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Relationship of Dopamine Type 2 Receptor Binding Potential With Fasting Neuroendocrine Hormones and Insulin Sensitivity in Human Obesity
Open accessAbstract
OBJECTIVE: Midbrain dopamine (DA) neurons, which are involved with reward and motivation, are modulated by hormones that regulate food intake (insulin, leptin, and acyl ghrelin [AG]). We hypothesized that these hormones are associated with deficits in DA signaling in obesity. RESEARCH DESIGN AND METHODS: We assessed the relationships between fasting levels of insulin and leptin, and AG, BMI, and insulin sensitivity index (SI) with the availability of central DA type 2 receptor (D2R). We measured D2R availability using positron emission tomography and [18F]fallypride (radioligand that competes with endogenous DA) in lean (n = 8) and obese (n = 14) females. Fasting hormones were collected prior to scanning and SI was determined by modified oral glucose tolerance test. RESULTS: Parametric image analyses revealed associations between each metabolic measure and D2R. The most extensive findings were negative associations of AG with clusters involving the striatum and inferior temporal cortices. Regional regression analyses also found extensive negative relationships between AG and D2R in the caudate, putamen, ventral striatum (VS), amygdala, and temporal lobes. SI was negatively associated with D2R in the VS, while insulin was not. In the caudate, BMI and leptin were positively associated with D2R availability. The direction of associations of leptin and AG with D2R availability are consistent with their opposite effects on DA levels (decreasing and increasing, respectively). After adjusting for BMI, AG maintained a significant relationship in the VS. We hypothesize that the increased D2R availability in obese subjects reflects relatively reduced DA levels competing with the radioligand. CONCLUSIONS: Our findings provide evidence for an association between the neuroendocrine hormones and DA brain signaling in obese females.
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“This is consistent with preclinical (40) and clinical (41) studies showing dynamic associations between the changes in neuroendocrine hormones (e.g. insulin, leptin, ghrelin) triggered by food restriction and brain DA signalling and those of recent reports of a relationship between addictive personality and maladaptive eating behaviours following bariatric surgery (42,43).”
From Obesity and addiction: Neurobiological overlaps (2013) · cites this paper as [41]
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InfluentialUpadhyay, J., Farr, O. M., Perakakis, N., Ghaly, W., & Mantzoros, C. S. (2017) · Medical Clinics of North America · doi:10.1016/j.mcna.2017.08.004 · Cited by 425
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Ziauddeen, H., Alonso‐Alonso, M., Hill, J. O., Kelley, M. J., & Khan, N. A. (2015) · Advances in Nutrition · doi:10.3945/an.115.008268 · Cited by 157
Basal Ganglia Dysfunction Contributes to Physical Inactivity in Obesity
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“However, more recent work has called this finding into question (Caravaggio et al., 2015; Cosgrove et al., 2015; Dunn et al., 2012; Guo et al., 2014; Karlsson et al., 2015, 2016; Steele et al., 2010; Tuominen et al., 2015).”
InfluentialHeni, M., Wagner, R., Kullmann, S., Gancheva, S., Roden, M., Peter, A., Stefan, N., Preissl, H., Häring, H.-U., & Fritsche, A. (2017) · Diabetes · doi:10.2337/db16-1380 · Cited by 115
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“Dunn and colleagues also used [(18)F]fallypride to determine D2/D3-receptor BP in lean and obese women (39).”
MethodStriatal dopamine regulates systemic glucose metabolism in humans and mice
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Exercise restores brain insulin sensitivity in sedentary adults who are overweight and obese
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“The power of our study to detect differences in D2R BPND estimates between normal-weight and obese groups as well as to detect correlations between D2R BPND estimates and BMI in the obese group was calculated based on results from previous studies of D2=D3 receptor availability (de Weijer et al., 2011; Dunn et al., 20…”
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“Furthermore, hormones that have been shown to change after RYGB, such as leptin and ghrelin [35,36,37], are also known to modulate the dopaminergic reward system [38,39,40,41] as well as alcohol consumption [41,42,43].”
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“Contrarily, other groups have shown higher striatal DA in obese individuals [77,99].”
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BackgroundAssociations between dopamine D2 receptor availability and BMI depend on age
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Insulin, Central Dopamine D2 Receptors, and Monetary Reward Discounting in Obesity
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“The unchanged ghrelin levels after RYGB in this study are in line with previous findings (Stoeckli et al., 2004) but in contrast to the study by Dunn et al., we observed no correlations between changes in BPND and changes in plasma levels of ghrelin (Dunn et al., 2012).”
InfluentialRoux-en-Y Gastric Bypass Increases Intravenous Ethanol Self-Administration in Dietary Obese Rats
Polston, J. E., Pritchett, C. E., Tomasko, J. M., Rogers, A. M., Leggio, L., Thanos, P. K., Volkow, N. D., & Hajnal, A. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083741 · Cited by 50
“Notably, hormones that have been shown to change after RYGB, such as leptin and ghrelin [26,27,28], are also known to modulate the dopaminergic reward system [29,30,31] as well as EtOH consumption [32,33].”
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Do Dopaminergic Impairments Underlie Physical Inactivity in People with Obesity?
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“Adding to the complexity of this issue, research has shown both that obese individuals have less D2 receptor binding compared to normal and overweight controls (Wang et al., 2001), as well as that higher BMI is related to increased D2 availability (Dunn et al., 2012).”
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“Furthermore, recent research suggests that hyperinsulinemia in response to high-glycemic food intake may be responsible for driving neurochemical changes associated with HP food addiction (Caravaggio et al., 2015; Caravaggio et al., 2018; Dunn et al., 2012).”
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“ability in NAc and VTA being found by several groups [84–86], while no difference [87, 88] or a rise [89, 90] were”
Effort-based decision-making is affected by overweight/obesity in major depressive disorder
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“, 2012 [43] [18F]-Fallypride D2/D3 BPND CAU, PUT, vSTR, SN 8:0 NW 23(2) <25 40(9) Fasted (8 h before scanning) None Secondary OB > NW in CAU 14:0 OB 40(5) >30 40(8)”
MethodResultLower dopamine tone in the striatum is associated with higher body mass index
Lee, Y., Kroemer, N. B., Oehme, L., Beuthien‐Baumann, B., Goschke, T., & Smolka, M. N. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.03.009 · Cited by 38
Neurobehavioral determinants of nutritional security in fetal growth–restricted individuals
Portella, A. K., & Silveira, P. P. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12390 · Cited by 37
Incidental rewarding cues influence economic decisions in people with obesity
Simmank, J., Murawski, C., Bode, S., & Horstmann, A. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00278 · Cited by 32
“…in Behavioral Neuroscience | www.frontiersin.org 12 October 2015 | Volume 9 | Article 278 by non-linear changes within the central balance of phasic and tonic dopaminergic signaling (Wang et al., 2001; de Weijer et al., 2011; Dunn et al., 2012; Guo et al., 2014; Horstmann et al., 2015a).”
BackgroundMethodInfluentialVinik, A. I., Cincotta, A. H., Scranton, R. E., Bohannon, N. J. V., Ezrokhi, M., & Gaziano, J. M. (2012) · Endocrine Practice · doi:10.4158/ep12187.or · Cited by 33
Orellana, E. R., Jamis, C., Horvath, N., & Hajnal, A. S. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.08.004 · Cited by 33
Mansur, R. B., Fries, G. R., Subramaniapillai, M., Frangou, S., Felice, F. G. D., Rasgon, N., McEwen, B. S., Brietzke, E. M., & McIntyre, R. S. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.10.020 · Cited by 34
Hartmann, H., Pauli, L. K., Janssen, L. K., Hühn, S., Ceglarek, U., & Horstmann, A. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12917 · Cited by 33
MacIntosh, B. J., Shirzadi, Z., Atwi, S., Detre, J. A., Dolui, S., Bryan, R. N., Launer, L. J., & Swardfager, W. (2019) · Human Brain Mapping · doi:10.1002/hbm.24844 · Cited by 33
“…changes in neural circuits, such as the prefrontal and ventral striatal regions involved in food reward processing, self-regulation and stress (Dunn et al., 2012; Ottino-González et al., 2017), which could influence regional neurovascular metabolism and hence, CBF. Evidence in support of…”
BackgroundSerotonin Transporter Binding in the Diencephalon Is Reduced in Insulin-Resistant Obese Humans
Versteeg, R. I., Koopman, K. E., Booij, J., Ackermans, M. T., Unmehopa, U. A., Fliers, E., la Fleur, S. E., & Serlie, M. J. M. (2016) · Neuroendocrinology · doi:10.1159/000450549 · Cited by 32
“Obese subjects have lower striatal dopamine D2/3 receptor (D2/3R) binding availability (13) and striatal D2/3R binding is associated with insulin sensitivity (14).”
The Role of Bromocriptine-Qr in the Management of Type 2 Diabetes Expert Panel Recommendations
Garber, A. J., Blonde, L., Bloomgarden, Z. T., Handelsman, Y., & Dagogo-Jack, S. E. (2013) · Endocrine Practice · doi:10.4158/ep12325.or · Cited by 31
Dopaminergic Pathways in Obesity-Associated Inflammation
Leite, F., & Ribeiro, L. V. P. T. (2019) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-019-09863-0 · Cited by 34
“…et al. 2008; Stice et al. 2013; Kenny 2011; Volkow and Wise 2005) and clinical studies (Wang et al. 2001; Haltia et al. 2007; Volkow et al. 2008; Dunn et al. 2012) suggested that overeating, particularly high-fat high-sugar diets, and obesity induces alterations on neural brain regions of the…”
BackgroundConverging vulnerability factors for compulsive food and drug use
Serafine, K. M., O’Dell, L. E., & Zorrilla, E. P. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108556 · Cited by 29
Kroemer, N. B., Burrasch, C., & Hellrung, L. (2016) · Progress in brain research · doi:10.1016/bs.pbr.2016.06.009 · Cited by 31
Savage, S. W., Zald, D. H., Cowan, R. L., Volkow, N. D., Marks-Shulman, P. A., Kessler, R. M., Abumrad, N. N., & Dunn, J. P. (2014) · Obesity · doi:10.1002/oby.20690 · Cited by 27
“We previously demonstrated that D2/D3R BPND in the striatum is negatively associated with fasting acyl ghrelin levels in a cohort of normal weight and obese females (10).”
Self-citationRaskin, P., & Cincotta, A. H. (2015) · Expert Review of Endocrinology & Metabolism · doi:10.1586/17446651.2016.1131119 · Cited by 28
O’Dell, L. E., & Nazarian, A. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.06.005 · Cited by 27
To Do or Not to Do: Dopamine, Affordability and the Economics of Opportunity
Beeler, J. A., & Mourra, D. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00006 · Cited by 28
Dorsal Striatal Dopamine, Food Preference and Health Perception in Humans
Wallace, D. L., Aarts, E., Dang, L. C., Greer, S. M., Jagust, W. J., & D’Esposito, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096319 · Cited by 24
“a positive relationship between binding and BMI, as found in [8]).”
BackgroundBabenko, V. N., Galyamina, A. G., Rogozin, I. B., Смагин, Д. А., & Kudryavtseva, N. N. (2020) · BMC Neuroscience · doi:10.1186/s12868-020-00560-w · Cited by 23
Obesity and Brain Positron Emission Tomography
Pak, K., Kim, S., & Kim, I. J. (2017) · Nuclear Medicine and Molecular Imaging · doi:10.1007/s13139-017-0483-8 · Cited by 23
“This inconsistency between studies may be related not only with the radiopharmaceuticals, but also with the experimental settings such as the time of the day, and food restriction [63].”
BackgroundKahleová, H., Tintěra, J., Thieme, L., Veleba, J., Klementová, M., Kudláčková, M., Malínská, H., Oliyarnyk, O., Marková, I., Haluzı́k, M., et al. (2019) · Clinical Nutrition · doi:10.1016/j.clnu.2020.10.005 · Cited by 20
Farr, O. M., & Mantzoros, C. S. (2016) · International Journal of Obesity · doi:10.1038/ijo.2016.231 · Cited by 20
Janssen, L. K., Herzog, N., Waltmann, M., Breuer, N., Wiencke, K., Rausch, F., Hartmann, H., Poessel, M., & Horstmann, A. (2019) · Current Addiction Reports · doi:10.1007/s40429-019-00268-w · Cited by 20
Obesity surgery: happy with less or eternally hungry?
Shin, A. C., & Berthoud, H. (2013) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.11.009 · Cited by 19
Striatal Dopamine Homeostasis is Altered in Mice Following Roux-en-Y Gastric Bypass Surgery
Reddy, I. A., Wasserman, D. H., Ayala, J. E., Hasty, A. H., Abumrad, N. N., & Galli, A. (2014) · ACS Chemical Neuroscience · doi:10.1021/cn500137d · Cited by 19
Self-citationStriatal Dopamine D2 Receptors Regulate Cost Sensitivity and Behavioral Thrift
Mourra, D., Gnazzo, F. G., Cobos, S., & Beeler, J. A. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.11.002 · Cited by 19
“Subsequent studies have yielded contradictory results (Volkow et al., 2008; de Weijer et al., 2011; Kessler et al., 2014; negative: Dunn et al., 2012; Eisenstein et al., 2013; de Weijer et al., 2014; Cosgrove et al., 2015; Karlsson et al., 2015; Tuominen et al., 2015).”
ResultEarly adversity and insulin: neuroendocrine programming beyond glucocorticoids
Batra, A., Latsko, M. S., Portella, A. K., & Silveira, P. P. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2021.09.003 · Cited by 17
Burke, M. V., & Small, D. M. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.02.036 · Cited by 17
la Fleur, S. E., & Serlie, M. J. M. (2014) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2014.06.001 · Cited by 16
Dunn, J. P., Abumrad, N. N., KESSLER, R. M., Patterson, B. W., Li, R., Marks–Shulman, P. A., & Tamboli, R. A. (2017) · Obesity · doi:10.1002/oby.22023 · Cited by 16
Self-citationBrain dopamine receptor system is not altered in obesity: Bayesian and frequentist meta‐analyses
Pak, K., & Nummenmaa, L. (2023) · Human Brain Mapping · doi:10.1002/hbm.26534 · Cited by 15
“One study with F18-Fallypride (Dunn et al., 2012) and two studies with C11-PHNO showed the higher DR availability in overweight/obese subjects while two studies with C11-Raclopride (Caravaggio et al., 2015; Haltia et al., 2008) and one study with I123-IBZM (van de Giessen et al., 2014) did not show the difference of D…”
BackgroundMethodResultInfluentialCaravaggio, F., Hahn, M., Nakajima, S., Gerretsen, P., Remington, G., & Graff-Guerrero, A. (2015) · Medical Hypotheses · doi:10.1016/j.mehy.2015.06.011 · Cited by 17
“These findings are consistent with previous PET studies which have employed other D2/3R radiotracers to examine the relationship between baseline D2/3R availability and insulin sensitivity [68,69].”
ResultRospond, B., Sadakierska−Chudy, A., Kazek, G., Krośniak, M., Bystrowska, B., & Filip, M. (2018) · Pharmacological Reports · doi:10.1016/j.pharep.2018.09.005 · Cited by 15
Striatal dopamine transporter changes after glucose loading in humans
Pak, K., Seo, S., Keun-young Kim, A., Lee, M. J., Shin, M., Suh, S., Im, H., Park, J., Kim, S., & Kim, I. J. (2019) · Diabetes Obesity and Metabolism · doi:10.1111/dom.13872 · Cited by 14
“As obesity can be defined as a BMI of 30 or more, individuals with both moderate and severe obesity can be included in the obese group in each study.(6,26,29) Moreover, as a fundamental limitation of DR availability acquired as assessed by PET scans is that endogenous dopamine competes with the radiopharmaceuticals fo…”
BackgroundThe dark side of compulsive eating and food addiction
Zorrilla, E. P., & Koob, G. F. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816207-1.00006-8 · Cited by 14
Ziomber, A., Rokita, E., Kaszuba-Zwoińska, J., Romańska, I., Michaluk, J., & Antkiewicz‐Michaluk, L. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00262 · Cited by 12
“, 2014) other experiments showed an opposite relationship (Dunn et al., 2012) or found no association between striatal DA D2 binding and BMI (Eisenstein et al.”
ResultHartmann, H., Janssen, L. K., Herzog, N., Morys, F., Fängström, D., Fallon, S. J., & Horstmann, A. (2023) · Appetite · doi:10.1016/j.appet.2023.106477 · Cited by 11
Cincotta, A. H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713255 · Cited by 11
Chamarthi, B., Vinik, A. I., Ezrokhi, M., & Cincotta, A. H. (2019) · Endocrinology Diabetes & Metabolism · doi:10.1002/edm2.101 · Cited by 10
Tabassum, A., Badulescu, S., Singh, E., Asoro, R., McIntyre, R. S., Teopiz, K. M., Llach, C.-D., Shah, H., & Mansur, R. B. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105907 · Cited by 9
“…co-occurrence of reward and metabolic dysfunction (e.g., IR) in highly prevalent and debilitating conditions like obesity (Ziauddeen et al., 2015; Dunn et al., 2012), depression (Satterthwaite et al., 2015; Treadway and Zald, 2011; Díaz-Carías et al., 2023), anxiety (Díaz-Carías et al., 2023;…”
BackgroundAl‐Alsheikh, A. S., Alabdulkader, S., Miras, A. D., & Goldstone, A. P. (2023) · Obesity Reviews · doi:10.1111/obr.13620 · Cited by 10
“64 By contrast, higher BMI has been associated with higher 18 F-fallypride BP in the dorsal and lateral striatum 59 ; in caudate 65 ; in midbrain, putamen, and ventral striatum, 66 and higher N-methyl benperidol BP in caudate.”
BackgroundTowards a translational approach to food addiction: Implications for bulimia nervosa
Leslie, M., Lambert, E., & Treasure, J. (2019) · Current Addiction Reports · doi:10.1007/s40429-019-00264-0 · Cited by 9
“[71] conducted a positron emission tomography (PET) study using the dopamine”
MethodDarcey, V. L., Guo, J., Chi, M., Chung, S. T., Courville, A. B., Gallagher, I., Herscovitch, P., Howard, R., LaNoire, M., Milley, L., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-02960-y · Cited by 18
Metadata
- Authors
- 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.
- Affiliations
- Vanderbilt University (US)
- National Institute on Drug Abuse (US)
- Washington University in St. Louis (US)
- Department of Surgery, Vanderbilt University School of Medicine, Nashville, Tennessee
- Corresponding author
- Dunn, Julia P.
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2012-04-11
- Volume
- 35
- Issue
- 5
- Pages
- 1105-1111
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- PMC
- PMC3329842
- OpenAlex
- W2003413351
- Cited by
- 148
- References
- 40
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 5 · 2023: 10 · 2022: 7 · 2021: 8 · 2020: 9 · 2019: 16 · 2018: 14 · 2017: 13 · 2016: 16 · 2015: 15 · 2014: 17 · 2013: 9 · 2012: 4
- FWCI
- 6.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Diabetes Care (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs (IK2 CX000943)
- Vanderbilt University
- National Institutes of Health (-015855, 5p60dk020593-31, DK 20593)
- Vanderbilt Digestive Diseases Research Center, Vanderbilt University Medical Center
- National Institute of Diabetes and Digestive and Kidney Diseases (DK058404, P60-DK020593, R01DK091748, DK 20593, DK 70860, R01DK070860, 56341, P30DK058404, P30DK056341, P30DK020593)
- National Institute of Environmental Health Sciences (K12ES015855)
- National Center for Research Resources (KL2RR024977, TL1RR024978, UL1RR024975)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- dopamine D2 receptor, obesity, insulin sensitivity, leptin, acylated ghrelin, insulin, neuroendocrine hormones, ventral striatum, caudate nucleus, putamen, amygdala, striatum, inferior temporal cortex, female, food intake regulation
- MeSH terms
- Adult, Basal Ganglia, Fasting, Female, Humans, Insulin Resistance, Middle Aged, Obesity, Body Mass Index, Receptors, Dopamine D2, Leptin, Positron-Emission Tomography, Ghrelin
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