Obesity - A Matter of Motivation?

Overview

Journal Exp Clin Endocrinol Diabetes

Specialty Endocrinology

Date 2022 Feb 19

PMID 35181879

Authors

Ruth Hanssen

Sharmili E Thanarajah

Marc Tittgemeyer

Jens C Bruning

Affiliations

Soon will be listed here.

Abstract

Excessive food intake and reduced physical activity have long been established as primary causes of obesity. However, the underlying mechanisms causing this unhealthy behavior characterized by heightened motivation for food but not for physical effort are unclear. Despite the common unjustified stigmatization that obesity is a result of laziness and lack of discipline, it is becoming increasingly clear that high-fat diet feeding and obesity cause alterations in brain circuits that are critical for the control of motivational behavior.In this mini-review, we provide a comprehensive overview of incentive motivation, its neural encoding in the dopaminergic mesolimbic system as well as its metabolic modulation with a focus on derangements of incentive motivation in obesity. We further discuss the emerging field of metabolic interventions to counteract motivational deficits and their potential clinical implications.

References

de Araujo I, Schatzker M, Small D . Rethinking Food Reward. Annu Rev Psychol. 2019; 71:139-164. DOI: 10.1146/annurev-psych-122216-011643. View

Giesen J, Havermans R, Douven A, Tekelenburg M, Jansen A . Will work for snack food: the association of BMI and snack reinforcement. Obesity (Silver Spring). 2010; 18(5):966-70. DOI: 10.1038/oby.2010.20. View

Leinninger G, Opland D, Jo Y, Faouzi M, Christensen L, Cappellucci L . Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab. 2011; 14(3):313-23. PMC: 3183584. DOI: 10.1016/j.cmet.2011.06.016. View

Fernandes A, da Silva J, Almeida J, Cui G, Gerfen C, Costa R . Postingestive Modulation of Food Seeking Depends on Vagus-Mediated Dopamine Neuron Activity. Neuron. 2020; 106(5):778-788.e6. PMC: 7710496. DOI: 10.1016/j.neuron.2020.03.009. View

Mathar D, Horstmann A, Pleger B, Villringer A, Neumann J . Is it Worth the Effort? Novel Insights into Obesity-Associated Alterations in Cost-Benefit Decision-Making. Front Behav Neurosci. 2016; 9:360. PMC: 4709417. DOI: 10.3389/fnbeh.2015.00360. View

Schmidt H, Mietlicki-Baase E, Ige K, Maurer J, Reiner D, Zimmer D . Glucagon-Like Peptide-1 Receptor Activation in the Ventral Tegmental Area Decreases the Reinforcing Efficacy of Cocaine. Neuropsychopharmacology. 2015; 41(7):1917-28. PMC: 4869061. DOI: 10.1038/npp.2015.362. View

Figlewicz D . Expression of receptors for insulin and leptin in the ventral tegmental area/substantia nigra (VTA/SN) of the rat: Historical perspective. Brain Res. 2016; 1645:68-70. DOI: 10.1016/j.brainres.2015.12.041. View

de Weijer B, van de Giessen E, Janssen I, Berends F, van de Laar A, Ackermans M . Striatal dopamine receptor binding in morbidly obese women before and after gastric bypass surgery and its relationship with insulin sensitivity. Diabetologia. 2014; 57(5):1078-80. PMC: 3980032. DOI: 10.1007/s00125-014-3178-z. View

Edwin Thanarajah S, Iglesias S, Kuzmanovic B, Rigoux L, Stephan K, Bruning J . Modulation of midbrain neurocircuitry by intranasal insulin. Neuroimage. 2019; 194:120-127. DOI: 10.1016/j.neuroimage.2019.03.050. View

10.

Naef L, Pitman K, Borgland S . Mesolimbic dopamine and its neuromodulators in obesity and binge eating. CNS Spectr. 2015; 20(6):574-83. DOI: 10.1017/S1092852915000693. View

11.

Skibicka K, Hansson C, Alvarez-Crespo M, Friberg P, Dickson S . Ghrelin directly targets the ventral tegmental area to increase food motivation. Neuroscience. 2011; 180:129-37. DOI: 10.1016/j.neuroscience.2011.02.016. View

12.

Flegal K, Kit B, Orpana H, Graubard B . Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA. 2013; 309(1):71-82. PMC: 4855514. DOI: 10.1001/jama.2012.113905. View

13.

Volkow N, Wang G, Baler R . Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci. 2010; 15(1):37-46. PMC: 3124340. DOI: 10.1016/j.tics.2010.11.001. View

14.

Pozzi M, Mazhar F, Peeters G, Vantaggiato C, Nobile M, Clementi E . A systematic review of the antidepressant effects of glucagon-like peptide 1 (GLP-1) functional agonists: Further link between metabolism and psychopathology: Special Section on "Translational and Neuroscience Studies in Affective Disorders"..... J Affect Disord. 2019; 257. DOI: 10.1016/j.jad.2019.05.044. View

15.

Bhaskaran K, Douglas I, Forbes H, Dos-Santos-Silva I, Leon D, Smeeth L . Body-mass index and risk of 22 specific cancers: a population-based cohort study of 5·24 million UK adults. Lancet. 2014; 384(9945):755-65. PMC: 4151483. DOI: 10.1016/S0140-6736(14)60892-8. View

16.

Jerlhag E, Egecioglu E, Dickson S, Douhan A, Svensson L, Engel J . Ghrelin administration into tegmental areas stimulates locomotor activity and increases extracellular concentration of dopamine in the nucleus accumbens. Addict Biol. 2007; 12(1):6-16. DOI: 10.1111/j.1369-1600.2006.00041.x. View

17.

Epstein L, Temple J, Neaderhiser B, Salis R, Erbe R, Leddy J . Food reinforcement, the dopamine D2 receptor genotype, and energy intake in obese and nonobese humans. Behav Neurosci. 2007; 121(5):877-86. PMC: 2213752. DOI: 10.1037/0735-7044.121.5.877. View

18.

Adams W, Sussman J, Kaur S, Dsouza A, Kieffer T, Winstanley C . 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. 2015; 42(12):3095-104. DOI: 10.1111/ejn.13117. View

19.

Jerlhag E . Systemic administration of ghrelin induces conditioned place preference and stimulates accumbal dopamine. Addict Biol. 2008; 13(3-4):358-63. DOI: 10.1111/j.1369-1600.2008.00125.x. View

20.

Pi-Sunyer X, Astrup A, Fujioka K, Greenway F, Halpern A, Krempf M . A Randomized, Controlled Trial of 3.0 mg of Liraglutide in Weight Management. N Engl J Med. 2015; 373(1):11-22. DOI: 10.1056/NEJMoa1411892. View