Association of Body Mass and Brain Activation during Gastric Distention: Implications for Obesity

Tomasi, Dardo; Wang, Gene-Jack; Wang, Ruiliang; Backus, Walter; Geliebter, Allan; Telang, Frank; Jayne, Millar C.; Wong, Christopher; Fowler, Joanna S.; Volkow, Nora D.

doi:10.1371/journal.pone.0006847

Title: Association of Body Mass and Brain Activation during Gastric Distention: Implications for Obesity

Journal Article · 31 August 2009 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0006847 · OSTI ID:1627383

Tomasi, Dardo ^[1]; Wang, Gene-Jack ^[2]; Wang, Ruiliang ^[3]; Backus, Walter ^[4]; Geliebter, Allan ^[5]; Telang, Frank ^[6]; Jayne, Millar C. ^[6]; Wong, Christopher ^[6]; Fowler, Joanna S. ^[7]; Volkow, Nora D. ^[6]

National Institutes of Health (NIH), Bethesda, MD (United States); DOE/OSTI
Brookhaven National Laboratory (BNL), Upton, NY (United States); Icahn School of Medicine at Mount Sinai, New York, NY (United States)
Brookhaven National Laboratory (BNL), Upton, NY (United States).
State University of New York (SUNY), Stony Brook, NY (United States)
Columbia University, New York, NY (United States)
National Institutes of Health (NIH), Bethesda, MD (United States)
Brookhaven National Laboratory (BNL), Upton, NY (United States).; Icahn School of Medicine at Mount Sinai, New York, NY (United States)

Gastric distention (GD), as it occurs during meal ingestion, signals a full stomach and it is one of the key mechanisms controlling food intake. Previous studies on GD showed lower activation of the amygdala for subjects with higher body mass index (BMI). Since obese subjects have dopaminergic deficits that correlate negatively with BMI and the amygdala is innervated by dopamine neurons, we hypothesized that BMI would correlate negatively with activation not just in the amygdala but also in other dopaminergic brain regions (midbrain and hypothalamus). We used functional magnetic resonance imaging (fMRI) to evaluate brain activation during GD in 24 healthy subjects with BMI range of 20–39 kg/m2 . Using multiple regression and cross-correlation analyses based on a family-wise error corrected threshold P = 0.05, we show that during slow GD to maximum volumes of 500 ml and 700 ml subjects with increased BMI had increased activation in cerebellum and left posterior insula, and decreased activation of dopaminergic (amygdala, midbrain, hypothalamus, thalamus) and serotonergic (pons) brain regions and anterior insula, regions that were functionally interconnected with one another. The negative correlation between BMI and BOLD responses to gastric distention in dopaminergic (midbrain, hypothalamus, amygdala, thalamus) and serotonergic (pons) brain regions is consistent with disruption of dopaminergic and serotonergic signaling in obesity. In contrast the positive correlation between BMI and BOLD responses in posterior insula and cerebellum suggests an opposing mechanism that promotes food intake in obese subjects that may underlie their ability to consume at once large food volumes despite increasing gastric distention.

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Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: National Center for Research Resources (NCRR); National Institute on Drug Abuse; National Institutes on Alcoholism and Alcohol Abuse; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0012704

OSTI ID:: 1627383

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 8 Vol. 4; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Neuromodulatory Role of Serotonin in the Ferret Thalamus Monckton, James E.; McCormick, David A. Journal of Neurophysiology, Vol. 87, Issue 4 https://doi.org/10.1152/jn.00650.2001	journal	April 2002
Hypothalamo-Cerebellar and Cerebello-Hypothalamic Pathways: A Review and Hypothesis Concerning Cerebellar Circuits Which May Influence Autonomic Centers and Affective Behavior Haines, D. E.; Dietrichs, E.; Sowa, T. E. Brain, Behavior and Evolution, Vol. 24, Issue 4 https://doi.org/10.1159/000121317	journal	January 1984
Odorant-Induced and Sniff-Induced Activation in the Cerebellum of the Human Sobel, Noam; Prabhakaran, Vivek; Hartley, Catherine A. The Journal of Neuroscience, Vol. 18, Issue 21 https://doi.org/10.1523/JNEUROSCI.18-21-08990.1998	journal	November 1998
Brain Mechanisms of Propofol-Induced Loss of Consciousness in Humans: a Positron Emission Tomographic Study Fiset, Pierre; Paus, Tomás; Daloze, Thierry The Journal of Neuroscience, Vol. 19, Issue 13 https://doi.org/10.1523/JNEUROSCI.19-13-05506.1999	journal	July 1999
Amygdalo-Hypothalamic Circuit Allows Learned Cues to Override Satiety and Promote Eating Petrovich, Gorica D.; Setlow, Barry; Holland, Peter C. The Journal of Neuroscience, Vol. 22, Issue 19 https://doi.org/10.1523/JNEUROSCI.22-19-08748.2002	journal	October 2002
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Prefronto-cerebellar neuromodulation affects appetite in obesity Marron, Elena M.; Viejo-Sobera, Raquel; Cuatrecasas, Guillem International Journal of Obesity, Vol. 43, Issue 10 https://doi.org/10.1038/s41366-018-0278-8	journal	December 2018
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Hypothalamic metabolic compartmentation during appetite regulation as revealed by magnetic resonance imaging and spectroscopy methods Lizarbe, Blanca; Benitez, Ania; Peláez Brioso, Gerardo A. Frontiers in Neuroenergetics, Vol. 5 https://doi.org/10.3389/fnene.2013.00006	journal	January 2013
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Implementation of a New Food Picture Database in the Context of fMRI and Visual Cognitive Food-Choice Task in Healthy Volunteers Gautier, Yentl; Meurice, Paul; Coquery, Nicolas Frontiers in Psychology, Vol. 10 https://doi.org/10.3389/fpsyg.2019.02620	journal	November 2019
Endogenous GLP-1 mediates postprandial reductions in activation in central reward and satiety areas in patients with type 2 diabetes ten Kulve, Jennifer S.; Veltman, Dick J.; van Bloemendaal, Liselotte Diabetologia, Vol. 58, Issue 12 https://doi.org/10.1007/s00125-015-3754-x	journal	September 2015
Mood Disorders and Obesity: Understanding Inflammation as a Pathophysiological Nexus Soczynska, Joanna K.; Kennedy, Sidney H.; Woldeyohannes, Hanna O. NeuroMolecular Medicine, Vol. 13, Issue 2 https://doi.org/10.1007/s12017-010-8140-8	journal	December 2010
Visceral adiposity and insular networks: associations with food craving Contreras-Rodríguez, Oren; Cano, Marta; Vilar-López, Raquel International Journal of Obesity, Vol. 43, Issue 3 https://doi.org/10.1038/s41366-018-0173-3	journal	August 2018
Prefronto-cerebellar neuromodulation affects appetite in obesity Marron, Elena M.; Viejo-Sobera, Raquel; Cuatrecasas, Guillem International Journal of Obesity, Vol. 43, Issue 10 https://doi.org/10.1038/s41366-018-0278-8	journal	December 2018
The role of glucagon-like peptide-1 impairment in obesity and potential therapeutic implications Madsbad, S. Diabetes, Obesity and Metabolism, Vol. 16, Issue 1 https://doi.org/10.1111/dom.12119	journal	May 2013
Obesity and addiction: neurobiological overlaps: Overlaps between drug and food addiction Volkow, N. D.; Wang, G. -J.; Tomasi, D. Obesity Reviews, Vol. 14, Issue 1 https://doi.org/10.1111/j.1467-789x.2012.01031.x	journal	September 2012
Beyond Pharmacotherapy: Understanding the Links between Obesity and Chronic Mental Illness Taylor, Valerie H.; McIntyre, Roger S.; Remington, Gary The Canadian Journal of Psychiatry, Vol. 57, Issue 1 https://doi.org/10.1177/070674371205700103	journal	January 2012
Early Life Stress Associated With Increased Striatal N -Acetyl-Aspartate: Cerebrospinal Fluid Corticotropin-Releasing Factor Concentrations, Hippocampal Volume, Body Mass, and Behavioral Correlates Coplan, Jeremy D.; Lu, Dunyue; El Sehamy, Alexander M. Chronic Stress, Vol. 2 https://doi.org/10.1177/2470547018768450	journal	January 2018
Striatocortical pathway dysfunction in addiction and obesity: differences and similarities Tomasi, Dardo; Volkow, Nora D. Critical Reviews in Biochemistry and Molecular Biology, Vol. 48, Issue 1 https://doi.org/10.3109/10409238.2012.735642	journal	November 2012

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