Exercising for food: Bringing the laboratory closer to nature

Journal of Experimental Biology

Volumn 217, Issue 18, 2014, Pages 3274-3282

  Fonseca, Ivana A T ^a   Passos, Renata L F ^a   Araújo, Fernanda A ^b   Lima, Milene R M ^a   Lacerda, Débora R ^a   Pires, Washington ^a   Soares, Danusa D ^a   Young, Robert J ^c,d   Rodrigues, Luiz Oswaldo C ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^c PONTIFICAL CATHOLIC UNIVERSITY OF MINAS GERAIS   (Brazil)

^d UNIVERSITY OF SALFORD   (United Kingdom)

Author keywords

Feeding behaviour; Motivation; Progressive ratio; Running wheel; Voluntary exercise

Indexed keywords

ANIMALIA; RATTUS;

ANIMAL; BODY TEMPERATURE; EATING; EXERCISE; MALE; MOTOR ACTIVITY; PHYSIOLOGY; RAT; RUNNING; TIME; WISTAR RAT;

ANIMALS; BODY TEMPERATURE; EATING; MALE; MOTOR ACTIVITY; PHYSICAL EXERTION; RATS; RATS, WISTAR; RUNNING; TIME FACTORS;

EID: 84924912348     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.108191     Document Type: Article

References (79)

1. Afonso, V. M. and Eikelboom, R. (2003). Relationship between wheel running, feeding, drinking, and body weight in male rats. Physiol. Behav. 80, 19-26.
2. Altemus, M., Glowa, J. R. and Murphy, D. L. (1993). Attenuation of food-restrictioninduced running by chronic fluoxetine treatment. Psychopharmacol. Bull. 29, 397-400.
3. Barcellos, L. A. M. (2011). Sistema Serotonérgico Está Envolvido na Modulação da Ingestão Alimentar e Massa Corporal de Maneira Dependente da Dieta e Treinamento Físico. 102F. Dissertação de mestrado apresentada no Programa de Pós-graduação em Ciências do Esporte, EEFFTO-UFMG, Belo Horizonte, Brasil.
4. Belke, T. W., Pierce, W. D. and Jensen, K. (2004). Effect of short-term prefeeding and body weight on wheel running and responding reinforced by the opportunity to run in a wheel. Behav. Processes 67, 1-10.
5. Blumstein, D. T. (1992). Multivariate analysis of golden marmot maximum running speed: a new method to study MRS in the field. Ecology 73, 1757-1767.
6. Boakes, R. A. and Dwyer, D. M. (1997). Weight loss in rats produced by running: effects of prior experience and individual housing. Q. J. Exp. Psychol. B 50, 129-148.
7. Brown, D. A., Johnson, M. S., Armstrong, C. J., Lynch, J. M., Caruso, N. M., Ehlers, L. B., Fleshner, M., Spencer, R. L. and Moore, R. L. (2007). Short-term treadmill running in the rat: what kind of stressor is it? J. Appl. Physiol. 103, 1979-1985.
8. Burden, V. R., White, B. D., Dean, R. G. and Martin, R. J. (1993). Activity of the hypothalamic-pituitary-adrenal axis is elevated in rats with activity-based anorexia. J. Nutr. 123, 1217-1225.
9. Burns, J. M., Williams, T. M., Secor, S. M., Owen-Smith, N., Bargmann, N. A. and Castellini, M. A. (2006). New insights into the physiology of natural foraging. Physiol. Biochem. Zool. 79, 242-249.
10. Careau, V. and Garland, T., Jr (2012). Performance, personality, and energetics: correlation, causation, and mechanism. Physiol. Biochem. Zool. 85, 543-571.
11. Castle, W. E. (1947). The domestication of the rat. Proc. Natl. Acad. Sci. USA 33, 109-117.
12. Challet, E., Pévet, P., Vivien-Roels, B. and Malan, A. (1997). Phase-advanced daily rhythms of melatonin, body temperature, and locomotor activity in food-restricted rats fed during daytime. J. Biol. Rhythms 12, 65-79.
13. Chappell, M. A., Garland, T., Jr, Rezende, E. L. and Gomes, F. R. (2004). Voluntary running in deer mice: speed, distance, energy costs and temperature effects. J. Exp. Biol. 207, 3839-3854.
14. Chappell, M. A., Garland, T., Jr, Robertson, G. F. and Saltzman, W. (2007). Relationships among running performance, aerobic physiology and organ mass in male Mongolian gerbils. J. Exp. Biol. 210, 4179-4197.
15. Christian, K. A., Baudinette, R. V. and Pamula, Y. (1997). Energetic costs of activity by lizards in the field. Funct. Ecol. 11, 392-397.
16. Collier, G. H. (1970). Work: a weak reinforcer. Trans. N. Y. Acad. Sci. 32, 557-576.
17. Cortright, R. N., Chandler, M. P., Lemon, P. W. and DiCarlo, S. E. (1997). Daily exercise reduces fat, protein and body mass in male but not female rats. Physiol. Behav. 62, 105-111.
18. Dewsbury, D. A. (1980). Wheel-running behavior in 12 species of muroid rodents. Behav. Processes 5, 271-280.
19. Dohm, M. R., Richardson, C. S. and Garland, T., Jr (1994). Exercise physiology of wild and random-bred laboratory house mice and their reciprocal hybrids. Am. J. Physiol. 267, R1098-R1108.
20. Duffy, P. H., Feuers, R. J., Leakey, J. A., Nakamura, K., Turturro, A. and Hart, R. W. (1989). Effect of chronic caloric restriction on physiological variables related to energy metabolism in the male Fischer 344 rat. Mech. Ageing Dev. 48, 117-133.
21. Duffy, P. H., Leakey, J. E., Pipkin, J. L., Turturro, A. and Hart, R. W. (1997). The physiologic, neurologic, and behavioral effects of caloric restriction related to aging, disease, and environmental factors. Environ. Res. 73, 242-248.
22. Ferguson, S. A. and Paule, M. G. (1997). Progressive ratio performance varies with body weight in rats. Behav. Processes 40, 177-182.
23. Garland, T., Jr, Kelly, S. A., Malisch, J. L., Kolb, E. M., Hannon, R. M., Keeney, B. K., Van Cleave, S. L. and Middleton, K. M. (2011). How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels. Proc. R. Soc. B 278, 574-581.
24. Gelegen, C., Collier, D. A., Campbell, I. C., Oppelaar, H. and Kas, M. J. (2006). Behavioral, physiological, and molecular differences in response to dietary restriction in three inbred mouse strains. Am. J. Physiol. 291, E574-E581.
25. Girard, I., McAleer, M. W., Rhodes, J. S. and Garland, T., Jr (2001). Selection for high voluntary wheel-running increases speed and intermittency in house mice (Mus domesticus). J. Exp. Biol. 204, 4311-4320.
26. Goodrick, C. L., Ingram, D. K., Reynolds, M. A., Freeman, J. R. and Cider, N. L. (1983). Differential effects of intermittent feeding and voluntary exercise on body weight and lifespan in adult rats. J. Gerontol. 38, 36-45.
27. Herrington, L. P. (1940). The heat regulation of small laboratory animals at various environmental temperatures. Am. J. Physiol. 129, 123-139.
28. Hill, J. O., Latiff, A. and DiGirolamo, M. (1985). Effects of variable caloric restriction on utilization of ingested energy in rats. Am. J. Physiol. 248, R549-R559.
29. Houston, A. I. and McNamara, J. M. (1989). The value of food: effects of open and closed economies. Anim. Behav. 37, 546-562.
30. Inglis, I. R., Langton, R., Forkman, B. and Lazarus, J. (2001). An information primacy model of exploratory and foraging behaviour. Anim. Behav. 62, 543-557.
31. Irschick, D. J. and Jayne, B. C. (1999). A field study of the effects of incline on the escape locomotion of a bipedal lizard, Callisaurus draconoides. Physiol. Biochem. Zool. 72, 44-56.
32. Kanarek, R. B., D'Anci, K. E., Jurdak, N. and Mathes, W. F. (2009). Running and addiction: precipitated withdrawal in a rat model of activity-based anorexia. Behav. Neurosci. 123, 905-912.
33. Kenagy, G. J. and Hoyt, D. F. (1989). Speed and time-energy budget for locomotion in golden-mantled ground squirrels. Ecology 70, 1834-1839.
34. Koch, L. G. and Britton, S. L. (2001). Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol. Genomics 5, 45-52.
35. Kramer, D. L. and McLaughlin, R. L. (2001). The behavioral ecology of intermittent locomotion. Am. Zool. 41, 137-153.
36. Krebs, J. R., Davies, N. B. and West, S. A. (2012). Introduction to Behavioural Ecology. Oxford: Wiley-Blackwell.
37. Lacerda, D. R. (2012). Efeito do Treinamento Físico no Esqueleto de Ratas com Obesidade Associada à Ovariectomia. 182F. Dissertação de mestrado apresentada no Programa de Pós-graduação em Ciências do Esporte), EEFFTO-UFMG, Belo Horizonte, Brasil.
38. Lambert, M. I. and Noakes, T. D. (1990). Spontaneous running increases VO2max and running performance in rats. J. Appl. Physiol. 68, 400-403.
39. Lambert, M. I., Van Zyl, C., Jaunky, R., Lambert, E. V. and Noakes, T. D. (1996). Tests of running performance do not predict subsequent spontaneous running in rats. Physiol. Behav. 60, 171-176.
40. Lane, M. A., Baer, D. J., Rumpler, W. V., Weindruch, R., Ingram, D. K., Tilmont, E. M., Cutler, R. G. and Roth, G. S. (1996). Calorie restriction lowers body temperature in rhesus monkeys, consistent with a postulated anti-aging mechanism in rodents. Proc. Natl. Acad. Sci. USA 93, 4159-4164.
41. Lattanzio, S. B. and Eikelboom, R. (2003). Wheel access duration in rats: I. Effects on feeding and running. Behav. Neurosci. 117, 496-504.
42. Lemon, W. C. and Barth, R. H. (1992). The effects of feeding rate on reproductive success in the zebra finch, Taeniopygia guttata. Anim. Behav. 44, 851-857.
43. Lima, N. R., Coimbra, C. C. and Marubayashi, U. (1998). Effect of intracerebroventricular injection of atropine on metabolic responses during exercise in untrained rats. Physiol. Behav. 64, 69-74.
44. Looy, H. and Eikelboom, R. (1989). Wheel running, food intake, and body weight in male rats. Physiol. Behav. 45, 403-405.
45. Mazur, J. E. (2002). Learning and Behavior. Upper Saddle River, NJ: Prentice-Hall Pearson.
46. McAdam, A. G. and Kramer, D. L. (1998). Vigilance as a benefit of intermittent locomotion in small mammals. Anim. Behav. 55, 109-117.
47. McSweeney, K. and Murphy, E. S. (2014). The Wiley-Blackwell Handbook of Operant and Classical Conditioning. Oxford, UK: Wiley.
48. Meijer, J. H. and Robbers, Y. (2014). Wheel running in the wild. Proc. R. Soc. B 281, 20140210-20140210.
49. Mondon, C. E., Dolkas, C. B., Sims, C. and Reaven, G. M. (1985). Spontaneous running activity in male rats: effect of age. J. Appl. Physiol. 58, 1553-1557.
50. Novak, C. M., Burghardt, P. R. and Levine, J. A. (2012). The use of a running wheel to measure activity in rodents: relationship to energy balance, general activity, and reward. Neurosci. Biobehav. Rev. 36, 1001-1014.
51. O'Connor, R. and Eikelboom, R. (2000). The effects of changes in housing on feeding and wheel running. Physiol. Behav. 68, 361-371.
52. Oliveira, M. C., Menezes-Garcia, Z., Henriques, M. C., Soriani, F. M., Pinho, V., Faria, A. M., Santiago, A. F., Cara, D. C., Souza, D. G., Teixeira, M. M. et al. (2013). Acute and sustained inflammation and metabolic dysfunction induced by high refined carbohydrate-containing diet in mice. Obesity (Silver Spring) 21, E396-E406.
53. Overton, J. M. and Williams, T. D. (2004). Behavioral and physiologic responses to caloric restriction in mice. Physiol. Behav. 81, 749-754.
54. Perrigo, G. and Bronson, F. H. (1983). Foraging effort, food intake, fat deposition and puberty in female mice. Biol. Reprod. 29, 455-463.
55. Pires, W., Wanner, S. P., La Guardia, R. B., Rodrigues, L. O., Silveira, S. A., Coimbra, C. C., Marubayashi, U. and Lima, N. R. (2007). Intracerebroventricular physostigmine enhances blood pressure and heat loss in running rats. J. Physiol. Pharmacol. 58, 3-17.
56. Pitts, G. C. (1984). Body composition in the rat: interactions of exercise, age, sex, and diet. Am. J. Physiol. 246, R495-R501.
57. Rezende, E. L., Kelly, S. A., Gomes, F. R., Chappell, M. A. and Garland, T., Jr (2006). Effects of size, sex, and voluntary running speeds on costs of locomotion in lines of laboratory mice selectively bred for high wheel-running activity. Physiol. Biochem. Zool. 79, 83-99.
58. Richard, D. and Rivest, S. (1989). The role of exercise in thermogenesis and energy balance. Can. J. Physiol. Pharmacol. 67, 402-409.
59. Routtenberg, A. and Kuznesof, A. W. (1967). Self-starvation of rats living in activity wheels on a restricted feeding schedule. J. Comp. Physiol. Psychol. 64, 414-421.
60. Rowland, N. E., Vaughan, C. H., Mathes, C. M. and Mitra, A. (2008). Feeding behavior, obesity, and neuroeconomics. Physiol. Behav. 93, 97-109.
61. Russell, J. C., Epling, W. F., Pierce, D., Amy, R. M. and Boer, D. P. (1987). Induction of voluntary prolonged running by rats. J. Appl. Physiol. 63, 2549-2553.
62. Severinsen, T. and Munch, I. C. (1999). Body core temperature during food restriction in rats. Acta Physiol. Scand. 165, 299-305.
63. Shamoun-Baranes, J. and van Loon, E. (2006). Energetic influence on gull flight strategy selection. J. Exp. Biol. 209, 3489-3498.
64. Sherwin, C. M. (1998). Voluntary wheel running: a review and novel interpretation. Anim. Behav. 56, 11-27.
65. Soares, D. D., Lima, N. R. V., Coimbra, C. C. and Marubayashi, U. (2003). Evidence that tryptophan reduces mechanical efficiency and running performance in rats. Pharmacol. Biochem. Behav. 74, 357-362.
66. Soares, D. D., Lima, N. R. V., Coimbra, C. C. and Marubayashi, U. (2004). Intracerebroventricular tryptophan increases heating and heat storage rate in exercising rats. Pharmacol. Biochem. Behav. 78, 255-261.
67. Speakman, J. R. and Mitchell, S. E. (2011). Caloric restriction. Mol. Aspects Med. 32, 159-221.
68. Stevenson, J. A. F., Box, B. M., Feleki, V. and Beaton, J. R. (1966). Bouts of exercise and food intake in the rat. J. Appl. Physiol. 21, 118-122.
69. Stubbs, R. J., Sepp, A., Hughes, D. A., Johnstone, A. M., Horgan, G. W., King, N. and Blundell, J. (2002). The effect of graded levels of exercise on energy intake and balance in free-living men, consuming their normal diet. Eur. J. Clin. Nutr. 56, 129-140.
70. Swallow, J. G., Hayes, J. P., Koteja, P. and Garland, T., Jr (2009). Selection experiments and experimental evolution of performance and physiology. In Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments (ed. J. R. T. Garland and M. R. Rose), pp. 301-351. Berkeley, CA: University of California Press.
71. Taylor, B. A. and Phillips, S. J. (1996). Detection of obesity QTLs on mouse chromosomes 1 and 7 by selective DNA pooling. Genomics 34, 389-398.
72. Tokuyama, K., Saito, M. and Okuda, H. (1982). Effects of wheel running on food intake and weight gain of male and female rats. Physiol. Behav. 28, 899-903.
73. Vaanholt, L. M., De Jong, B., Garland, T., Jr, Daan, S. and Visser, G. H. (2007). Behavioural and physiological responses to increased foraging effort in male mice. J. Exp. Biol. 210, 2013-2024.
74. Wanner, S. P., Guimarães, J. B., Rodrigues, L. O. C., Marubayashi, U., Coimbra, C. C. and Lima, N. R. (2007). Muscarinic cholinoceptors in the ventromedial hypothalamic nucleus facilitate tail heat loss during physical exercise. Brain Res. Bull. 73, 28-33.
75. Weinstein, R. B. (1995). Locomotor behavior of nocturnal ghost crabs on the beach: focal animal sampling and instantaneous velocity from three-dimensional motion analysis. J. Exp. Biol. 198, 989-999.
76. Young, R. J. (1997). The importance of food presentation for animal welfare and conservation. Proc. Nutr. Soc. 56, 1095-1104.
77. Young, R. J. (2003). Environmental Enrichment for Captive Animals. Oxford: Blackwell Science.
78. Young, R. J. and Lawrence, A. B. (1996). The effects of high and low rates of food reinforcement on the behaviour of pigs. Appl. Anim. Behav. Sci. 49, 365-374.
79. Zar, J. H. (2010). Biostatistical Analysis. Upper Saddle River, NJ: Prentice-Hall/Pearson.