Basal Ganglia Dysfunction Contributes to Physical Inactivity in Obesity

Cell Metabolism

Volumn 25, Issue 2, 2017, Pages 312-321

  Friend, Danielle M ^a   Devarakonda, Kavya ^a   O'Neal, Timothy J ^a   Skirzewski, Miguel ^e   Papazoglou, Ioannis ^a   Kaplan, Alanna R ^b   Liow, Jeih San ^d   Guo, Juen ^a   Rane, Sushil G ^a   Rubinstein, Marcelo ^f,g,h   Alvarez, Veronica A ^b   Hall, Kevin D ^a   Kravitz, Alexxai V ^a,c  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^e EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^f INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

^g UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^h UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

D2; dopamine; exercise; obese; obesity; physical activity; striatum; weight loss

Indexed keywords

DOPAMINE; DOPAMINE 2 RECEPTOR; PROTEIN BINDING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; CORPUS STRIATUM; DIET INDUCED OBESITY; MOUSE; NERVE CELL; NONHUMAN; PHYSICAL INACTIVITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WEIGHT GAIN; ACTION POTENTIAL; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; LIPID DIET; MALE; METABOLISM; MOUSE MUTANT; MOVEMENT (PHYSIOLOGY); OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BASAL GANGLIA; CORPUS STRIATUM; DIET, HIGH-FAT; MALE; MICE, INBRED C57BL; MICE, OBESE; MOVEMENT; NEURONS; OBESITY; PHYSICAL CONDITIONING, ANIMAL; PROTEIN BINDING; RECEPTORS, DOPAMINE D2; WEIGHT GAIN;

EID: 85009423453     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.12.001     Document Type: Article

References (71)

1. Adams, W.K., Sussman, J.L., Kaur, S., D'souza, A.M., Kieffer, T.J., Winstanley, C.A., Long-term, calorie-restricted intake of a high-fat diet in rats reduces impulse control and ventral striatal D2 receptor signalling—two markers of addiction vulnerability. Eur. J. Neurosci. 42 (2015), 3095–3104.
2. Alexander, G.E., Crutcher, M.D., Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13 (1990), 266–271.
3. Bauman, A.E., Reis, R.S., Sallis, J.F., Wells, J.C., Loos, R.J., Martin, B.W., Lancet Physical Activity Series Working Group. Correlates of physical activity: why are some people physically active and others not?. Lancet 380 (2012), 258–271.
4. Beeler, J.A., Faust, R.P., Turkson, S., Ye, H., Zhuang, X., Low dopamine D2 receptor increases vulnerability to obesity via reduced physical activity not increased appetitive motivation. Biol. Psychiatry 79 (2015), 887–897.
5. Bello, E.P., Mateo, Y., Gelman, D.M., Noaín, D., Shin, J.H., Low, M.J., Alvarez, V.A., Lovinger, D.M., Rubinstein, M., Cocaine supersensitivity and enhanced motivation for reward in mice lacking dopamine D2 autoreceptors. Nat. Neurosci. 14 (2011), 1033–1038.
6. Berglind, D., Willmer, M., Eriksson, U., Thorell, A., Sundbom, M., Uddén, J., Raoof, M., Hedberg, J., Tynelius, P., Näslund, E., Rasmussen, F., Longitudinal assessment of physical activity in women undergoing Roux-en-Y gastric bypass. Obes. Surg. 25 (2015), 119–125.
7. Berglind, D., Willmer, M., Tynelius, P., Ghaderi, A., Naslund, E., Rasmussen, F., Accelerometer-measured versus self-reported physical activity levels and sedentary behavior in women before and 9 months after roux-en-Y gastric bypass. Obes. Surg. 26 (2016), 1463–1470.
8. Blum, K., Braverman, E.R., Wood, R.C., Gill, J., Li, C., Chen, T.J., Taub, M., Montgomery, A.R., Sheridan, P.J., Cull, J.G., Increased prevalence of the Taq I A1 allele of the dopamine receptor gene (DRD2) in obesity with comorbid substance use disorder: a preliminary report. Pharmacogenetics 6 (1996), 297–305.
9. Blum, K., Liu, Y., Shriner, R., Gold, M.S., Reward circuitry dopaminergic activation regulates food and drug craving behavior. Curr. Pharm. Des. 17 (2011), 1158–1167.
10. Bond, D.S., Jakicic, J.M., Unick, J.L., Vithiananthan, S., Pohl, D., Roye, G.D., Ryder, B.A., Sax, H.C., Wing, R.R., Pre- to postoperative physical activity changes in bariatric surgery patients: self report vs. objective measures. Obesity (Silver Spring) 18 (2010), 2395–2397.
11. Brownson, R.C., Boehmer, T.K., Luke, D.A., Declining rates of physical activity in the United States: what are the contributors?. Annu. Rev. Public Health 26 (2005), 421–443.
12. Caravaggio, F., Raitsin, S., Gerretsen, P., Nakajima, S., Wilson, A., Graff-Guerrero, A., Ventral striatum binding of a dopamine D2/3 receptor agonist but not antagonist predicts normal body mass index. Biol. Psychiatry 77 (2015), 196–202.
13. Carlin, J., Hill-Smith, T.E., Lucki, I., Reyes, T.M., Reversal of dopamine system dysfunction in response to high-fat diet. Obesity (Silver Spring) 21 (2013), 2513–2521.
14. Carpenter, C.L., Wong, A.M., Li, Z., Noble, E.P., Heber, D., Association of dopamine D2 receptor and leptin receptor genes with clinically severe obesity. Obesity (Silver Spring) 21 (2013), E467–E473.
15. 18F]desmethoxyfallypride. Synapse 65 (2011), 778–787.
16. Cosgrove, K.P., Veldhuizen, M.G., Sandiego, C.M., Morris, E.D., Small, D.M., Opposing relationships of BMI with BOLD and dopamine D2/3 receptor binding potential in the dorsal striatum. Synapse 69 (2015), 195–202.
17. Cui, G., Jun, S.B., Jin, X., Pham, M.D., Vogel, S.S., Lovinger, D.M., Costa, R.M., Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494 (2013), 238–242.
18. Davis, J.F., Tracy, A.L., Schurdak, J.D., Tschöp, M.H., Lipton, J.W., Clegg, D.J., Benoit, S.C., Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav. Neurosci. 122 (2008), 1257–1263.
19. de Boer, J.O., van Es, A.J., Roovers, L.C., van Raaij, J.M., Hautvast, J.G., Adaptation of energy metabolism of overweight women to low-energy intake, studied with whole-body calorimeters. Am. J. Clin. Nutr. 44 (1986), 585–595.
20. de Groot, L.C., van Es, A.J., van Raaij, J.M., Vogt, J.E., Hautvast, J.G., Adaptation of energy metabolism of overweight women to alternating and continuous low energy intake. Am. J. Clin. Nutr. 50 (1989), 1314–1323.
21. de Rezende, L.F., Rey-López, J.P., Matsudo, V.K., do Carmo Luiz, O., Sedentary behavior and health outcomes among older adults: a systematic review. BMC Public Health, 14, 2014, 333.
22. de Weijer, B.A., van de Giessen, E., van Amelsvoort, T.A., Boot, E., Braak, B., Janssen, I.M., van de Laar, A., Fliers, E., Serlie, M.J., Booij, J., Lower striatal dopamine D2/3 receptor availability in obese compared with non-obese subjects. EJNMMI Res., 1, 2011, 37.
23. DeLong, M.R., Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13 (1990), 281–285.
24. Dobbs, L.K., Kaplan, A.R., Lemos, J.C., Matsui, A., Rubinstein, M., Alvarez, V.A., Dopamine regulation of lateral inhibition between striatal neurons gates the stimulant actions of cocaine. Neuron 90 (2016), 1100–1113.
25. Dunn, J.P., Kessler, R.M., Feurer, I.D., Volkow, N.D., Patterson, B.W., Ansari, M.S., Li, R., Marks-Shulman, P., Abumrad, N.N., Relationship of dopamine type 2 receptor binding potential with fasting neuroendocrine hormones and insulin sensitivity in human obesity. Diabetes Care 35 (2012), 1105–1111.
26. Ekkekakis, P., Lind, E., Exercise does not feel the same when you are overweight: the impact of self-selected and imposed intensity on affect and exertion. Int. J. Obes. 30 (2006), 652–660.
27. Ekkekakis, P., Vazou, S., Bixby, W.R., Georgiadis, E., The mysterious case of the public health guideline that is (almost) entirely ignored: call for a research agenda on the causes of the extreme avoidance of physical activity in obesity. Obes. Rev. 17 (2016), 313–329.
28. Franklin, K.B.J., Paxinos, G., The Mouse Brain in Stereotaxic Coordinates. 1997, Academic Press.
29. Gerfen, C.R., Engber, T.M., Mahan, L.C., Susel, Z., Chase, T.N., Monsma, F.J. Jr., Sibley, D.R., D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250 (1990), 1429–1432.
30. Guo, J., Jou, W., Gavrilova, O., Hall, K.D., Persistent diet-induced obesity in male C57BL/6 mice resulting from temporary obesigenic diets. PLoS One, 4, 2009, e5370.
31. Guo, J., Simmons, W.K., Herscovitch, P., Martin, A., Hall, K.D., Striatal dopamine D2-like receptor correlation patterns with human obesity and opportunistic eating behavior. Mol. Psychiatry 19 (2014), 1078–1084.
32. Hajnal, A., Margas, W.M., Covasa, M., Altered dopamine D2 receptor function and binding in obese OLETF rat. Brain Res. Bull. 75 (2008), 70–76.
33. Hornykiewicz, O., A brief history of levodopa. J. Neurol. 257:Suppl 2 (2010), S249–S252.
34. Horstmann, A., Fenske, W.K., Hankir, M.K., Argument for a non-linear relationship between severity of human obesity and dopaminergic tone. Obes. Rev. 16 (2015), 821–830.
35. Huang, X.F., Zavitsanou, K., Huang, X., Yu, Y., Wang, H., Chen, F., Lawrence, A.J., Deng, C., Dopamine transporter and D2 receptor binding densities in mice prone or resistant to chronic high fat diet-induced obesity. Behav. Brain Res. 175 (2006), 415–419.
36. Johnson, P.M., Kenny, P.J., Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat. Neurosci. 13 (2010), 635–641.
37. Karlsson, H.K., Tuominen, L., Tuulari, J.J., Hirvonen, J., Parkkola, R., Helin, S., Salminen, P., Nuutila, P., Nummenmaa, L., Obesity is associated with decreased μ-opioid but unaltered dopamine D2 receptor availability in the brain. J. Neurosci. 35 (2015), 3959–3965.
38. Karlsson, H.K., Tuulari, J.J., Tuominen, L., Hirvonen, J., Honka, H., Parkkola, R., Helin, S., Salminen, P., Nuutila, P., Nummenmaa, L., Weight loss after bariatric surgery normalizes brain opioid receptors in morbid obesity. Mol. Psychiatry 21 (2016), 1057–1062.
39. Kenny, P.J., Reward mechanisms in obesity: new insights and future directions. Neuron 69 (2011), 664–679.
40. Kessler, R.M., Zald, D.H., Ansari, M.S., Li, R., Cowan, R.L., Changes in dopamine release and dopamine D2/3 receptor levels with the development of mild obesity. Synapse 68 (2014), 317–320.
41. Kilpatrick, I.C., Jones, M.W., Phillipson, O.T., A semiautomated analysis method for catecholamines, indoleamines, and some prominent metabolites in microdissected regions of the nervous system: an isocratic HPLC technique employing coulometric detection and minimal sample preparation. J. Neurochem. 46 (1986), 1865–1876.
42. Kravitz, A.V., Freeze, B.S., Parker, P.R., Kay, K., Thwin, M.T., Deisseroth, K., Kreitzer, A.C., Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466 (2010), 622–626.
43. Lammertsma, A.A., Hume, S.P., Simplified reference tissue model for PET receptor studies. Neuroimage 4 (1996), 153–158.
44. Le Moine, C., Bloch, B., D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol. 355 (1995), 418–426.
45. Lemos, J.C., Friend, D.M., Kaplan, A.R., Shin, J.H., Rubinstein, M., Kravitz, A.V., Alvarez, V.A., Enhanced GABA transmission drives bradykinesia following loss of dopamine D2 receptor signaling. Neuron 90 (2016), 824–838.
46. Levey, A.I., Hersch, S.M., Rye, D.B., Sunahara, R.K., Niznik, H.B., Kitt, C.A., Price, D.L., Maggio, R., Brann, M.R., Ciliax, B.J., Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc. Natl. Acad. Sci. USA 90 (1993), 8861–8865.
47. Martin, C.K., Heilbronn, L.K., de Jonge, L., DeLany, J.P., Volaufova, J., Anton, S.D., Redman, L.M., Smith, S.R., Ravussin, E., Effect of calorie restriction on resting metabolic rate and spontaneous physical activity. Obesity (Silver Spring) 15 (2007), 2964–2973.
48. Mathes, W.F., Nehrenberg, D.L., Gordon, R., Hua, K., Garland, T. Jr., Pomp, D., Dopaminergic dysregulation in mice selectively bred for excessive exercise or obesity. Behav. Brain Res. 210 (2010), 155–163.
49. Michaelides, M., Thanos, P.K., Kim, R., Cho, J., Ananth, M., Wang, G.J., Volkow, N.D., PET imaging predicts future body weight and cocaine preference. Neuroimage 59 (2012), 1508–1513.
50. Murray, S., Tulloch, A., Gold, M.S., Avena, N.M., Hormonal and neural mechanisms of food reward, eating behaviour and obesity. Nat. Rev. Endocrinol. 10 (2014), 540–552.
51. Narayanaswami, V., Thompson, A.C., Cassis, L.A., Bardo, M.T., Dwoskin, L.P., Diet-induced obesity: dopamine transporter function, impulsivity and motivation. Int. J. Obes. 37 (2013), 1095–1103.
52. Noble, E.P., Blum, K., Ritchie, T., Montgomery, A., Sheridan, P.J., Allelic association of the D2 dopamine receptor gene with receptor-binding characteristics in alcoholism. Arch. Gen. Psychiatry 48 (1991), 648–654.
53. Ramirez-Marrero, F.A., Miles, J., Joyner, M.J., Curry, T.B., Self-reported and objective physical activity in postgastric bypass surgery, obese and lean adults: association with body composition and cardiorespiratory fitness. J. Phys. Act. Health 11 (2014), 145–151.
54. Ravussin, Y., Gutman, R., LeDuc, C.A., Leibel, R.L., Estimating energy expenditure in mice using an energy balance technique. Int. J. Obes. 37 (2013), 399–403.
55. Redman, L.M., Heilbronn, L.K., Martin, C.K., de Jonge, L., Williamson, D.A., Delany, J.P., Ravussin, E., Pennington CALERIE Team. Metabolic and behavioral compensations in response to caloric restriction: implications for the maintenance of weight loss. PLoS One, 4, 2009, e4377.
56. Sharma, S., Merghani, A., Mont, L., Exercise and the heart: the good, the bad, and the ugly. Eur. Heart J. 36 (2015), 1445–1453.
57. Steele, K.E., Prokopowicz, G.P., Schweitzer, M.A., Magunsuon, T.H., Lidor, A.O., Kuwabawa, H., Kumar, A., Brasic, J., Wong, D.F., Alterations of central dopamine receptors before and after gastric bypass surgery. Obes. Surg. 20 (2010), 369–374.
58. Stice, E., Spoor, S., Bohon, C., Small, D.M., Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322 (2008), 449–452.
59. Thompson, J., Thomas, N., Singleton, A., Piggott, M., Lloyd, S., Perry, E.K., Morris, C.M., Perry, R.H., Ferrier, I.N., Court, J.A., D2 dopamine receptor gene (DRD2) Taq1 A polymorphism: reduced dopamine D2 receptor binding in the human striatum associated with the A1 allele. Pharmacogenetics 7 (1997), 479–484.
60. Tuominen, L., Tuulari, J., Karlsson, H., Hirvonen, J., Helin, S., Salminen, P., Parkkola, R., Hietala, J., Nuutila, P., Nummenmaa, L., Aberrant mesolimbic dopamine-opiate interaction in obesity. Neuroimage 122 (2015), 80–86.
61. van de Giessen, E., la Fleur, S.E., de Bruin, K., van den Brink, W., Booij, J., Free-choice and no-choice high-fat diets affect striatal dopamine D2/3 receptor availability, caloric intake, and adiposity. Obesity (Silver Spring) 20 (2012), 1738–1740.
62. van de Giessen, E., la Fleur, S.E., Eggels, L., de Bruin, K., van den Brink, W., Booij, J., High fat/carbohydrate ratio but not total energy intake induces lower striatal dopamine D2/3 receptor availability in diet-induced obesity. Int. J. Obes. 37 (2013), 754–757.
63. Volkow, N.D., Wise, R.A., How can drug addiction help us understand obesity?. Nat. Neurosci. 8 (2005), 555–560.
64. Volkow, N.D., Wang, G.J., Telang, F., Fowler, J.S., Thanos, P.K., Logan, J., Alexoff, D., Ding, Y.S., Wong, C., Ma, Y., Pradhan, K., Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. Neuroimage 42 (2008), 1537–1543.
65. Volkow, N.D., Wang, G.J., Logan, J., Alexoff, D., Fowler, J.S., Thanos, P.K., Wong, C., Casado, V., Ferre, S., Tomasi, D., Caffeine increases striatal dopamine D2/D3 receptor availability in the human brain. Transl. Psychiatry, 5, 2015, e549.
66. Vucetic, Z., Carlin, J.L., Totoki, K., Reyes, T.M., Epigenetic dysregulation of the dopamine system in diet-induced obesity. J. Neurochem. 120 (2012), 891–898.
67. Wang, G.J., Volkow, N.D., Logan, J., Pappas, N.R., Wong, C.T., Zhu, W., Netusil, N., Fowler, J.S., Brain dopamine and obesity. Lancet 357 (2001), 354–357.
68. Wang, G.J., Tomasi, D., Convit, A., Logan, J., Wong, C.T., Shumay, E., Fowler, J.S., Volkow, N.D., BMI modulates calorie-dependent dopamine changes in accumbens from glucose intake. PLoS One, 9, 2014, e101585.
69. Westerterp, K.R., Obesity and physical activity. Int. J. Obes. Relat. Metab. Disord. 23:Suppl 1 (1999), 59–64.
70. Wiers, C.E., Shumay, E., Cabrera, E., Shokri-Kojori, E., Gladwin, T.E., Skarda, E., Cunningham, S.I., Kim, S.W., Wong, T.C., Tomasi, D., et al. Reduced sleep duration mediates decreases in striatal D2/D3 receptor availability in cocaine abusers. Transl. Psychiatry, 6, 2016, e752.
71. Zhang, C., Wei, N.L., Wang, Y., Wang, X., Zhang, J.G., Zhang, K., Deep brain stimulation of the nucleus accumbens shell induces anti-obesity effects in obese rats with alteration of dopamine neurotransmission. Neurosci. Lett. 589 (2015), 1–6.