Effects of voluntary exercise on spontaneous physical activity and food consumption in mice: Results from an artificial selection experiment

Physiology and Behavior

Volumn 149, Issue , 2015, Pages 86-94

  Copes, Lynn E ^a,c   Schutz, Heidi ^b,d   Dlugosz, Elizabeth M ^b,e   Acosta, Wendy ^b   Chappell, Mark A ^b   Garland, Theodore ^b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Quinnipiac University   (United States)

^d PACIFIC LUTHERAN UNIVERSITY   (United States)

^e UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Compensatory behavior; Energy intake; Food consumption; Non exercise activity thermogenesis; Spontaneous physical activity; Wheel running

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BODY HEIGHT; BODY MASS; CAGE; CHROMOSOME PAIRING; CONTROLLED STUDY; ENERGY BALANCE; EXERCISE; FEMALE; FOOD INTAKE; HEART VENTRICLE; MOUSE; NONHUMAN; PHENOTYPE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RETROPERITONEAL FAT; SPONTANEOUS PHYSICAL ACTIVITY; ADIPOSE TISSUE; ANIMAL; EATING; ENERGY METABOLISM; GENETIC SELECTION; GENETICS; MOTOR ACTIVITY; NEWBORN; PHYSIOLOGY;

ADIPOSE TISSUE; ANIMALS; ANIMALS, NEWBORN; BODY MASS INDEX; EATING; ENERGY METABOLISM; FEMALE; MICE; MOTOR ACTIVITY; PHYSICAL CONDITIONING, ANIMAL; SELECTION, GENETIC;

EID: 84930937141     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2015.05.025     Document Type: Article

References (66)

1. McAllister E.J., Dhurandhar N.V., Keith S.W., Aronne L.J., Barger J., Baskin M., et al. Ten putative contributors to the obesity epidemic. Crit. Rev. Food Sci. Nutr. 2009, 49:868-913.
2. Levine J.A., McCrady S.K., Lanningham-Foster L.M., Kane P.H., Foster R.C., Manohar C.U. The role of free-living daily walking in human weight gain and obesity. Diabetes 2007, 57:548-554.
3. Ross R., McGuire K.A. Incidental physical activity is positively associated with cardiorespiratory fitness. Med. Sci. Sports Exerc. 2011, 43:2189-2194.
4. Thompson D., Karpe F., Lafontan M., Frayn K. Physical activity and exercise in the regulation of human adipose tissue physiology. Physiol. Rev. 2012, 92:157-191.
5. Teske J.A., Billington C.J., Kotz C.M. Mechanisms underlying obesity resistance associated with high spontaneous physical activity. Neuroscience 2013, 256:91-100.
6. Garland T., Schutz H., Chappell M.A., Keeney B.K., Meek T.H., Copes L.E., et al. The biological control of voluntary exercise, spontaneous physical activity and daily energy expenditure in relation to obesity: human and rodent perspectives. J. Exp. Biol. 2011, 214:206-229.
7. Cook C.M., Schoeller D.A. Physical activity and weight control: conflicting findings. Curr. Opin. Clin. Nutr. Metab. Care. 2011, 14:419-424.
8. Johannsen D.L., Ravussin E. Spontaneous physical activity: relationship between fidgeting and body weight control. Curr. Opin. Endocrinol. Diabetes Obes. 2008, 15:409-415.
9. Levine J.A. Nonexercise activity thermogenesis - liberating the life-force. J. Intern. Med. 2007, 262:273-287.
10. Colbert L.H., Schoeller D.A. Expending our physical activity (measurement) budget wisely. J. Appl. Physiol. 2011, 111:606-607.
11. Novak C.M., Burghardt P.R., Levine J.A. The use of a running wheel to measure activity in rodents: relationship to energy balance, general activity, and reward. Neurosci. Biobehav. Rev. 2012, 36:1001-1014.
12. Teske J.A., Perez-Leighton C.E., Billington C.J., Kotz C.M. Methodological considerations for measuring spontaneous physical activity in rodents. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2014, 306:R714-R721.
13. Teske J., Billington C., Kuskowski M., Kotz C. Spontaneous physical activity protects against fat mass gain. Int. J. Obes. 2012, 36:603-613.
14. Malisch J., Breuner C., Kolb E., Wada H., Hannon R., Chappell M., et al. Behavioral despair and home-cage activity in mice with chronically elevated baseline corticosterone concentrations. Behav. Genet. 2009, 39:192-201.
15. Gebczynski A.K., Konarzewski M. Locomotor activity of mice divergently selected for basal metabolic rate: a test of hypotheses on the evolution of endothermy. J. Evol. Biol. 2009, 22:1212-1220.
16. Zombeck J.A., DeYoung E.K., Brzezinska W.J., Rhodes J.S. Selective breeding for increased home cage physical activity in collaborative cross and Hsd:ICR mice. Behav. Genet. 2011, 41:571-582.
17. Garland T., Kelly S.A., Malisch J.L., Kolb E.M., Hannon R.M., Keeney B.K., et al. How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels. Proc. R. Soc. B Biol. Sci. 2011, 278:574-581.
18. Eisenmann J.C., Wickel E.E. The biological basis of physical activity in children: revisited. Pediatr. Exerc. Sci. 2009, 21:257-272.
19. Rhodes J.S., Gammie S.C., Garland T.J. Neurobiology of mice selected for high voluntary wheel-running activity. Integr. Comp. Biol. 2005, 45:438-455.
20. Chow L.S., Greenlund L.J., Asmann Y.W., Short K.R., McCrady S.K., Levine J.A., et al. Impact of endurance training on murine spontaneous activity, muscle mitochondrial DNA abundance, gene transcripts, and function. J. Appl. Physiol. 2007, 102:1078-1089.
21. Swallow J.G., Carter P.A., Garland T. Artificial selection for increased wheel-running behavior in house mice. Behav. Genet. 1998, 28:227-237.
22. Careau V., Wolak M.E., Carter P.A., Garland T. Limits to behavioral evolution: the quantitative genetics of a complex trait under directional selection. Evolution 2013, 67:3102-3119.
23. Belke T.W., Garland T. A brief opportunity to run does not function as a reinforcer for mice selected for high daily wheel-running rates. J. Exp. Anal. Behav. 2007, 88:199-213.
24. Gomes F.R., Rezende E.L., Malisch J.L., Lee S.K., Rivas D.A., Kelly S.A., et al. Glycogen storage and muscle glucose transporters (GLUT-4) of mice selectively bred for high voluntary wheel running. J. Exp. Biol. 2009, 212:238-248.
25. Swallow J.G., Hayes J.P., Koteja P., Garland T. Selection experiments and experimental evolution of performance and physiology. Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments 2009, 301-351.
26. Swallow J.G., Koteja P., Carter P.A., Garland T. Food consumption and body composition in mice selected for high wheel-running activity. J. Comp. Physiol. B-Biochem. Syst. Environ. Physiol. 2001, 171:651-659.
27. Koteja P., Swallow J.G., Carter P.A., Garland T. Energy cost of wheel running in house mice: implications for coadaptation of locomotion and energy budgets. Physiol. Biochem. Zool. 1999, 72:238-249.
28. Koteja P., Garland T., Sax J.K., Swallow J.G., Carter P.A. Behaviour of house mice artificially selected for high levels of voluntary wheel running. Anim. Behav. 1999, 58:1307-1318.
29. Meek T., Eisenmann J., Garland T. Western diet increases wheel running in mice selectively bred for high voluntary wheel running. Int. J. Obes. 2010, 34:960-969.
30. Rezende E.L., Gomes F.R., Chappell M.A., Garland T. Running behavior and its energy cost in mice selectively bred for high voluntary locomotor activity. Physiol. Biochem. Zool. 2009, 82:662-679.
31. O2,max but not voluntary wheel running in mice. J. Exp. Biol. 2010, 213:510-519.
32. Templeman N.M., Schutz H., Garland T., McClelland G.B. Do mice bred selectively for high locomotor activity have a greater reliance on lipids to power submaximal aerobic exercise?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 303:101-111.
33. Keeney B., Meek T., Middleton K., Holness L., Garland T. Sex differences in cannabinoid receptor-1 (CB1) pharmacology in mice selectively bred for high voluntary wheel-running behavior. Pharmacol. Biochem. Behav. 2012, 101:528-537.
34. Koteja P., Swallow J.G., Carter P.A., Garland T. Maximum cold-induced food consumption in mice selected for high locomotor activity: implications for the evolution of endotherm energy budgets. J. Exp. Biol. 2001, 204:1177-1190.
35. Vaanholt L.M., De Jong B., Garland T., Daan S., Visser G.H. Behavioural and physiological responses to increased foraging effort in male mice. J. Exp. Biol. 2007, 210:2013-2024.
36. Vaanholt L.M., Garland T., Daan S., Visser G.H. Wheel-running activity and energy metabolism in relation to ambient temperature in mice selected for high wheel-running activity. J. Comp. Physiol. B-Biochem. Syst. Environ. Physiol. 2007, 177:109-118.
37. Koteja P., Carter P.A., Swallow J.G., Garland T. Food wasting by house mice: variation among individuals, families, and genetic lines. Physiol. Behav. 2003, 80:375-383.
38. Girard I., Rezende E., Garland T. Leptin levels and body composition of mice selectively bred for high voluntary locomotor activity. Physiol. Biochem. Zool. 2007, 80:568-579.
39. Saltin B., Golnick P.D. Skeletal muscle adaptability: significance for metabolism and performance. Handbook of Physiology, Section 10: Skeletal Muscle 1983, 555-631. American Physiological Society, Williams and Wilkins Baltimore, Bethesda, Maryland. L.D. Peachy, R.H. Adrian, S.R. Geiger (Eds.).
40. Garland T., Morgan M.T., Swallow J.G., Rhodes J.S., Girard I., Belter J.G., et al. Evolution of a small-muscle polymorphism in lines of house mice selected for high activity levels. Evolution 2002, 56:1267-1275.
41. Dlugosz E.M., Chappell M.A., McGillivray D.G., Syme D.A., Garland T. Locomotor trade-offs in mice selectively bred for high voluntary wheel running. J. Exp. Biol. 2009, 212:2612-2618.
42. Kelly S.A., Bell T.A., Selitsky S.R., Buus R.J., Hua K., Weinstock G.M., et al. A novel intronic single nucleotide polymorphism in the myosin heavy polypeptide 4 gene is responsible for the mini-muscle phenotype characterized by major reduction in hind-limb muscle mass in mice. Genetics 2013, 195:1385-1395.
43. Burnham K., Anderson D. Model Selection and Multi-model Inference: A Practical Information-theoretic Approach 2002, Springer, New York.
44. Rhodes J.S., Hosack G.R., Girard I., Kelley A.E., Mitchell G.S., Garland T. Differential sensitivity to acute administration of cocaine, GBR 12909, and fluoxetine in mice selectively bred for hyperactive wheel-running behavior. Psychopharmacology 2001, 158:120-131.
45. de Visser L., van den Bos R., Spruijt B.M. Automated home cage observations as a tool to measure the effects of wheel running on cage floor locomotion. Behav. Brain Res. 2005, 160:382-388.
46. Basterfield L., Lumley L.K., Mathers J.C. Wheel running in female C57BL/6J mice: impact of oestrus and dietary fat and effects on sleep and body mass. Int. J. Obes. 2009, 33:212-218.
47. Jung A.P., Curtis T.S., Turner M.J., Lightfoot J.T. Physical activity and food consumption in high- and low-active inbred mouse strains. Med. Sci. Sports Exerc. 2010, 42:1826-1833.
48. Meek T.H., Dlugosz E.M., Vu K.T., Garland T. Effects of leptin treatment and Western diet on wheel running in selectively bred high runner mice. Physiol. Behav. 2012, 106:252-258.
49. Swallow J.G., Koteja P., Carter P.A., Garland T. Food consumption and body composition in mice selected for high wheel-running activity. J. Comp. Physiol. B-Biochem. Syst. Environ. Physiol. 2001, 171:651-659.
50. Hillebrand J.J.G., Koeners M.P., de Rijke C.E., Kas M.J.H., Adan R.A.H. Leptin treatment in activity-based anorexia. Biol. Psychiatry 2005, 58:165-171.
51. Gelegen C., Collier D.A., Campbell I.C., Oppelaar H., van den Heuvel J., Adan R.A., et al. Difference in susceptibility to activity-based anorexia in two inbred strains of mice. Eur. Neuropsychopharmacol. 2007, 17:199-205.
52. Kolb E.M., Rezende E.L., Holness L., Radtke A., Lee S.K., Obenaus A., et al. Mice selectively bred for high voluntary wheel running have larger midbrains: support for the mosaic model of brain evolution. J. Exp. Biol. 2013, 216:515-523.
53. Taylor C.R., Schmidt-Nielsen K., Raab J.L. Scaling of energetic cost of running to body size in mammals. Am. K. Physiol. 1970, 219:1104-1107.
54. Taylor C.R., Heglund N.C., Maloiy G.M.O. Energetics and mechanics of terrestrial locomotion. 1. Metabolic energy-consumption as a function of speed and body size in birds and mammals. J. Exp. Biol. 1982, 97:1-21.
55. Careau V., Bininda-Emonds O.R., Ordonez G., Garland T. Are voluntary wheel running and open-field behavior correlated in mice? Different answers from comparative and artificial selection approaches. Behav. Genet. 2012, 42:830-844.
56. Sherwin C.M. Voluntary wheel running: a review and novel interpretation. Anim. Behav. 1998, 56:11-27.
57. Majdak P., Bucko P.J., Holloway A.L., Bhattacharya T.K., DeYoung E.K., Kilby C.N., et al. Behavioral and pharmacological evaluation of a selectively bred mouse model of home cage hyperactivity. Behav. Genet. 2014, 44:516-534.
58. Pontifex M.B., Saliba B.J., Raine L.B., Picchietti D.L., Hillman C.H. Exercise improves behavioral, neurocognitive, and scholastic performance in children with attention-deficit/hyperactivity disorder. J. Pediatr. 2013, 162:543-551.
59. Archer T., Garcia D. Physical exercise improves cognition and health in ADHD. Journal of Novel Physiotherapies 2014, 4:208-211.
60. Harri M., Lindblom J., Malinen H., Hyttinen M., Lapvetelainen T., Eskola S., et al. Effect of access to a running wheel on behavior of C57BL/6J mice. Lab. Anim. Sci. 1999, 49:401-405.
61. McGillivray D.G., Garland T., Dlugosz E.M., Chappell M.A., Syme D.A. Changes in efficiency and myosin expression in the small-muscle phenotype of mice selectively bred for high voluntary running activity. J. Exp. Biol. 2009, 212:977-985.
62. Booth F.W., Laye M.J., Lees S.J., Rector R.S., Thyfault J.P. Reduced physical activity and risk of chronic disease: the biology behind the consequences. Eur. J. Appl. Physiol. 2008, 102:381-390.
63. Booth F.W., Lees S.J. Fundamental questions about genes, inactivity, and chronic diseases. Physiol. Genomics 2007, 28:146-157.
64. Kelly S.A., Nehrenberg D.L., Hua K., Garland T., Pomp D. Exercise, weight loss, and changes in body composition in mice: phenotypic relationships and genetic architecture. Physiol. Genomics 2011, 43:199-212.
65. Ekkekakis P. Let them roam free? Physiological and psychological evidence for the potential of self-selected exercise intensity in public health. Sports Med. 2009, 39:857-888.
66. Owen N., Healy G.N., Matthews C.E., Dunstan D.W. Too much sitting: the population health science of sedentary behavior. Exerc. Sport Sci. Rev. 2010, 38:105-113.