Striatal enkephalinergic differences in rats selectively bred for intrinsic running capacity

Brain Research

Volumn 1572, Issue , 2014, Pages 11-17

  Monroe, Derek C ^a   Holmes, Philip V ^b   Koch, Lauren G ^c   Britton, Steven L ^c   Dishman, Rodney K ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b University of Georgia   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Activity wheel; Enkephalin; In situ hybridization; Nucleus accumbens; Olfactory tubercle

Indexed keywords

ENKEPHALIN; MESSENGER RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CORPUS STRIATUM; ENKEPHALINERGIC ACTIVITY; FEMALE; GENE EXPRESSION; IN SITU HYBRIDIZATION; LINE DIFFERENCE; MALE; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TREADMILL EXERCISE; ANIMAL; GENETICS; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; RUNNING;

ANIMALS; ENKEPHALINS; FEMALE; MALE; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; OLFACTORY TUBERCLE; RATS; RNA, MESSENGER; RUNNING; VENTRAL STRIATUM;

EID: 84903639550     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.05.014     Document Type: Article

References (69)

1. T.W. Belke, and J.P. Wagner The reinforcing property and the rewarding aftereffect of wheel running in rats: a combination of two paradigms Behav. Process. 68 2 2005 165 172
2. K.C. Berridge, and T.E. Robinson What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev. 28 3 1998 309 369
3. A. Bjornebekk, A.A. Mathé, and S. Brené The antidepressant effect of running is associated with increased hippocampal cell proliferation Int. J. Neuropsychopharmacol. 8 3 2005 357 368
4. M.J. Blake, E.A. Stein, and A.J. Vomachka Effects of exercise training on brain opioid peptides and serum LH in female rats Pept 5 5 1984 953 958
5. K.T. Borer Nonhomeostatic control of human appetite and physical activity in regulation of energy balance Exer. Sport Sci. Rev. 38 3 2010 114 121 (110.1097/JES.1090b1013e3181e3728f)
6. S. Brené, A. Bjørnebekk, E. Åberg, A.A. Mathé, L. Olson, and M. Werme Running is rewarding and antidepressive Physiol. Behav. 92 1-2 2007 136 140 10.1016/j.physbeh.2007.05.015
7. C.R. Burgess Histamine and orexin in the control of arousal, locomotion, and motivation J. of Neurosci 30 8 2010 2810 2811 10.1523/jneurosci.0045-10.2010
8. R.N. Cardinal, J.A. Parkinson, J. Hall, and B.J. Everitt Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex Neurosci. Biobehav. Rev. 26 3 2002 321 352 10.1016/s0149-7634(02)00007-6
9. A. Carta, S. Fenu, and M. Morelli Alterations in GAD67, dynorphin and enkephalin mRNA in striatal output neurons following priming in the 6-OHDA model of Parkinson's disease Neurol. Sci. 22 1 2001 59 60
10. R.A. Depue, and P.F. Collins Neurobiology of the structure of personality: dopamine, facilitation of incentive motivation, and extraversion Behav. Brain Sci. 22 3 1999 491 517
11. R.K. Dishman Gene-physical activity interactions in the etiology of obesity: behavioral considerations Obesity 16 S3 2008 S60 S65
12. R.K. Dishman, and P.V. Holmes Opioids and exercise: animal models functional H. Boecker, C.H. Hillman, L. Scheef, H.K. Strüder, Functional Neuroimaging in Exercise and Sport Sciences 2012 Springer New York, NY 45 58
13. P.F. Durieux, B. Bearzatto, S. Guiducci, T. Buch, A. Waisman, M. Zoli, and A. de Kerchove d'Exaerde D2R striatopallidal neurons inhibit both locomotor and drug reward processes Nat. Neurosci. 12 4 2009 393 395
14. M. Eriksson, F. Rasmussen, and P. Tynelius Genetic factors in physical activity and the equal environment assumption-the Swedish young male twins study Behav. Genet. 36 2 2006 238 247
15. S. Ena, A. de Kerchove d'Exaerde, and S.N. Schiffmann Unraveling the differential functions and regulation of striatal neuron sub-populations in motor control, reward, and motivational processes Front. Behav. Neurosci. 5 2011 47
16. T.E. Foley, B.N. Greenwood, H.E. Day, L.G. Koch, S.L. Britton, and M. Fleshner Elevated central monoamine receptor mRNA in rats bred for high endurance capacity: implications for central fatigue Behav. Brain Res. 174 1 2006 132 142
17. E. Garcia-Rill The basal ganglia and the locomotor regions Brain Res. Rev. 11 1 1986 47 63 10.1016/0165-0173(86)90009-3
18. C.R. Gerfen, J.F. McGinty, and W.S. Young Dopamine differentially regulates dynorphin, substance P, and enkephalin expression in striatal neurons: in situ hybridization histochemical analysis J. Neurosci. 11 4 1991 1016 1031
19. C.R. Gerfen, and W.S. Young Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study Brain Res. 460 1 1988 161 167
20. P.E. Gilliam, W.W. Spirduso, T.P. Martin, T.J. Walters, R.E. Wilcox, and R.P. Farrar The effects of exercise training on [3H]-spiperone binding in rat striatum Pharmacol. Biochem. Behav. 20 6 1984 863 867 10.1016/0091-3057(84) 90008-x
21. N.C. Gonzalez, R.A. Howlett, K.K. Henderson, L.G. Koch, S.L. Britton, H.E. Wagner, and P.D. Wagner Systemic oxygen transport in rats artificially selected for running endurance Respir. Physiol. Neurobiol. 151 2 2006 141 150
22. B.N. Greenwood, T.E. Foley, T.V. Le, P.V. Strong, A.B. Loughridge, H.E.W. Day, and M. Fleshner Long-term voluntary wheel running is rewarding and produces plasticity in the mesolimbic reward pathway Behav. Brain Res. 217 2 2011 354 362
23. F.E. Grubbs, and G. Beck Extension of sample sizes and percentage points for significance tests of outlying observations Technometrics 14 4 1972 847 854
24. J.L. Groves-Chapman, P.S. Murray, K.L. Stevens, D.C. Monroe, L.G. Koch, S.L. Britton, and R.K. Dishman Changes in mRNA levels for brain-derived neurotrophic factor after wheel running in rats selectively bred for high- and low-aerobic capacity Brain Res. 1425 0 2011 90 97 10.1016/j.brainres.2011.09.059
25. S.N. Haber Neuroanatomy of reward: a view from the ventral striatum J.A. Gottfried, Neurobiology of Sensation and Reward 2011 CRC Press Boca Raton, FL
26. S. Hattori, M. Naoi, and H. Nishino Striatal dopamine turnover during treadmill running in the rat: relation to the speed of running Brain Res. Bull. 35 1 1994 41 49 10.1016/0361-9230(94)90214-3
27. M. Hayward, and M. Low The contribution of endogenous opioids to food reward is dependent on sex and background strain Neuroscience 144 1 2007 17 25
28. J.C. Horvitz Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum Behav. Brain Res. 137 1-2 2002 65 74 10.1016/s0166-4328(02)00285-1
29. R.A. Howlett, S.D. Kirkton, N.C. Gonzalez, H.E. Wagner, S.L. Britton, L.G. Koch, and P.D. Wagner Peripheral oxygen transport and utilization in rats following continued selective breeding for endurance running capacity J. Appl. Physiol. 106 6 2009 1819 1825
30. M.A. Høydal, U. Wisløff, and O.J. Kemi Running speed and maximal oxygen uptake in rats and mice: practical implications for exercise training, Elligsen O. Eur. J Cardiovasc. Prev. Rehabil. 14 6 2007 753 760
31. S. Ikemoto Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex Brain Res. Rev. 56 1 2007 27 78
32. I.H. Iversen Techniques for establishing schedules with wheel running as reinforcement in rats J. Exp. Anal. Behav. 60 1 1993 219 238
33. P.W. Kalivas, E. Widerlöv, D. Stanley, G. Breese, and A. Prange Enkephalin action on the mesolimbic system: a dopamine-dependent and a dopamine-independent increase in locomotor activity J. Pharmacol. Exp. Ther. 227 1 1983 229 237
34. A.M. Knab, R.S. Bowen, A.T. Hamilton, A.A. Gulledge, and J.T. Lightfoot Altered dopaminergic profiles: Implications for the regulation of voluntary physical activity Behav. Brain Res. 204 1 2009 147 152 10.1016/j.bbr.2009.05.034
35. A.M. Knab, and J.T. Lightfoot Does the difference between physically active and couch potato lie in the dopamine system? Int. J. Biol. Sci. 6 2 2010 133
36. L.G. Koch, and S.L. Britton Artificial selection for intrinsic aerobic endurance running capacity in rats Physiol. Genomics 5 1 2001 45 52
37. L.G. Koch, and S.L. Britton Development of animal models to test the fundamental basis of gene-environment interactions Obesity 16 S3 2008 S28 S32
38. L.G. Koch, S.L. Britton, and U. Wisløff A rat model system to study complex disease risks, fitness, aging, and longevity Trends Cardiovasc. Med. 22 2 2012 29 34
39. A.V. Kravitz, B.S. Freeze, P.R. Parker, K. Kay, M.T. Thwin, K. Deisseroth, and A.C. Kreitzer Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry Nature 466 7306 2010 622 626
40. C. Le Moine, E. Normand, A. Guitteny, B. Fouque, R. Teoule, and B. Bloch Dopamine receptor gene expression by enkephalin neurons in rat forebrain Proc. Natl. Acad. Sci. 87 1 1990 230 234
41. B. Lett, V. Grant, M. Byrne, and M. Koh Pairings of a distinctive chamber with the aftereffect of wheel running produce conditioned place preference Appetite 34 1 2000 87 94
42. S. Li, H. Jiang, M. Stachowiak, P. Hudson, V. Owyang, K. Nanry, and J. Hong Influence of nigrostriatal dopaminergic tone on the biosynthesis of dynorphin and enkephalin in rat striatum Mol. Brain Res. 8 3 1990 219 225
43. J.T. Lightfoot, M.J. Turner, M. Daves, A. Vordermark, and S.R. Kleeberger Genetic influence on daily wheel running activity level Physiol. Genomics 19 3 2004 270 276
44. J.T. Lightfoot, M.J. Turner, D. Pomp, S.R. Kleeberger, and L.J. Leamy Quantitative trait loci for physical activity traits in mice Physiol. Genomics 32 3 2008 401 408
45. W.F. Mathes, D.L. Nehrenberg, R. Gordon, K. Hua, T. Garland Jr., and D. Pomp Dopaminergic dysregulation in mice selectively bred for excessive exercise or obesity Behav. Brain Res. 210 2 2010 155 163
46. G. Mogenson Limbic-motor integration Prog. Psychobiol. Physiol. Psychol 12 1987 117 170
47. M. Morales-Mulia, P. de Gortari, M.-I. Amaya, and M. Méndez Acute ethanol administration differentially alters enkephalinase and aminopeptidase N activity and mRNA levels in regions of the nigrostriatal pathway J. Mol. Neurosci. 49 2 2013 289 300
48. A. Nikoshkov, K. Drakenberg, X. Wang, M. Horvath, E. Keller, and Y. Hurd Opioid neuropeptide genotypes in relation to heroin abuse: dopamine tone contributes to reversed mesolimbic proenkephalin expression Proc. Natl. Acad. Sci. USA 105 2 2008 786 791 10.1073/pnas0710902105
49. C.M. Novak, C. Escande, P.R. Burghardt, M. Zhang, M.T. Barbosa, E.N. Chini, and J.A. Levine Spontaneous activity, economy of activity, and resistance to diet-induced obesity in rats bred for high intrinsic aerobic capacity Horm. Behav. 58 3 2010 355 367
50. A. Parent, and L.-N. Hazrati Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop Brain Res. Rev. 20 1 1995 91 127 10.1016/0165-0173(94)00007-c
51. A.I. Persson, A.S. Naylor, I.H. Jonsdottir, F. Nyberg, P.S. Eriksson, and T. Thorlin Differential regulation of hippocampal progenitor proliferation by opioid receptor antagonists in running and non running spontaneously hypertensive rats Eur. J. Neurosci. 19 7 2004 1847 1855
52. M.D. Roberts, J.D. Brown, L.P. Oberle, A.J. Heese, R.G. Toedebusch, K.D. Wells, and T.E. Childs Phenotypic and molecular differences between rats selectively bred to voluntarily run high vs. low nightly distances Am. J. Physiol.-Regul., Integr. Comparat. Physiol 304 11 2013 R1024 R1035
53. J.D. Salamone, M. Correa, S. Mingote, and S.M. Weber Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse J. Pharm. Exp. Therap 305 2003 1 8
54. A.J.W. Scheurink, G.J. Boersma, R. Nergårdh, and P. Södersten Neurobiology of hyperactivity and reward: Agreeable restlessness in Anorexia Nervosa Physiol. Behav. 100 5 2010 490 495 10.1016/j.physbeh.2010.03.016
55. C.M. Sherwin Voluntary wheel running: a review and novel interpretation Anim. Behav. 56 1 1998 11 27 10.1006/anbe.1998.0836
56. R.L. Simonen, L. Perusse, T. Rankinen, T. Rice, D.C. Rao, and C. Bouchard Familial aggregation of physical activity levels in the Quebec family study Med. Sci. Sports Exerc. 34 7 2002 1137 1142
57. J. Smith, J. Feldman, and B. Schmidt Neural mechanisms generating locomotion studied in mammalian brain stem-spinal cord in vitro FASEB J. 2 7 1988 2283 2288
58. Smith, K.S., Berridge, K.C., Aldridge, J.W. (2011). Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. In: Proceedings of the National Academy of Sciences. doi:10.1073/pnas. 1101920108.
59. J.H. Stubbe, D.I. Boomsma, J.M. Vink, B.K. Cornes, N.G. Martin, A. Skytthe, and J. Kaprio Genetic influences on exercise participation in 37.051 twin pairs from seven countries PloS One 1 1 2006 e22
60. D.J. Surmeier, W.-J. Song, and Z. Yan Coordinated expression of dopamine receptors in neostriatal medium spiny neurons J. Neurosci. 16 20 1996 6579 6591
61. J.G. Swallow, P.A. Carter, and T. Garland Jr Artificial selection for increased wheel-running behavior in house mice Behav. Genet. 28 3 1998 227 237
62. K. Takakusaki, K. Saitoh, H. Harada, and M. Kashiwayanagi Role of basal ganglia-brainstem pathways in the control of motor behaviors Neurosci. Res. 50 2 2004 137 151
63. F. Tang, and W. Man The regional distribution of thyrotropin releasing hormone, leu-enkephalin, met-enkephalin, substance P, somatostatin and cholecystokinin in the rat brain and pituitary Neuropeptides 19 4 1991 287 292
64. J.D. Van Hoomissen, H.O. Chambliss, P.V. Holmes, and R.K. Dishman Effects of chronic exercise and imipramine on mRNA for BDNF after olfactory bulbectomy in rat Brain Res. 974 1-2 2003 228 235
65. R.P. Waters, R.B. Pringle, G.L. Forster, K.J. Renner, J.L. Malisch, T. Garland Jr., and J,G. Swallow Selection for increased voluntary wheel-running affects behavior and brain monoamines in mice Brain Res. 1508 2013 9 22
66. R.P. Waters, K. Renner, R. Pringle, C.H. Summers, S. Britton, L. Koch, and J. Swallow Selection for aerobic capacity affects corticosterone, monoamines and wheel-running activity Physiol. Behav. 93 4 2008 1044 1054
67. M. Werme, C. Messer, L. Olson, L. Gilden, P. Thoren, E.J. Nestler, and S. Brene Delta FosB regulates wheel running J. Neurosci. 22 18 2002 8133 8138
68. R.A. Wise Dopamine, learning and motivation Nat. Rev. Neurosci. 5 6 2004 483 494
69. W.S. Young, T.I. Bonner, and M.R. Brann Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain Proc. Natl. Acad. Sci. 83 24 1986 9827 9831