Intrinsic brain subsystem associated with dietary restraint, disinhibition and hunger: an fMRI study
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Eating behaviors are closely related to body weight, and eating traits are depicted in three dimensions: dietary restraint, disinhibition, and hunger. The current study aims to explore whether these aspects of eating behaviors are related to intrinsic brain activation, and to further investigate the relationship between the brain activation relating to these eating traits and body weight, as well as the link between function connectivity (FC) of the correlative brain regions and body weight. Our results demonstrated positive associations between dietary restraint and baseline activation of the frontal and the temporal regions (i.e., food reward encoding) and the limbic regions (i.e., homeostatic control, including the hypothalamus). Disinhibition was positively associated with the activation of the frontal motivational system (i.e., OFC) and the premotor cortex. Hunger was positively related to extensive activations in the prefrontal, temporal, and limbic, as well as in the cerebellum. Within the brain regions relating to dietary restraint, weight status was negatively correlated with FC of the left middle temporal gyrus and left inferior temporal gyrus, and was positively associated with the FC of regions in the anterior temporal gyrus and fusiform visual cortex. Weight status was positively associated with the FC within regions in the prefrontal motor cortex and the right ACC serving inhibition, and was negatively related with the FC of regions in the frontal cortical-basal ganglia-thalamic circuits responding to hunger control. Our data depicted an association between intrinsic brain activation and dietary restraint, disinhibition, and hunger, and presented the links of their activations and FCs with weight status.
KeywordsObesity Functional magnetic resonance imaging Resting state Functional connectivity Three factor eating questionnaire
Compliance with ethical standards
All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.
This paper is supported by National Natural Science Foundation of China under Grant Nos. 61473235, 81271549, 61131003, 81470816, 61431013, 81201081, 81227901, 81120108005; the Fundamental Research Funds for the Central Universities No. QN2012031; the Shaanxi Provincial Natural Science Foundation under Grant No. 2015JM3117.
Data collection and sharing project was funded in part by the New York State Office of Mental Health and Research Foundation for Mental Hygiene. Additional project support provided by the NKI Center for Advanced Brain Imaging (CABI), the Brain Research Foundation (Chicago, IL), the Stavros Niarchos Foundation, and NIH grant P50 MH086385-S1. The project Directors were F. Xavier Castellanos, Bennett Leventhal, and Michael Milham. The Project Coordinator was Kate Nooner. David Gutman and Maarten Mennes finished Computational Infrastructure and Data Analytic Development/Support. The NKI/Rockland Sample Team included Melissa Benedict, Bharat Biswal, Barbara Coffey, Stan Colcombe, David Guilfoyle, David Gutman, Harold S. Koplewicz, Matthew Hoptman, Dan Javitt, Larry Maayan, Maarten Mennes, Kate Nooner, Nunzio Pomara. I would like to express my gratitude to Heather S. Pixley for the English editing of this paper.
Conflict of interest
The authors declare that they have no conflicts of interest.
Informed consent was obtained when study participants joined the International Neuroimaging Data-sharing Initiative (INDI) database.
- Bond, M. J., McDowell, A. J., & Wilkinson, J. Y. (2001). The measurement of dietary restraint, disinhibition and hunger: an examination of the factor structure of the Three Factor Eating Questionnaire (TFEQ). International Journal of Obesity and Related Metabolic Disorders, 25(6), 900–906. doi: 10.1038/sj.ijo.0801611.CrossRefPubMedGoogle Scholar
- Born, J. M., Lemmens, S. G., Rutters, F., Nieuwenhuizen, A. G., Formisano, E., Goebel, R., et al. (2010). Acute stress and food-related reward activation in the brain during food choice during eating in the absence of hunger. International Journal of Obesity, 34(1), 172–181. doi: 10.1038/ijo.2009.221.CrossRefPubMedGoogle Scholar
- Born, J. M., Lemmens, S. G., Martens, M. J., Formisano, E., Goebel, R., & Westerterp-Plantenga, M. S. (2011). Differences between liking and wanting signals in the human brain and relations with cognitive dietary restraint and body mass index. The American Journal of Clinical Nutrition, 94(2), 392–403.CrossRefPubMedGoogle Scholar
- Castellanos, E. H., Charboneau, E., Dietrich, M. S., Park, S., Bradley, B. P., Mogg, K., et al. (2009). Obese adults have visual attention bias for food cue images: evidence for altered reward system function. International Journal of Obesity, 33(9), 1063–1073. doi: 10.1038/ijo.2009.138.CrossRefPubMedGoogle Scholar
- DelParigi, A., Chen, K., Salbe, A. D., Reiman, E. M., & Tataranni, P. A. (2005). Sensory experience of food and obesity: a positron emission tomography study of the brain regions affected by tasting a liquid meal after a prolonged fast. NeuroImage, 24(2), 436–443. doi: 10.1016/j.neuroimage.2004.08.035.CrossRefPubMedGoogle Scholar
- Drapeau, V., Provencher, V., Lemieux, S., Despres, J. P., Bouchard, C., & Tremblay, A. (2003). Do 6-y changes in eating behaviors predict changes in body weight? Results from the Quebec Family Study. International Journal of Obesity and Related Metabolic Disorders, 27(7), 808–814.CrossRefPubMedGoogle Scholar
- García-García, I., Jurado, M. Á., Garolera, M., Segura, B., Sala-Llonch, R., Marqués-Iturria, I., et al. (2013). Alterations of the salience network in obesity: A resting-state fMRI study. Human Brain Mapping, 34(11), 2786–2797. doi: 10.1002/hbm.22104.
- Gu, H., Salmeron, B. J., Ross, T. J., Geng, X., Zhan, W., Stein, E. A., et al. (2010). Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity. NeuroImage, 53(2), 593–601. doi: 10.1016/j.neuroimage.2010.06.066.CrossRefPubMedPubMedCentralGoogle Scholar
- Hays, N. P., Bathalon, G. P., Roubenoff, R., McCrory, M. A., & Roberts, S. B. (2006). Eating Behavior and Weight Change in Healthy Postmenopausal Women: Results of a 4-Year Longitudinal Study. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 61(6), 608–615.CrossRefGoogle Scholar
- Hinton, E. C., Parkinson, J. A., Holland, A. J., Arana, F. S., C. Roberts, A., & Owen, A. M. (2004). Neural contributions to the motivational control of appetite in humans. European Journal of Neuroscience, 20(5), 1411–1418, doi: 10.1111/j.1460-9568.2004.03589.x.
- Hon, N., Epstein, R. A., Owen, A. M., & Duncan, J. (2006). Frontoparietal activity with minimal decision and control. The Journal of Neuroscience, 26(38), 9805–9809, doi: 10.1523/jneurosci.3165-06.2006.
- Killgore, W. D. S., Young, A. D., Femia, L. A., Bogorodzki, P., Rogowska, J., & Yurgelun-Todd, D. A. (2003). Cortical and limbic activation during viewing of high- versus low-calorie foods. NeuroImage, 19(4), 1381–1394, doi: 10.1016/S1053-8119(03)00191-5.
- Kullmann, S., Pape, A. A., Heni, M., Ketterer, C., Schick, F., Haring, H. U., et al. (2013). Functional network connectivity underlying food processing: disturbed salience and visual processing in overweight and obese adults. Cerebral Cortex, 23(5), 1247–1256. doi: 10.1093/cercor/bhs124.CrossRefPubMedGoogle Scholar
- Matthews, S. C., Paulus, M. P., Simmons, A. N., Nelesen, R. A., & Dimsdale, J. E. (2004). Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function. NeuroImage, 22(3), 1151–1156. doi: 10.1016/j.neuroimage.2004.03.005.CrossRefPubMedGoogle Scholar
- Molnar-Szakacs, I., Iacoboni, M., Koski, L., & Mazziotta, J. C. (2005). Functional Segregation within Pars Opercularis of the Inferior Frontal Gyrus: Evidence from fMRI Studies of Imitation and Action Observation. Cerebral Cortex, 15(7), 986–994. doi: 10.1093/cercor/bhh199.CrossRefPubMedGoogle Scholar
- Nooner, K. B., Colcombe, S., Tobe, R., Mennes, M., Benedict, M., Moreno, A., et al. (2012). The NKI-Rockland Sample: A Model for Accelerating the Pace of Discovery Science in Psychiatry. [Review]. Frontiers in Neuroscience, 6, doi: 10.3389/fnins.2012.00152.
- Ochner, C. N., Laferrère, B., Afifi, L., Atalayer, D., Geliebter, A., & Teixeira, J. (2012). Neural responsivity to food cues in fasted and fed states pre and post gastric bypass surgery. Neuroscience Research, 74(2), 138–143. doi: 10.1016/j.neures.2012.08.002.CrossRefPubMedPubMedCentralGoogle Scholar
- Riou, M.-È., Doucet, É., Provencher, V., Weisnagel, S. J., Piché, M.-È., Dubé, M.-C., et al. (2011). Influence of physical activity participation on the associations between eating behaviour traits and body mass index in healthy postmenopausal women. Journal of Obesity, 2011, 9. doi: 10.1155/2011/465710.CrossRefGoogle Scholar
- Rothemund, Y., Preuschhof, C., Bohner, G., Bauknecht, H.-C., Klingebiel, R., Flor, H., et al. (2007). Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. NeuroImage, 37(2), 410–421. doi: 10.1016/j.neuroimage.2007.05.008.CrossRefPubMedGoogle Scholar
- Siep, N., Roefs, A., Roebroeck, A., Havermans, R., Bonte, M. L., & Jansen, A. (2009). Hunger is the best spice: an fMRI study of the effects of attention, hunger and calorie content on food reward processing in the amygdala and orbitofrontal cortex. Behavioural Brain Research, 198(1), 149–158. doi: 10.1016/j.bbr.2008.10.035.CrossRefPubMedGoogle Scholar
- Tataranni, P. A., Gautier, J.-F., Chen, K., Uecker, A., Bandy, D., Salbe, A. D., et al. (1999). Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proceedings of the National Academy of Sciences, 96(8), 4569–4574. doi: 10.1073/pnas.96.8.4569.CrossRefGoogle Scholar
- Westenhoefer, J., Stunkard, A. J., & Pudel, V. (1999). Validation of the flexible and rigid control dimensions of dietary restraint. International Journal of Eating Disorders, 26(1), 53–64. doi: 10.1002/(SICI)1098-108X(199907)26:1<53::AID-EAT7>3.0.CO;2-N.CrossRefPubMedGoogle Scholar