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Perspective food addiction, caloric restriction, and dopaminergic neurotransmission

Published online by Cambridge University Press:  28 May 2013

Arwen Urrsula Malgorzata Stankowska  and
Albert Gjedde
Arwen Urrsula Malgorzata Stankowska*
Affiliation:
Department of Human Nutrition, University of Copenhagen, Copenhagen, Denmark
Albert Gjedde
Affiliation:
Department of Neuroscience and Pharmacology, University of Copenhagen, Copenhagen, Denmark Center for Healthy Aging, Faculty of Health Sciences, University of Copenhagen, Blegdamsvej, Copenhagen, Denmark Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada Department of Radiology and Radiological Science, Johns Hopkins University, Baltimore, Maryland, USA
*
Arwen U. M. Stankowska, Department of Human Nutrition, University of Copenhagen, Rolighedsvej 30, 1958 Frederiksberg C, Copenhagen, Denmark. Tel: +45 53347600; Fax: +45 3536 0116; E-mail: [email protected]
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Abstract

People attempt to change their lifestyle when obesity impairs their quality of life. The attempts often fail when multiple habits must be changed in unison. Here we explore relations among food addiction, the neurobiology of habits, and caloric restriction, when people seek to return to normal eating behaviour, with particular emphasis on the role of dopaminergic neurotransmission.

Severely obese individuals have specific neurobiological characteristics in common with drug abusers, including low availability of dopamine receptors in the striatum, impaired neuronal responses to dopamine, and reduced activity in prefrontal regions of the cerebral cortex. The neurobiological characteristics suggest that obese people also have a pathological dependence in common with addicts, in the form of food addiction.

Malnutrition and dieting both relate to binge eating, possibly as a compensation for a reduced cognitive reward condition. The combination of caloric restriction and food addiction imparts a high risk of relapse as a result of further reduction of dopaminergic neurotransmission and the subsequent loss of reward. As with drugs of abuse, ingestion of large quantities of sugar in circumstances of uncontrolled eating increases dopamine release in the nucleus accumbens. This and other evidence suggests that abuse of food is a habit learned by means of mechanisms centred in the basal ganglia, with an increased risk of relapse in the presence of associative amplifiers. This risk is predicted by the relationship between dopamine receptor availability in the striatum and sensation-seeking in the form of an inverted U, suggested by recent findings, consistent with two opposite states of hypodopaminergic and hyperdopaminergic neuromodulation.

Keywords

caloric restrictiondopaminereinforcementrewardsubstance-related disorders
Type
Review Article
Information
Acta Neuropsychiatrica , Volume 25 , Issue 5 , October 2013 , pp. 257 - 267
Copyright
Copyright © Scandinavian College of Neuropsychopharmacology 2013 

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References

1.Hoebel, BG, Hernandez, L, Schwartz, DH, Mark, GP, Hunter, GA. Microdialysis studies of brain norepinephrine, serotonin, and dopamine release during ingestive behavior – theoretical and clinical implications. Ann N Y Acad Sci 1989;575:171–193.CrossRefGoogle ScholarPubMed
2.Kelley, AE, Baldo, BA, Pratt, WE. A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J Comp Neurol 2005;493:72–85.CrossRefGoogle ScholarPubMed
3.De Silva, A, Salem, V, Long, CJet al. The gut hormones PYY(3-36) and GLP-1(7-36) amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metab 2011;14:700–706.CrossRefGoogle ScholarPubMed
4.Figlewicz, DP, Sipols, AJ. Energy regulatory signals and food reward. Pharmacol Biochem Behav 2010;97:15–24.CrossRefGoogle ScholarPubMed
5.Erikssen, G. Physical fitness and changes in mortality – the survival of the fittest. Sports Med 2001;31:571–576.CrossRefGoogle ScholarPubMed
6.Rot, M, Collins, KA, Fitterling, HL. Physical exercise and depression. Mt Sinai J Med 2009;76:204–214.Google Scholar
7.Platek, SM, Keenan, JP, Shackleford, TK. Evolutionary Cognitive Neuroscience. London: The MIT press, 2007.Google ScholarPubMed
8.Helmich, I, Latini, A, Sigwalt, A et al. Neurobiological alterations induced by exercise and their impact on depressive disorders [corrected]. [Erratum appears in Clin Pract Epidemiol Ment Health. 2010;7:106]. Clinical Practice & Epidemiology in Mental Health [Electronic Resource]: CP & EMH;6:115–25.CrossRefGoogle Scholar
9.Shils, ME, Shike, M, Ross, AC, Caballero, B, Cousins, RJ. Modern Nutrition in Health and Disease. Baltimore: Lippincott Williams & Wilkins, 2006.Google Scholar
10.Fullerton, DT, Getto, CJ, Swift, WJ, Carlson, IH. Sugar, opioids and binge eating. Brain Res Bull 1985;14:673–680.CrossRefGoogle ScholarPubMed
11.Cohen, MX, Young, J, Baek, JM, Kessler, C, Ranganath, C. Individual differences in extraversion and dopamine genetics predict neural reward responses. Cogn Brain Res 2005;25:851–861.CrossRefGoogle ScholarPubMed
12.Blum, K, Sheridan, PJ, Wood, RCet al. The D-2 dopamine receptor gene as a determinant of reward deficiency syndrome. J R Soc Med 1996;89:396–400.CrossRefGoogle Scholar
13.McInnis, KJ. Diet, exercise, and the challenge of combating obesity in primary care. J Cardiovas Nurs 2003;18:93–100; quiz 101-2.CrossRefGoogle ScholarPubMed
14.Fabricatore, AN, Wadden, TA, Higginbotham, AJet al. Intentional weight loss and changes in symptoms of depression: a systematic review and meta-analysis. Int J Obes 2011;35:1363–1376.CrossRefGoogle ScholarPubMed
15.Bear, MF, Connors, BW, Paradiso, MA. Neuroscience: Exploring the Brain, 3rd edition. Baltimore: Lippincott Williams and Wilkins, 2006.Google Scholar
16.World Health Organization. http://www.dimdi.de/static/en/klassi/icd/icd10/onlinewho/index.htmGoogle Scholar
17.Volkow, ND, Fowler, JS, Wang, GJ, Swanson, JM, Telang, F. Dopamine in drug abuse and addiction – results of imaging studies and treatment implications. Arch Neurol 2007;64:1575–1579.CrossRefGoogle ScholarPubMed
18.Seger, D. Cocaine, metamfetamine, and MDMA abuse: the role and clinical importance of neuroadaptation. Clin Toxicol 2010;48:695–708.CrossRefGoogle ScholarPubMed
19.Gjedde, A, Kumakura, Y, Cumming, P, Linnet, J, Moller, A. Inverted-U-shaped correlation between dopamine receptor availability in striatum and sensation seeking. Proc Nat Acad Sci U S A 2010;107:3870–3875.CrossRefGoogle ScholarPubMed
20.Belin, D, Mar, AC, Dalley, JW, Robbins, TW, Everitt, BJ. High impulsivity predicts the switch to compulsive cocaine-taking. Science 2008;320:1352–1355.CrossRefGoogle ScholarPubMed
21.Ersche, KD, Turton, AJ, Pradhan, S, Bullmore, ET, Robbins, TW. Drug addiction endophenotypes: impulsive versus sensation-seeking personality traits. Biol Psychiatry 2010;68:770–773.CrossRefGoogle ScholarPubMed
22.Dalley, JW, Fryer, TD, Brichard, Let al. Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 2007;315:1267–1270.CrossRefGoogle ScholarPubMed
23.Ishibashi, K, Robertson, C, Brown, Aet al. Differential roles of dopamine D1- and D2-like receptors in impulsivity: a preliminary PET study. J Cereb Blood Flow Metab 2012;32:S82–S83.Google Scholar
24.Volkow, ND, Wang, GJ, Fowler, JSet al. Prediction of reinforcing responses to psychostimulants in humans by brain dopamine D-2 receptor levels. Am J Psychiatry 1999;156:1440–1443.CrossRefGoogle Scholar
25.Martinez, D, Gil, R, Slifstein, Met al. Alcohol dependence is associated with blunted dopamine transmission in the ventral striatum. Biol Psychiatry 2005;58:779–786.CrossRefGoogle ScholarPubMed
26.Di Chiara, G, Bassareo, V. Reward system and addiction: what dopamine does and doesn't do. Curr Opin Pharmacol 2007;7:69–76.CrossRefGoogle Scholar
27.Everitt, BJ, Robbins, TW. Neural systems of reinforcement for drug addition: from actions to habits to compulsion. Nat Neurosci 2006;9:979–979.CrossRefGoogle Scholar
28.Haber, SN, Fudge, JL, McFarland, NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 2000;20:2369–2382.CrossRefGoogle ScholarPubMed
29.Wang, GJ, Volkow, ND, Logan, Jet al. Brain dopamine and obesity. Lancet 2001;357:354–357.CrossRefGoogle ScholarPubMed
30.Wang, GJ, Volkow, ND, Thanos, PK, Fowler, JS. Similarity between obesity and drug addiction as assessed by neurofunctional imaging: a concept review. J Addic Dis 2004;23:39–53.CrossRefGoogle ScholarPubMed
31.Steele, KE, Prokopowicz, GP, Schweitzer, MAet al. Alterations of central dopamine receptors before and after gastric bypass surgery. Obes Surg 2010;20:369–374.CrossRefGoogle ScholarPubMed
32.Dunn, JP, Cowan, RL, Volkow, NDet al. Decreased dopamine type 2 receptor availability after bariatric surgery: preliminary findings. Brain Res 2010;1350:123–130.CrossRefGoogle ScholarPubMed
33.Davis, C, Fox, J. Sensitivity to reward and body mass index (BMI): evidence for a non-linear relationship. Appetite 2008;50:43–49.CrossRefGoogle ScholarPubMed
34.Wang, GJ, Geliebter, A, Volkow, NDet al. Enhanced striatal dopamine release during food stimulation in binge eating disorder. Obesity 2011;19:1601–1608.CrossRefGoogle ScholarPubMed
35.Stice, E, Yokum, S, Blum, K, Bohon, C. Weight gain is associated with reduced striatal response to palatable food. J Neurosci 2010;30:13105–13109.CrossRefGoogle ScholarPubMed
36.Haltia, LT, Rinne, JO, Merisaari, Het al. Effects of intravenous glucose on dopaminergic function in the human brain in vivo. Synapse 2007;61:748–756.CrossRefGoogle ScholarPubMed
37.Davis, C, Claridge, G. The eating disorders as addiction: a psychobiological perspective. Addict Behav 1998;23:463–475.CrossRefGoogle ScholarPubMed
38.Bohon, C, Stice, E, Spoor, S. Female emotional eaters show abnormalities in consummatory and anticipatory food reward: a functional magnetic resonance imaging study. Int J Eat Disord 2009;42:210–221.CrossRefGoogle ScholarPubMed
39.Gearhardt, AN, Yokum, S, Orr, PTet al. Neural correlates of food addiction. Arch Gen Psychiatry 2011;68:808–816.CrossRefGoogle ScholarPubMed
40.Gearhardt, AN, Corbin, WR, Brownell, KD. Preliminary validation of the Yale Food Addiction Scale. Appetite 2009;52:430–436.CrossRefGoogle ScholarPubMed
41.Corcos, M, Nezelof, S, Speranza, Met al. Psychoactive substance consumption in eating disorders. Eat Behav 2001;2:27–38.CrossRefGoogle ScholarPubMed
42.Colantuoni, C, Rada, P, McCarthy, Jet al. Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res 2002;10:478–488.CrossRefGoogle ScholarPubMed
43.Avena, NM, Rada, P, Hoebel, BG. Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 2008;32:20–39.CrossRefGoogle ScholarPubMed
44.Rada, P, Avena, NM, Hoebel, BG. Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 2005;134:737–744.CrossRefGoogle ScholarPubMed
45.Bello, NT, Lucas, LR, Hajnal, A. Repeated sucrose access influences dopamine D2 receptor density in the striatum. Neuroreport 2002;13:1575–1578.CrossRefGoogle ScholarPubMed
46.Bocarsly, ME, Berner, LA, Hoebel, BG, Avena, NM. Rats that binge eat fat-rich food do not show somatic signs or anxiety associated with opiate-like withdrawal: implications for nutrient-specific food addiction behaviors. Physiol Behav 2011;104:865–872.CrossRefGoogle ScholarPubMed
47.Pothos, EN, Creese, I, Hoebel, BG. Restricted eating with weight loss selectively decreases extracellular dopamine in the nucleus accumbens and alters dopamine response to amphetamine, morphine, and food intake. J Neurosci 1995;15:6640–6650.CrossRefGoogle ScholarPubMed
48.Carr, KD, Kim, GY, de Vaca, SC. Rewarding and locomotor-activating effects of direct dopamine receptor agonists are augmented by chronic food restriction in rats. Psychopharmacology 2001;154:420–428.CrossRefGoogle ScholarPubMed
49.Polivy, J, Herman, CP. Dieting and binging – a causal analysis. Am Psychol 1985;40:193–201.CrossRefGoogle ScholarPubMed
50.Bulik, CM, Sullivan, PF, Carter, FA, Joyce, PR. Initial manifestations of disordered eating behavior: dieting versus binging. Int J Eat Disord 1997;22:195–201.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
51.Wardle, J, Beales, S. Control and loss of control over eating: an experimental investigation. J Abnorm Psychol 1988;97:35–40.CrossRefGoogle ScholarPubMed
52.Ogden, J. The Psychology of Eating – From Healthy to Disordered Behaviour. Blackwell Publishing, 2003.Google Scholar
53.Frank, GK, Bailer, UF, Henry, SEet al. Increased dopamine D2/D3 receptor binding after recovery from anorexia nervosa measured by positron emission tomography and C-11 raclopride. Biol Psychiatry 2005;58:908–912.CrossRefGoogle Scholar
54.Frieling, H, Römer, KD, Scholz, Set al. Epigenetic dysregulation of dopaminergic genes in eating disorders. Int J Eat Disord 2010;43:577–583.CrossRefGoogle ScholarPubMed
55.Johnson, PM, Kenny, PJ. Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 2010;13:635–641.CrossRefGoogle ScholarPubMed
56.Peters, A. Does sugar addiction really cause obesity? Front Neuroenergetics 2012;3.CrossRefGoogle ScholarPubMed
57.Peters, A, Kubera, B, Hubold, C, Langemann, D. The selfish brain: stress and eating behavior. Front Neurosci 2011;5.CrossRefGoogle ScholarPubMed
58.Dunn, JP, Kessler, RM, Feurer, IDet al. Relationship of dopamine type 2 receptor binding potential with fasting neuroendocrine hormones and insulin sensitivity in human obesity. Diabetes Care 2012;35:1105–1111.CrossRefGoogle ScholarPubMed
59.Gejl, M, Egefjord, L, Lerche, Set al. Glucagon-like peptide-1 decreases intracerebral glucose content by activating hexokinase and changing glucose clearance during hyperglycemia. J Cereb Blood Flow Metab 2012;32:2146–2152.CrossRefGoogle ScholarPubMed
60.Davis, C, Curtis, C, Levitan, RDet al. Evidence that ‘food addiction’ is a valid phenotype of obesity. Appetite 2011;57:711–717.CrossRefGoogle ScholarPubMed
61.Langlois, K, Garriguet, D. Sugar consumption among Canadians of all ages. Health Rep 2011;22:23–27.Google ScholarPubMed
62.Wang, YC, Bleich, SN, Gortmaker, SL. Increasing caloric contribution from sugar-sweetened beverages and 100% fruit juices among US children and adolescents, 1988–2004. Pediatrics 2008;121:E1604–E1614.CrossRefGoogle ScholarPubMed
63.Thornley, S, Stewart, A, Marshall, R, Jackson, R. Per capita sugar consumption is associated with severe childhood asthma: an ecological study of 53 countries. Prim Care Respir J 2011;20:75–78.CrossRefGoogle ScholarPubMed
64.Hodgkins, C, Frost-Pineda, K, Gold, MS. Weight gain during substance abuse treatment. J Addict Dis 2007;26:41–50.CrossRefGoogle ScholarPubMed
65.Stice, E, Yokum, S, Burger, KS, Epstein, LH, Small, DM. Youth at risk for obesity show greater activation of striatal and somatosensory regions to food. J Neurosci 2011;31:4360–4366.CrossRefGoogle ScholarPubMed
66.Davis, CA, Levitan, RD, Reid, Cet al. Dopamine for “Wanting” and Opioids for “Liking”: a comparison of obese adults with and without binge eating. Obesity 2009;17:1220–1225.CrossRefGoogle ScholarPubMed
67.Sinha, R, Fox, HC, Hong, KIAet al. Effects of adrenal sensitivity, stress- and cue-induced craving, and anxiety on subsequent alcohol relapse and treatment outcomes. Arch Gen Psychiatry 2011;68:942–952.CrossRefGoogle ScholarPubMed
68.Miller, NS, Gold, MS. Management of withdrawal syndromes and relapse prevention in drug and alcohol dependence. Am Fam Physician 1998;58:139–146.Google ScholarPubMed
69.Hodgkins, CC, Jacobs, WS, Gold, MS. Weight gain after adolescent drug addiction treatment and supervised abstinence. Psychiatr Ann 2003;33:112–116.CrossRefGoogle Scholar
70.McCloughen, A, Foster, K. Weight gain associated with taking psychotropic medication: an integrative review. Int J Ment Health Nurs 2011;20:202–222.CrossRefGoogle ScholarPubMed
71.Volkow, ND, Fowler, JS, Wang, GJ. The addicted human brain viewed in the light of imaging studies: brain circuits and treatment strategies. Neuropharmacology 2004;47:3–13.CrossRefGoogle ScholarPubMed
72.Meule, A, Westenhöfer, J, Kübler, A. Food cravings mediate the relationship between rigid, but not flexible control of eating behavior and dieting success. Appetite 2011;57:582–584.CrossRefGoogle Scholar
73.Hagan, MM, Tomaka, J, Moss, DE. Relation of dieting in college and high school students to symptoms associated with semi-starvation. J Health Psychol 2000;5:7–15.CrossRefGoogle ScholarPubMed
74.Keys, A. Experimental human starvation – general and metabolic results of a loss of one 4th the body weight in 6 months. Federation Proceedings 1946;5:55–55.Google Scholar
75.Blum, K, Chen, ALC, Chen, TJHet al. Activation instead of blocking mesolimbic dopaminergic reward circuitry is a preferred modality in the long term treatment of reward deficiency syndrome (RDS): a commentary. Theor Biol Med Model 2008;5.CrossRefGoogle Scholar
76.Blum, K, Chen, TJH, Chen, ALCet al. Dopamine D2 receptor Taq A1 allele predicts treatment compliance of LG839 in a subset analysis of pilot study in the Netherlands. Gene Ther Mol Biol 2008;12:129–140.Google Scholar
77.Kjaer, TW, Bertelsen, C, Piccini, Pet al. Increased dopamine tone during meditation-induced change of consciousness. Cogn Brain Res 2002;13:255–259.CrossRefGoogle ScholarPubMed
78.Heatherton, TF, Baumeister, RF. Binge eating as escape from self-awareness. Psychol Bull 1991;110:86–108.CrossRefGoogle ScholarPubMed
79.Wisniewski, L, Kelly, E. The application of dialectical behavior therapy to the treatment of eating disorders. Cogn Behav Prac 2003;10:131–138.CrossRefGoogle Scholar
80.Iacovino, JM, Gredysa, DM, Altman, M, Wilfley, DE. Psychological treatments for binge eating disorder. Curr Psychiatry Rep 2012;14:432–446.CrossRefGoogle ScholarPubMed