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Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals
Abstract
The neural systems regulating food intake in obese individuals remain poorly understood. Previous studies applied positron emission tomography and manipulated hunger and satiety to investigate differences in appetitive processing between obese and normal-weight individuals. However, it is not known whether manipulation of stimulus value may yield different neural activity in obese as compared to control subjects when intrinsic physiological states are kept constant. We used functional magnetic resonance imaging to investigate 13 obese and 13 normal-weight subjects and manipulated food motivation by presenting visual food stimuli differing in their caloric content and energy density. In contrast to controls, obese women selectively activated the dorsal striatum while viewing high-caloric foods. Moreover, in the high-calorie condition body mass index (BMI) predicted activation in the dorsal striatum, anterior insula, claustrum, posterior cingulate, postcentral and lateral orbitofrontal cortex. The results indicate that in obese individuals simple visual stimulation with food stimuli activates regions related to reward anticipation and habit learning (dorsal striatum). Additionally, high-calorie food images yielded BMI-dependent activations in regions associated with taste information processing (anterior insula and lateral orbitofrontal cortex), motivation (orbitofrontal cortex), emotion as well as memory functions (posterior cingulate). Collectively, the results suggest that the observed activation is independent of the physiological states of hunger and satiation, and thus may contribute to pathological overeating and obesity. Some of the observed activations (dorsal striatum, orbitofrontal cortex) are likely to be dopamine-mediated.
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“Recent studies that used the conventional blood oxygenation level-dependent fMRI have shown selective overactivity in the nucleus accumbens and related brain areas in obese compared with lean individuals when shown imagines of highly palatable food (6)(7)(8)(9)(10)(11)”
From Effects of dietary glycemic index on brain regions related to reward and craving in men (2013) · cites this paper as [8]
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BackgroundThe effects of energy balance, obesity-proneness and sex on the neuronal response to sweet taste
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“1 NeuroAdaptations Group, Max Planck Institute of Psychiatry, Munich, Germany 2 Neuroscience Domain, Institute of Life and Health Sciences (ICVS), University of Minho, Braga, Portugal 3 ICVS/3B’s - PT Government Associate Laboratory, Braga/Guimarães, Portugal Edited by: John D. Salamone, University…”
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Effects of obesogenic diets on learning and habitual responding
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Pott, W., Albayrak, Ö., Hinney, A., Hebebrand, J., & Pauli‐Pott, U. (2013) · Obesity Facts · doi:10.1159/000348792 · Cited by 22
Watanabe, Y. (2013) · Medical Science Monitor · doi:10.12659/msm.889234 · Cited by 22
Insulin sensitivity and brain reward activation in overweight H ispanic girls: a pilot study
Adam, T. C., Tsao, S., Page, K. A., Hu, H., Hasson, R. E., & Goran, M. I. (2013) · Pediatric Obesity · doi:10.1111/j.2047-6310.2013.00210.x · Cited by 21
“Regions of interest were established based on the relevant literature (24,25) and a cluster threshold of 10 voxels.”
Yeung, A. W. K., & Wong, N. S. M. (2020) · Nutrients · doi:10.3390/nu12103010 · Cited by 21
“Indeed, when viewing high-caloric food pictures, women with obesity had a higher activity level in the striatum than women with normal-weight, and the activity levels of striatum, insula, and cingulate were positively correlated to the body mass index [35].”
BackgroundLi, L., Yu, H., Zhong, M., Liu, S., Wei, W., Meng, Y., Li, M., Li, T., & Wang, Q. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.955741 · Cited by 25
“(15) reported that, in overweight and obese subjects, decreased activation in striatal areas during food consumption compared with striatal enhanced activation to high-caloric foodrelated cues might be the reason for overeating and consequent weight gain (16).”
BackgroundExercise-related changes in between-network connectivity in overweight/obese adults
Legget, K. T., Wylie, K. P., Cornier, M., Melanson, E. L., Paschall, C. J., & Tregellas, J. R. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.02.031 · Cited by 22
Mind and brain in delay of gratification.
Zayas, V., Mischel, W., & Pandey, G. (2014) · American Psychological Association eBooks · doi:10.1037/14322-007 · Cited by 22
Hunt, K. F., Dunn, J., le Roux, C. W., Reed, L. J., Marsden, P. K., Patel, A. G., & Amiel, S. A. (2016) · Diabetes Care · doi:10.2337/dc15-2721 · Cited by 21
Derman, R. C., & Ferrario, C. R. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.03.012 · Cited by 21
“Furthermore, several brain imaging studies in healthy, overweight, and obese subjects have found that food cues elicit activations in corticolimbic regions, and that the magnitude of these effects is enhanced in overweight and obese populations (Rothemund et al., 2007; Stoeckel et al., 2008; Bruce et al., 2010; Yokum…”
BackgroundClarke, R. E., Verdejo‐García, A., & Andrews, Z. B. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14455 · Cited by 21
“In obesity, pictures of highly palatable foods increase BOLD activity in corticostriatal regions, which encompass the orbitofrontal cortex (OFC), anterior cingulate cortex (ACC), insula and striatum, compared to normal weight controls (Rothemund et al. 2007; Stoeckel et al. 2008; Yokum et al. 2011).”
BackgroundInhibition of food craving is a metabolically active process in the brain in obese men
Wang, G., Kojori, E. S., Yuan, K., Wiers, C. E., Manza, P., Wong, C., Fowler, J. S., & Volkow, N. D. (2019) · International Journal of Obesity · doi:10.1038/s41366-019-0484-z · Cited by 21
Nock, N. L., Dimitropoulos, A., Tkach, J. A., Frasure, H. E., & vonGruenigen, V. (2012) · BMC Neuroscience · doi:10.1186/1471-2202-13-74 · Cited by 23
“Obese women shown pictures of high-calorie foods were found to have increased activation in the dorsal striatum [38,39], a brain region implicated in reward anticipation and cue-induced drug craving and drug seeking [40].”
BackgroundIMAGING IN ENDOCRINOLOGY: The use of functional MRI to study the endocrinology of appetite
Salem, V., & Dhillo, W. S. (2015) · European Journal of Endocrinology · doi:10.1530/eje-14-0716 · Cited by 20
Large Portions Encourage the Selection of Palatable Rather Than Filling Foods
Brunstrom, J. M., Jarvstad, A., Griggs, R. L., Potter, C., Evans, N. R., Martin, A., Brooks, J. C. W., & Rogers, P. J. (2016) · Journal of Nutrition · doi:10.3945/jn.116.235184 · Cited by 20
Kahleová, 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
van Ruiten, C. C., Veltman, D. J., Wijdeveld, M., ten Kulve, J. S., Kramer, M. H. H., Nieuwdorp, M., & IJzerman, R. G. (2022) · Diabetes Obesity and Metabolism · doi:10.1111/dom.14732 · Cited by 20
Tan, Z., Hu, Y., Ji, G., Li, G., Ding, Y., Zhang, W., Wang, J., Jia, Z., Zhang, L., Li, H., et al. (2022) · Brain Topography · doi:10.1007/s10548-022-00906-z · Cited by 20
Domínguez, P. R. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.12.010 · Cited by 22
Unrecognized Sleep Loss Accumulated in Daily Life Can Promote Brain Hyperreactivity to Food Cue
Katsunuma, R., Oba, K., Kitamura, S., Motomura, Y., Terasawa, Y., Nakazaki, K., Hida, A., Moriguchi, Y., & Mishima, K. (2017) · SLEEP · doi:10.1093/sleep/zsx137 · Cited by 20
Enhanced food-related responses in the ventral medial prefrontal cortex in narcolepsy type 1
van Holst, R. J., Janssen, L. K., van Mierlo, P., Lammers, G. J., Cools, R., Overeem, S., & Aarts, E. (2018) · Scientific Reports · doi:10.1038/s41598-018-34647-6 · Cited by 20
Food-Related Odors and the Reward Circuit: Functional MRI
Frasnelli, J., Hummel, C., Bojanowski, V., Warr, J., Gerber, J. C., & Hummel, T. R. (2015) · Chemosensory Perception · doi:10.1007/s12078-015-9193-8 · Cited by 24
“Obese women exhibited activation of striatum (caudate and putamen), but individuals with normal weight did not (Rothemund et al. 2007).”
BackgroundNakamura, Y., & Koike, S. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.647143 · Cited by 19
“For these analyses, we set the amygdala (468 voxels) and insula cortex (3628 voxels) as ROIs based on previous studies (Rothemund et al., 2007; Schienle et al., 2009; Kerr et al., 2015; Sun et al., 2015; van Rijn et al., 2018; Chikazoe et al., 2019; Nakamura et al., 2020) showing that the insula and amygdala were rela…”
MethodVugt, D. A. V., Krzemien, A. A., Alsaadi, H., Palerme, S., & Reid, R. L. (2013) · Obesity · doi:10.1002/oby.20148 · Cited by 19
“Adiposity and hunger have been shown to increase brain responsiveness to appetitive stimuli (22,32-37).”
BackgroundDeep brain stimulation for obesity: past, present, and future targets
Dupré, D. A., Tomycz, N. D., Oh, M. Y., & Whiting, D. M. (2015) · Neurosurgical FOCUS · doi:10.3171/2015.3.focus1542 · Cited by 22
Metabolic imaging in obesity: underlying mechanisms and consequences in the whole body
Iozzo, P. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12880 · Cited by 20
Food Addiction Spectrum: A Theoretical Model from Normality to Eating and Overeating Disorders
Piccinni, A., Marazziti, D., Vanelli, F., Franceschini, C., Baroni, S., Costanzo, D., Cremone, I. M., Veltri, A., & Dell’Osso, L. (2015) · Current Medicinal Chemistry · doi:10.2174/0929867322666150227153015 · Cited by 22
Brain regulation of appetite in twins
Melhorn, S. J., Mehta, S. H., Kratz, M., Tyagi, V., Webb, M. F., Noonan, C., Buchwald, D., Goldberg, J. H., Maravilla, K. R., Grabowski, T. J., et al. (2016) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.121095 · Cited by 19
Modeling interactions between brain function, diet adherence behaviors, and weight loss success
Szabo‐Reed, A. N., Martin, L. E., Hu, J., Yeh, H., Powell, J. N., Lepping, R. J., Patrician, T. M., Breslin, F. J., Donnelly, J. E., & Savage, C. R. (2020) · Obesity Science & Practice · doi:10.1002/osp4.403 · Cited by 18
Ventral frontal satiation-mediated responses to food aromas in obese and normal-weight women
Eiler, W. J. A., Džemidžić, M., Case, K. R., Armstrong, C. L. H., Mattes, R. D., Cyders, M. A., Considine, R. V., & Kareken, D. A. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.080788 · Cited by 19
“This absence of a differential response is in conflict with reports of appetizing food images that did activate the lateral OFC in fasted, obese adults and children (21, 68, 69) [however, a number of studies did not report within-group findings for obese subjects alone (70, 72)].”
BackgroundResultChinese Food Image Database for Eating and Appetite Studies
Li, X., Pan, Y., Han, Y., Liang, Q., Yang, X., Meng, X., & Gao, X. Z. (2022) · Nutrients · doi:10.3390/nu14142916 · Cited by 18
“Changes in the calories in a food image can change food motivation, as highcalorie food images induce activation in the medial and lateral prefrontal cortex, and low-calorie food images induce activation in the orbitofrontal cortex [16,17].”
BackgroundTriglyceride sensing in the reward circuitry: A new insight in feeding behaviour regulation
Cansell, C., & Luquet, S. H. (2015) · Biochimie · doi:10.1016/j.biochi.2015.07.004 · Cited by 21
Propensity to Obesity Impacts the Neuronal Response to Energy Imbalance
Cornier, M., Legget, K. T., Thomas, E. A., Bechtell, J. L., Bessesen, D. H., & Tregellas, J. R. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00052 · Cited by 18
“It is unclear, though, if these findings are a consequence or cause of obesity (Rothemund et al., 2007; Stoeckel et al., 2008; Martin et al., 2010).”
Using High Spatial Resolution to Improve BOLD fMRI Detection at 3T
Iranpour, J., Morrot, G., Claise, B., Jean, B., & Bonny, J.-M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141358 · Cited by 18
Franssen, S., Jansen, A. T. M., van den Hurk, J., Roebroeck, A. F., & Roefs, A. (2020) · Appetite · doi:10.1016/j.appet.2020.104609 · Cited by 21
Metadata
- Authors
- Rothemund, Y., Preuschhof, C., Bohner, G., Bauknecht, H.-C., Klingebiel, R., Flor, H., & Klapp, B. F.
- Affiliations
- Stiftung Charité (DE)
- Max Planck Society (DE)
- Heidelberg University (DE)
- Corresponding author
- Rothemund, Yvonne
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2007-08
- Volume
- 37
- Issue
- 2
- Pages
- 410-421
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W1976544983
- Cited by
- 679
- References
- 67
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 13 · 2023: 25 · 2022: 34 · 2021: 38 · 2020: 35 · 2019: 43 · 2018: 35 · 2017: 44 · 2016: 45 · 2015: 56 · 2014: 69 · 2013: 50 · 2012: 73
- FWCI
- 8.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (FL 156/29)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- obesity, dorsal striatum, food motivation, energy density, reward anticipation, habit learning, anterior insula, orbitofrontal cortex, posterior cingulate cortex, body mass index, dopamine, overeating
- MeSH terms
- Adult, Brain Mapping, Corpus Striatum, Female, Food, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Obesity, Photic Stimulation
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