Mascó DH, Toscano-Silva M, de Amorim HA, Silva Araújo BH, Simoes PS, da Graça Naffah-Mazzacoratti M, Mortara RA, Scorza FA, Cavalheiro EA, Arida RM (in press) Early exercise promotes positive hippocampal plasticity and improves spatial memory in the adult life of rats. Hippocampus, in press.
29. Griffin E.W., Bechara R.G., Birch A.M., Kelly A.M. Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus 2009, 19:973-980.
30. Haettig J., Stefanko D.P., Multani M.L., Figueroa D.X., McQuown S.C., Wood M.A. HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner. Learn Mem 2011, 18(2):71-79.
31. Halperin J.M., Healey D.M. The influences of environmental enrichment, cognitive enhancement, and physical exercise on brain development: can we alter the developmental trajectory of ADHD?. Neurosci Biobehav Rev 2011, 35(3):621-634.
32. Hopkins M.E., Bucci D.J. Interpreting the effects of exercise on fear conditioning: the influence of time of day. Behav Neurosci 2010, 124(6):868-872.
33. Hopkins M.E., Bucci D.J. Mechanisms underlying exercise-induced improvement in object recognition memory. Neurobiol Learn Mem 2010, 94:278-284.
34. Kealy J., Commins S. The rat perirhinal cortex: a review of anatomy, physiology, plasticity, and function. Prog Neurobiol 2011, 93(4):522-548.
35. Kesslak J.P., So V., Choi J., Cotman C.W., Gomez-Pinilla F. Learning upregulates brain-derived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance?. Behav Neurosci 1998, 112(4):1012-1019.
36. Lores-Arnaiz S., Bustamante J., Czernizyniec A., Galeano P., González Gervasoni M., Rodil Martínez A., Paglia N., Cores V., Lores-Arnaiz M.R. Exposure to enriched environments increases brain nitric oxide synthase and improves cognitive performance in prepubertal but not in young rats. Behav Brain Rev 2007, 184(2):117-123.
37. McCormick C.M., Mathews I.Z. Adolescent development, hypothalamic-pituitary-adrenal function, and programming of adult learning and memory. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34(5):756-765.
38. Ma W., Höhmann C.F., Coyle J.T., Juliano S.L. Lesions of the basal forebrain alter stimulus-evoked metabolic activity in mouse somatosensory cortex. J Comp Neurol 1989, 288(3):414-427.
39. Molteni R., Ying Z., Gómez-Pinilla F. Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. Eur J Neurosci 2002, 16(6):1107-1116.
40. Mumby D.G., Piterkin P., Lecluse V., Lehmann H. Perirhinal cortex damage and anterograde object-recognition in rats after long retention intervals. Behav Brain Res 2007, 185(2):82-87.
41. Naimark A., Barkai E., Matar M.A., Kaplan Z., Kozlovsky N., Cohen H. Upregulation of neurotrophic factors selectively in frontal cortex in response to olfactory discrimination learning. Neural Plast 2007, 2007:13427.
42. Nithianantharajah J., Hannan A.J. The neurobiology of brain and cognitive reserve: mental and physical activity as modulators of brain disorders. Prog Neurobiol 2009, 89(4):369-382.
43. O'Callaghan R.M., Ohle R., Kelly A.M. The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning. Behav Brain Res 2007, 176(2):362-366.
44. Paylor R., Morrison S.K., Rudy J.W., Waltrip L.T., Wehner J.M. Brief exposure to an enriched environment improves performance on the Morris water task and increases hippocampal cytosolic protein kinase C activity in young rats. Behav Brain Res 1992, 52(1):49-59.
45. Romeo R.D., McEwen B.S. Stress and the adolescent brain. Ann N Y Acad Sci 2006, 1094:202-214.
46. Ruis M.A., te Brake J.H., Buwalda B., De Boer S.F., Meerlo P., Korte S.M., Blokhuis H.J., Koolhaas J.M. Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 1999, 24(3):285-300.
47. Smith K.S., Morrell J.I. Comparison of infant and adult rats in exploratory activity, diurnal patterns, and responses to novel and anxiety-provoking environments. Behav Neurosci 2007, 121(3):449-461.
48. Squire L.R., Wixted J.T., Clark R.E. Recognition memory and the medial temporal lobe: a new perspective. Nat Rev Neurosci 2007, 8(11):872-883.
49. Stansfield K.H., Kirstein C.L. Effects of novelty on behavior in the adolescent and adult rat. Dev Psychobiol 2006, 48(1):10-15.
50. Stranahan A.M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006, 9(4):526-533.
51. Tokuyama W., Okuno H., Hashimoto T., Xin Li Y., Miyashita Y. BDNF upregulation during declarative memory formation in monkey inferior temporal cortex. Nat Neurosci 2000, 3(11):1134-1142.
52. Vaynman S., Ying Z., Gomez-Pinilla F. Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 2003, 122(3):647-657.
53. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20(10):2580-2590.
54. Warburton E.C., Brown M.W. Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia 2010, 48(8):2262-2272.
55. Weiss I.C., Pryce C.R., Jongen-Rêlo A.L., Nanz-Bahr N.I., Feldon J. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 2004, 152(2):279-295.
56. Williams B.M., Luo Y., Ward C., Redd K., Gibson R., Kuczaj S.A., McCoy J.G. Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiol Behav 2001, 73(4):649-658.
57. Winters B.D., Saksida L.M., Bussey T.J. Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci Biobehav Rev 2008, 32(5):1055-1070.