Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Nummenmaa, Lauri ^a,b   Hirvonen, Jussi ^b   Hannukainen, Jarna C ^b   Immonen, Heidi ^b,c   Lindroos, Markus M ^b   Salminen, Paulina ^c   Nuutila, Pirjo ^b,c  

^a AALTO UNIVERSITY   (Finland)

^b TURKU PET CENTRE   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORODEOXYGLUCOSE F 18; INSULIN; NEUTRAL INSULIN; GLUCOSE;

AMYGDALOID NUCLEUS; ARTICLE; BOLD SIGNAL; CAUDATE NUCLEUS; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUCOSE BRAIN LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HEMODYNAMICS; HUMAN; HYPERINSULINEMIA; INSULA; LIMBIC CORTEX; MORBID OBESITY; OBESITY; ORBITAL CORTEX; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; STIMULUS RESPONSE; ANTICIPATION; BRAIN MAPPING; LIMBIC SYSTEM; METABOLISM; PATHOPHYSIOLOGY; REWARD;

ANTICIPATION, PSYCHOLOGICAL; BRAIN MAPPING; CAUDATE NUCLEUS; CORPUS STRIATUM; GLUCOSE; HUMANS; LIMBIC SYSTEM; OBESITY; REWARD;

EID: 84856514258     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031089     Document Type: Article

References (59)

1. WHO (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 894: i-xii, 1-253.
2. Volkow ND, Wise RA, (2005) How can drug addiction help us understand obesity? Nature Neuroscience 8: 555-560.
3. Berridge KC, (1996) Food reward: Brain substrates of wanting and liking. Neuroscience and Biobehavioral Reviews 20: 1-25.
4. Ikemoto S, Panksepp J, (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Research Reviews 31: 6-41.
5. Kelley AE, (2004) Ventral striatal control of appetitive motivation: Role in ingestive behavior and reward-related learning. Neuroscience and Biobehavioral Reviews 27: 765-776.
6. Killgore WDS, Young AD, Femia LA, Bogorodzki P, Rogowska J, et al. (2003) Cortical and limbic activation during viewing of high- versus low-calorie foods. NeuroImage 19: 1381-1394.
7. LaBar KS, Gitelman DR, Parrish TB, Kim YH, Nobre AC, et al. (2001) Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behavioral Neuroscience 115: 493-500.
8. Pelchat ML, Johnson A, Chan R, Valdez J, Ragland JD, (2004) Images of desire: food-craving activation during fMRI. NeuroImage 23: 1486-1493.
9. Wang GJ, Volkow ND, Telang F, Jayne M, Ma J, et al. (2004) Exposure to appetitive food stimuli markedly activates the human brain. Neuroimage 21: 1790-1797.
10. Stoeckel LE, Weller RE, Cook EW Iii, Twieg DB, Knowlton RC, et al. (2008) Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage 41: 636-647.
11. Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, et al. (2001) Brain dopamine and obesity. Lancet 357: 354-357.
12. Small DM, Jones-Gotman M, Dagher A, (2003) Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. NeuroImage 19: 1709-1715.
13. Kelley AE, Berridge KC, (2002) The neuroscience of natural rewards: Relevance to addictive drugs. Journal of Neuroscience 22: 3306-3311.
14. Volkow ND, Wang GJ, Fowler JS, Telang F, (2008) Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philosophical Transactions of the Royal Society B-Biological Sciences 363: 3191-3200.
15. Cornell CE, Rodin J, Weingarten H, (1989) Stimulus-induced eating when satiated. Physiol Behav 45.
16. Koob GF, Volkow ND, (2010) Neurocircuitry of Addiction. Neuropsychopharmacology 35: 217-238.
17. Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, et al. (2008) Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: Possible contributing factors. NeuroImage 42: 1537-1543.
18. Verdejo-Garcia A, Bechara A, (2009) A somatic marker theory of addiction. Neuropharmacology 56: 48-62.
19. Rothemund Y, Preuschhof C, Bohner G, Bauknecht H-C, Klingebiel R, et al. (2007) Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. NeuroImage 37: 410-421.
20. Franken IHA, Muris P, (2005) Individual differences in reward sensitivity are related to food craving and relative body weight in healthy women. Appetite 45: 198-201.
21. Beaver JB, Lawrence AD, van Ditzhuijzen J, Davis MH, Woods A, et al. (2006) Individual differences in reward drive predict neural responses to images of food. Journal of Neuroscience 26: 5160-5166.
22. Passamonti L, Rowe JB, Schwarzbauer C, Ewbank MP, von dem Hagen E, et al. (2009) Personality Predicts the Brain's Response to Viewing Appetizing Foods: The Neural Basis of a Risk Factor for Overeating. J Neurosci 29: 43-51.
23. Dagher A, (2009) The neurobiology of appetite: hunger as addiction. International Journal of Obesity 33: S30-S33.
24. Berridge KC, Ho C-Y, Richard JM, DiFeliceantonio AG, (2010) The tempted brain eats: Pleasure and desire circuits in obesity and eating disorders. Brain Research 1350: 43-64.
25. Stoeckel LE, Kim J, Weller RE, Cox JE, Cook EW Iii, et al. (2009) Effective connectivity of a reward network in obese women. Brain Research Bulletin 79: 388-395.
26. Sokoloff L, (1999) Energetics of functional activation in neural tissues. Neurochemical Research 24: 321-329.
27. DeFronzo RA, Tobin JD, Andres R, (1979) Glucose clamp technique: a method for quantifying insulin secretion and resistance. AmJPhysiol 237: E214-E223.
28. Bradley MM, Lang PJ, (1994) Measuring emotion- The Self-Assessment Mannequin and the semantic differential. Journal of Behavior Therapy and Experimental Psychiatry 25: 49-59.
29. Kaisti KK, Langsjo JW, Aalto S, Oikonen V, Sipila H, et al. (2003) Effects of sevoflurane, propofol and adjunct nitrous oxide on regional cerebral blood flow, oxygen consumption, and blood volume in humans. Anesthesiology 99: 603-613.
30. Kaisti KK, Metsahonkala L, Teras M, Oikonen V, Aalto S, et al. (2002) Effects of surgical levels of propofol and sevoflurane anesthesia on cerebral blood flow in healthy subjects studied with positron emission tomography. Anesthesiology 96: 1358-1370.
31. Hamacher K, Coenen HH, Stocklin G, (1986) Efficient Stereospecific Synthesis of No-Carrier-Added 2-[F-18]-Fluoro-2-Deoxy-D-Glucose Using Aminopolyether Supported Nucleophilic-Substitution. Journal of Nuclear Medicine 27: 235-238.
32. Graham MM, Muzi M, Spence AM, O'Sullivan F, Lewellen TK, et al. (2002) The FDG lumped constant in normal human brain. Journal of Nuclear Medicine 43: 1157-1166.
33. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH, (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19: 1233-1239.
34. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, et al. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15: 273-289.
35. Amaro E, Barker GJ, (2006) Study design in MRI: Basic principles. Brain and Cognition 60: 220-232.
36. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, et al. (1997) Psychophysiological and Modulatory Interactions in Neuroimaging. NeuroImage 6: 218-229.
37. Passamonti L, Rowe JB, Ewbank M, Hampshire A, Keane J, et al. (2008) Connectivity from the ventral anterior cingulate to the amygdala is modulated by appetitive motivation in response to facial signals of aggression. NeuroImage 43: 562-570.
38. Kriegeskorte N, Simmons WK, Bellgowan PSF, Baker CI, (2009) Circular analysis in systems neuroscience: the dangers of double dipping. Nature Neuroscience 12: 535-540.
39. Gitelman DR, Penny WD, Ashburner J, Friston KJ, (2003) Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. NeuroImage 19: 200-207.
40. Volkow ND, Fowler JS, Wang GJ, Swanson JM, (2004) Dopamine in drug abuse and addiction: results from imaging studies and treatment implications. Molecular Psychiatry 9: 557-569.
41. Haltia LT, Savontaus E, Vahlberg T, Rinne JO, Kaasinen V, (2010) Acute hormonal changes following intravenous glucose challenge in lean and obese human subjects. Scandinavian Journal of Clinical & Laboratory Investigation 70: 275-280.
42. Haltia LT, Rinne JO, Merisaari H, Maguire RP, Savontaus E, et al. (2007) Effects of intravenous glucose on Dopaminergic function in the human brain in vivo. Synapse 61: 748-756.
43. Volkow ND, Wang G-J, Telang F, Fowler JS, Thanos PK, et al. (2008) Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: Possible contributing factors. NeuroImage 42: 1537-1543.
44. Ambroggi F, Ishikawa A, Fields HL, Nicola SM, (2008) Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons. Neuron 59: 648-661.
45. Volkow ND, Wang GJ, Fowler JS, Logan J, Jayne M, et al. (2002) "Nonhedonic" food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect. Synapse 44: 175-180.
46. Small DM, Zatorre RJ, Dagher A, Evans AC, Jones-Gotman M, (2001) Changes in brain activity related to eating chocolate- From pleasure to aversion. Brain 124: 1720-1733.
47. O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, et al. (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304: 452-454.
48. Balleine BW, Delgado MR, Hikosaka O, (2007) The role of the dorsal striatum in reward and decision-making. Journal of Neuroscience 27: 8161-8165.
49. Russchen FT, Bakst I, Amaral DG, Price JL, (1985) The Amygdalostriatal Projections in the Monkey- an Anterograde Tracing Study. Brain Research 329: 241-257.
50. Friedman DP, Aggleton JP, Saunders RC, (2002) Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: Combined anterograde and retrograde tracing study in the macaque brain. Journal of Comparative Neurology 450: 345-365.
51. Will MJ, Franzblau EB, Kelley AE, (2004) The amygdala is critical for opioid-mediated binge eating of fat. NeuroReport 15: 1857-1860.
52. Baldo BA, Alsene KM, Negron A, Kelley AE, (2005) Hyperphagia induced by GABAA receptor-mediated inhibition of the nucleus accumbens shell: Dependence on intact neural output from the central amygdaloid region. Behavioral Neuroscience 119: 1195-1206.
53. Naqvi NH, Bechara A, (2009) The hidden island of addiction: the insula. Trends in Neurosciences 32: 56-67.
54. Baicy K, London ED, Monterosso J, Wong M-L, Delibasi T, et al. (2007) Leptin replacement alters brain response to food cues in genetically leptin-deficient adults. Proceedings of the National Academy of Sciences 104: 18276-18279.
55. Rosenbaum M, Sy M, Pavlovich K, Leibel RL, Hirsch J, (2008) Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. The Journal of Clinical Investigation 118: 2583-2591.
56. Cornier M-A, Salzberg AK, Endly DC, Bessesen DH, Rojas DC, et al. (2009) The Effects of Overfeeding on the Neuronal Response to Visual Food Cues in Thin and Reduced-Obese Individuals. PLoS ONE 4: e6310.
57. Stice E, Spoor S, Bohon C, Veldhuizen MG, Small DM, (2008) Relation of Reward From Food Intake and Anticipated Food Intake to Obesity: A Functional Magnetic Resonance Imaging Study. Journal of Abnormal Psychology 117: 924-935.
58. Lemmens SG, Rutters F, Born JM, Westerterp-Plantenga MS, (in press) Stress augments food 'wanting' and energy intake in visceral overweight subjects in the absence of hunger Physiology & Behavior In Press, Corrected Proof.
59. Nathan PJ, Bullmore ET, (2009) From taste hedonics to motivational drive: central mu-opioid receptors and binge-eating behaviour. International Journal of Neuropsychopharmacology 12: 995-1008.