Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-09T07:09:20.835Z Has data issue: false hasContentIssue false
  • English
  • Français

Brain dopamine and serotonin transporter binding are associated with visual attention bias for food in lean men

Published online by Cambridge University Press:  17 March 2016

K. E. Koopman ,
A. Roefs ,
D. C. E. Elbers ,
E. Fliers ,
J. Booij ,
M. J. Serlie  and
S. E. la Fleur
K. E. Koopman
Affiliation:
Department of Endocrinology & Metabolism, Academic Medical Center Amsterdam, University of Amsterdam, The Netherlands
A. Roefs
Affiliation:
Faculty of Psychology & Neuroscience, Maastricht University, Maastricht, The Netherlands
D. C. E. Elbers
Affiliation:
Department of Endocrinology & Metabolism, Academic Medical Center Amsterdam, University of Amsterdam, The Netherlands
E. Fliers
Affiliation:
Department of Endocrinology & Metabolism, Academic Medical Center Amsterdam, University of Amsterdam, The Netherlands
J. Booij
Affiliation:
Department of Nuclear Medicine, Academic Medical Center Amsterdam, University of Amsterdam, The Netherlands
M. J. Serlie
Affiliation:
Department of Endocrinology & Metabolism, Academic Medical Center Amsterdam, University of Amsterdam, The Netherlands
S. E. la Fleur*
Affiliation:
Department of Endocrinology & Metabolism, Academic Medical Center Amsterdam, University of Amsterdam, The Netherlands
*
*Address for correspondence: Dr S. E. la Fleur, Department of Endocrinology & Metabolism, Academic Medical Center, University of Amsterdam, Meibergdeef 9, 1105 AZ, Amsterdam, The Netherlands. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

In rodents, the striatal dopamine (DA) system and the (hypo)thalamic serotonin (5-HT) system are involved in the regulation of feeding behavior. In lean humans, little is known about the relationship between these brain neurotransmitter systems and feeding. We studied the relationship between striatal DA transporters (DAT) and diencephalic 5-HT transporters (SERT), behavioral tasks and questionnaires, and food intake.

Method

We measured striatal DAT and diencephalic SERT binding with [123I]FP-CIT SPECT in 36 lean male subjects. Visual attention bias for food (detection speed and distraction time) and degree of impulsivity were measured using response-latency-based computer tasks. Craving and emotional eating were assessed with questionnaires and ratings of hunger by means of VAS scores. Food intake was assessed through a self-reported online diet journal.

Results

Striatal DAT and diencephalic SERT binding negatively correlated with food detection speed (p = 0.008, r = −0.50 and p = 0.002, r = −0.57, respectively), but not with food distraction time, ratings of hunger, craving or impulsivity. Striatal DAT and diencephalic SERT binding did not correlate with free choice food intake, whereas food detection speed positively correlated with total caloric intake (p = 0.001, r = 0.60), protein intake (p = 0.01, r = 0.44), carbohydrate intake (p = 0.03, r = 0.39) and fat intake (p = 0.06, r = 0.35).

Conclusions

These results indicate a role for the central 5-HT and DA system in the regulation of visual attention bias for food, which contributes to the motivation to eat, in non-obese, healthy humans. In addition, this study confirms that food detection speed, measured with the latency-based computer task, positively correlates with total food and macronutrient intake.

Keywords

Dopaminefood intakelean manserotoninvisual attention bias
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 8 , June 2016 , pp. 1707 - 1717
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baldo, BA, Sadeghian, K, Basso, AM, Kelley, AE (2002). Effects of selective dopamine D1 or D2 receptor blockade within nucleus accumbens subregions on ingestive behavior and associated motor activity. Behavioural Brain Research 137, 165–177.Google Scholar
Beeler, JA, Frazier, CR, Zhuang, X (2012). Dopaminergic enhancement of local food-seeking is under global homeostatic control. European Journal of Neuroscience 35, 146–159.CrossRefGoogle ScholarPubMed
Berridge, KC (2007). The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology 191, 391–431.CrossRefGoogle ScholarPubMed
Berridge, KC (2009). ‘Liking’ and ‘wanting’ food rewards: brain substrates and roles in eating disorders. Physiololgy and Behavior 97, 537–550.Google Scholar
Booij, J, Hemelaar, TG, Speelman, JD, de, BK, Janssen, AG, van Royen, EA (1999). One-day protocol for imaging of the nigrostriatal dopaminergic pathway in Parkinson's disease by [123I]FPCIT SPECT. Journal of Nuclear Medicine 40, 753–761.Google ScholarPubMed
Borgers, AJ, Koopman, KE, Bisschop, PH, Serlie, MJ, Swaab, DF, Fliers, E, la Fleur, SE, Alkemade, A (2014). Decreased serotonin transporter immunoreactivity in the human hypothalamic infundibular nucleus of overweight subjects. Frontiers in Neuroscience 8, 106.Google Scholar
Breisch, ST, Zemlan, FP, Hoebel, BG (1976). Hyperphagia and obesity following serotonin depletion by intraventricular p-chlorophenylalanine. Science 192, 382–385.CrossRefGoogle ScholarPubMed
Castellanos, EH, Charboneau, E, Dietrich, MS, Park, S, Bradley, BP, Mogg, K, Cowan, RL (2009). Obese adults have visual attention bias for food cue images: evidence for altered reward system function. International Journal of Obesity 33, 1063–1073.Google Scholar
Chen, X, Margolis, KJ, Gershon, MD, Schwartz, GJ, Sze, JY (2012). Reduced serotonin reuptake transporter (SERT) function causes insulin resistance and hepatic steatosis independent of food intake. PLoS ONE 7, e32511.Google Scholar
Daws, LC, Gould, GG (2011). Ontogeny and regulation of the serotonin transporter: providing insights into human disorders. Pharmacology & Therapeutics 131, 61–79.CrossRefGoogle ScholarPubMed
de Weijer, BA, van de Giessen, E, van Amelsvoort, TA, Boot, E, Braak, B, Janssen, IM, van de Laar, A, Fliers, E, Serlie, MJ, Booij, J (2011). Lower striatal dopamine D2/3 receptor availability in obese compared with non-obese subjects. EJNMMI Research 1, 37.CrossRefGoogle ScholarPubMed
Derryberry, D (1989). Effects of goal-related motivational states on the orienting of spatial attention. Acta Psychologica 72, 199–220.CrossRefGoogle ScholarPubMed
Erritzoe, D, Frokjaer, VG, Haahr, MT, Kalbitzer, J, Svarer, C, Holst, KK, Hansen, DL, Jernigan, TL, Lehel, S, Knudsen, GM (2010). Cerebral serotonin transporter binding is inversely related to body mass index. Neuroimage 52, 284–289.Google Scholar
Fairburn, CG, Beglin, SJ (1994). Assessment of eating disorders: interview or self-report questionnaire? International Journal of Eating Disorders 16, 363–370.Google Scholar
Fava, M, Judge, R, Hoog, SL, Nilsson, ME, Koke, SC (2000). Fluoxetine versus sertraline and paroxetine in major depressive disorder: changes in weight with long-term treatment. Journal of Clinical Psychiatry 61, 863–867.Google Scholar
Field, M, Cox, WM (2008). Attentional bias in addictive behaviors: a review of its development, causes, and consequences. Drug Alcohol Dependence 97, 1–20.Google Scholar
Field, M, Munafo, MR, Franken, IH (2009). A meta-analytic investigation of the relationship between attentional bias and subjective craving in substance abuse. Psychological Bulletin 135, 589–607.Google Scholar
German, CL, Baladi, MG, McFadden, LM, Hanson, GR, Fleckenstein, AE (2015). Regulation of the dopamine and vesicular monoamine transporters: pharmacological targets and implications for disease. Pharmacological Reviews 67, 1005–24.CrossRefGoogle ScholarPubMed
Gordon, I, Weizman, R, Rehavi, M (1996). Modulatory effect of agents active in the presynaptic dopaminergic system on the striatal dopamine transporter. European Journal of Pharmacology 298, 27–30.Google Scholar
Haider, S, Haleem, DJ (2000). Decreases of brain serotonin following a food restriction schedule of 4 weeks in male and female rats. Medical Science Monitor 6, 1061–1067.Google ScholarPubMed
Halford, JC, Harrold, JA, Boyland, EJ, Lawton, CL, Blundell, JE (2007). Serotonergic drugs : effects on appetite expression and use for the treatment of obesity. Drugs 67, 27–55.Google Scholar
Hardman, CA, Scott, J, Field, M, Jones, A (2014). To eat or not to eat. The effects of expectancy on reactivity to food cues. Appetite 76, 153–160.CrossRefGoogle ScholarPubMed
Kelley, AE, Baldo, BA, Pratt, WE, Will, MJ (2005). Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiology and Behavior 86, 773–795.CrossRefGoogle ScholarPubMed
Kilbourn, MR, Sherman, PS, Pisani, T (1992). Repeated reserpine administration reduces in vivo [18F]GBR 13119 binding to the dopamine uptake site. European Journal of Pharmacology 216, 109–112.CrossRefGoogle Scholar
Koopman, KE, Booij, J, Fliers, E, Serlie, MJ, la Fleur, SE (2013). Diet-induced changes in the Lean Brain: Hypercaloric high-fat-high-sugar snacking decreases serotonin transporters in the human hypothalamic region. Molecular Metabolism 2, 417–422.Google Scholar
Koopman, KE, Caan, MW, Nederveen, AJ, Pels, A, Ackermans, MT, Fliers, E, la Fleur, SE, Serlie, MJ (2014 a). Hypercaloric diets with increased meal frequency, but not meal size, increase intrahepatic triglycerides: a randomized controlled trial. Hepatology 60, 545–553.Google Scholar
Koopman, KE, la Fleur, SE, Fliers, E, Serlie, MJ, Booij, J (2012). Assessing the optimal time point for the measurement of extrastriatal serotonin transporter binding with 123I-FP-CIT SPECT in healthy, male subjects. Journal of Nuclear Medicine 53, 1087–1090.Google Scholar
Koopman, KE, Roefs, A, Elbers, C, Fliers, E, Booij, J, Serlie, MJ, la Fleur, SE (2014 b). Striatal dopamine transporter binding correlates with body composition, energy expenditure, and visual attention bias for food-related cues. Diabetes 63, A519.Google Scholar
Kuikka, JT, Tammela, L, Karhunen, L, Rissanen, A, Bergstrom, KA, Naukkarinen, H, Vanninen, E, Karhu, J, Lappalainen, R, Repo-Tiihonen, E, Tiihonen, J, Uusitupa, M (2001). Reduced serotonin transporter binding in binge eating women. Psychopharmacology 155, 310–314.Google Scholar
Lam, DD, Heisler, LK (2007). Serotonin and energy balance: molecular mechanisms and implications for type 2 diabetes. Expert Reviews in Molecular Medicine 9, 1–24.CrossRefGoogle ScholarPubMed
Luce, KH, Crowther, JH (1999). The reliability of the eating disorder examination-self-report questionnaire version (EDE-Q). International Journal of Eating Disorders 25, 349–351.Google Scholar
Mathews, TA, Fedele, DE, Coppelli, FM, Avila, AM, Murphy, DL, Andrews, AM (2004). Gene dose-dependent alterations in extraneuronal serotonin but not dopamine in mice with reduced serotonin transporter expression. Journal of Neuroscience Methods 140, 169–181.CrossRefGoogle Scholar
Myerson, J, Green, L, Warusawitharana, M (2001). Area under the curve as a measure of discounting. Journal of the Experimental Analysis of Behavior 76, 235–243.Google Scholar
Nijs, IM, Franken, IH, Muris, P (2007). The modified trait and state food-cravings questionnaires: development and validation of a general index of food craving. Appetite 49, 38–46.Google Scholar
Nijs, IM, Muris, P, Euser, AS, Franken, IH (2010). Differences in attention to food and food intake between overweight/obese and normal-weight females under conditions of hunger and satiety. Appetite 54, 243–254.CrossRefGoogle ScholarPubMed
Palmiter, RD (2008). Dopamine signaling in the dorsal striatum is essential for motivated behaviors: lessons from dopamine-deficient mice. Annals of the New York Academy of Sciences 1129, 35–46.Google Scholar
Patton, JH, Stanford, MS, Barratt, ES (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology 51, 768–774.Google Scholar
Raeder, MB, Bjelland, I, Emil, VS, Steen, VM (2006). Obesity, dyslipidemia, and diabetes with selective serotonin reuptake inhibitors: the hordaland health study. Journal of Clinical Psychiatry 67, 1974–1982.Google Scholar
Rattray, M, Baldessari, S, Gobbi, M, Mennini, T, Samanin, R, Bendotti, C (1996). p-Chlorphenylalanine changes serotonin transporter mRNA levels and expression of the gene product. Journal of Neurochemistry 67, 463–472.Google Scholar
Rothman, KJ (2008). BMI-related errors in the measurement of obesity. International Journal of Obesity 32 (Suppl. 3), S56–S59.Google Scholar
Saller, CF, Stricker, EM (1976). Hyperphagia and increased growth in rats after intraventricular injection of 5,7-dihydroxytryptamine. Science 192, 385–387.Google Scholar
Schag, K, Schonleber, J, Teufel, M, Zipfel, S, Giel, KE (2013). Food-related impulsivity in obesity and binge eating disorder–a systematic review. Obesity Reviews 14, 477–495.Google Scholar
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.CrossRefGoogle ScholarPubMed
Smith, SR, Weissman, NJ, Anderson, CM, Sanchez, M, Chuang, E, Stubbe, S, Bays, H, Shanahan, WR (2010). Multicenter, placebo-controlled trial of lorcaserin for weight management. New England Journal of Medicine 363, 245–256.CrossRefGoogle ScholarPubMed
Tetley, A, Brunstrom, J, Griffiths, P (2009). Individual differences in food-cue reactivity. The role of BMI and everyday portion-size selections. Appetite 52, 614–620.CrossRefGoogle ScholarPubMed
Thomsen, G, Ziebell, M, Jensen, PS, da Cuhna-Bang, S, Knudsen, GM, Pinborg, LH (2012). No correlation between body mass index and striatal dopamine transporter availability in healthy volunteers using SPECT and [I]PE2I. Obesity 21, 1803–1806.Google Scholar
Tindell, AJ, Berridge, KC, Zhang, J, Pecina, S, Aldridge, JW (2005). Ventral pallidal neurons code incentive motivation: amplification by mesolimbic sensitization and amphetamine. European Journal of Neuroscience 22, 2617–2634.CrossRefGoogle ScholarPubMed
van de Giessen, E, Celik, F, Schweitzer, DH, van den Brink, W, Booij, J (2014). Dopamine D2/3 receptor availability and amphetamine-induced dopamine release in obesity. Journal of Psychopharmacology 28, 866–873.Google Scholar
van de Giessen, E, Hesse, S, Caan, MW, Zientek, F, Dickson, JC, Tossici-Bolt, L, Sera, T, Asenbaum, S, Guignard, R, Akdemir, UO, Knudsen, GM, Nobili, F, Pagani, M, Vander, BT, Van, LK, Varrone, A, Tatsch, K, Booij, J, Sabri, O (2013). No association between striatal dopamine transporter binding and body mass index: a multi-center European study in healthy volunteers. Neuroimage 64, 61–67.CrossRefGoogle ScholarPubMed
van Strien, T, Frijters, JE, Bergers, GP, Defares, PB (1986). Dutch eating behaviour questionnaire for assessment of restrained, emotional and external eating behaviour. International Journal of Eating Disorders 5, 295–315.Google Scholar
Volkow, ND, Wang, GJ, Baler, RD (2011). Reward, dopamine and the control of food intake: implications for obesity. Trends Cognitive Sciences 15, 37–46.Google Scholar
Waldbillig, RJ, Bartness, TJ, Stanley, BG (1981). Increased food intake, body weight, and adiposity in rats after regional neurochemical depletion of serotonin. Journal of Comparative and Physiological Psychology 95, 391–405.Google Scholar
Wang, GJ, Volkow, ND, Logan, J, Pappas, NR, Wong, CT, Zhu, W, Netusil, N, Fowler, JS (2001). Brain dopamine and obesity. Lancet 357, 354–357.Google Scholar
Werthmann, J, Field, M, Roefs, A, Nederkoorn, C, Jansen, A (2014 a). Attention bias for chocolate increases chocolate consumption–an attention bias modification study. Journal of Behavior Therapy and Experimental Psychiatry 45, 136–143.CrossRefGoogle ScholarPubMed
Werthmann, J, Renner, F, Roefs, A, Huibers, MJ, Plumanns, L, Krott, N, Jansen, A (2014 b). Looking at food in sad mood: do attention biases lead emotional eaters into overeating after a negative mood induction? Eating Behaviors 15, 230–236.Google Scholar
Werthmann, J, Roefs, A, Nederkoorn, C, Jansen, A (2013). Desire lies in the eyes: attention bias for chocolate is related to craving and self-endorsed eating permission. Appetite 70, 81–89.Google Scholar
Wittmann, M, Leland, DS, Paulus, MP (2007). Time and decision making: differential contribution of the posterior insular cortex and the striatum during a delay discounting task. Experimental Brain Research 179, 643–653.Google Scholar
Zhuang, X, Oosting, RS, Jones, SR, Gainetdinov, RR, Miller, GW, Caron, MG, Hen, R (2001). Hyperactivity and impaired response habituation in hyperdopaminergic mice. Proceedings of the National Academy of Sciences USA 98, 1982–1987.Google Scholar
Supplementary material: PDF

Koopman supplementary material

Figure S1 and Table S1

Download Koopman supplementary material(PDF)
PDF 179.6 KB