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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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InfluentialDietary Restraint Violations Influence Reward Responses in Nucleus Accumbens and Amygdala
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“…and the NAcc were further related to many other rewards, such as erotic films (Karama et al. 2002), pictures of highcalorie-food in obese people (Rothemund et al. 2007), pictures of one’s own children (Leibenluft et al. 2004), or photos of alcoholic drinks presented to alcoholics (Braus et al.…”
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“Importantly, obese and lean subjects differ in brain activity during consumption and anticipation of palatable food [104,177,202,203].”
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“Obese women show a heightened brain response to food cues in the dorsal and ventral striatum (62, 63), and patients with eating disorders have altered gray-matter density in the hypothalamus (64) and altered brain responses in the hypothalamus (65) and dorsal striatum (66).”
BackgroundHeni, M., Kullmann, S., Ketterer, C., Guthoff, M., Bayer, M., Staiger, H., Machicao, F. E., Häring, H., Preissl, H. T., Veit, R., et al. (2013) · Human Brain Mapping · doi:10.1002/hbm.22223 · Cited by 77
“…brain regions related to hedonic aspects of food cues, especially the striatum, showed significantly reduced dopamine D2 receptor availability [Wang et al., 2001] and exhibited greater activation to high caloric food stimuli in obese individuals [Rothemund et al., 2007; Stoeckel et al., 2008].”
BackgroundFaulconbridge, L. F., Ruparel, K., Loughead, J., Allison, K. C., Hesson, L. A., Fabricatore, A. N., Rochette, A., Ritter, S., Hopson, R. D., Sarwer, D. B., et al. (2016) · Obesity · doi:10.1002/oby.21464 · Cited by 78
“Several research groups (7-10) have shown differences in response to food cues in this pathway in”
BackgroundHe, Q., Xiao, L., Xue, G., Wong, S. W. H., Ames, S. L., Schembre, S. M., & Bechara, A. (2014) · Nutrition Journal · doi:10.1186/1475-2891-13-92 · Cited by 76
“These results are consistent with the idea that these systems, which were previously shown to have altered activity in cases of other substance addictions, also show some altered responses to visual food cues in obese individuals [46,61-65].”
ResultCornier, M., Legget, K. T., Thomas, E. A., Bechtell, J. L., Eichman, L. C., Bessesen, D. H., & Tregellas, J. R. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.01.002 · Cited by 76
“Regions of increased response include areas such as the hypothalamus, amygdala, hippocampus, orbitofrontal and prefrontal cortex, and insula [7,10,11].”
Nielsen, M. Ø., Rostrup, E., Wulff, S., Glenthoj, B. Y., & Ebdrup, B. H. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.2582 · Cited by 76
Navas (2017) · doi:10.1002/hbm.23407 · Cited by 71
“The increased responsivity of the ventral and dorsal striatum to high-palatable food in obese individuals is consistent with previous fMRI studies showing increased striatal activation in response to food cues [Rothemund et al., 2007; Simon et al., 2014].”
BackgroundResultInfluentialFood cue reactivity: Neurobiological and behavioral underpinnings
Kanoski, S. E., & Boutelle, K. N. (2022) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-022-09724-x · Cited by 78
“This appetitive network includes the hippocampus [111], the amygdala [112, 113], the insula [113], the striatum, [114, 115] anterior cingulate cortex (Acc) [116], the orbitofrontal cortex (OFC) and prefrontal cortex (PFC) (see Fig.”
Fletcher, P. C., Napolitano, A., Skeggs, A. L., Miller, S. R., Delafont, B., Cambridge, V. C., de Wit, S., Nathan, P. J., Brooke, A. C., O’Rahilly, S., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3323-10.2010 · Cited by 75
“We should acknowledge that the imaging parameters used did not optimize acquisition of data from orbitofrontal cortex, which previous work has implicated in such tasks (Killgore and Yurgelun-Todd, 2005; Porubská et al., 2006; Rothemund et al., 2007; Führer et al., 2008; Schienle et al., 2009).”
InfluentialThe effects of high-intensity exercise on neural responses to images of food
Crabtree, D. R., Chambers, E. S., Hardwick, R. M., & Blannin, A. K. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.071381 · Cited by 75
“A further limitation of the current research is that only lean physically active men were studied, because previous studies have suggested that the response of central reward regions to images of HC is greater in obese individuals than in lean controls (16, 50).”
BackgroundDopamine D 2/3 receptor availability and amphetamine-induced dopamine release in obesity
van de Giessen, E., Celik, F., Schweitzer, D. H., van den Brink, W., & Booij, J. (2014) · Journal of Psychopharmacology · doi:10.1177/0269881114531664 · Cited by 78
Miccoli, L., Delgado, R., Rodríguez‐Ruiz, S., Guerra, P. M., García-Mármol, E., & Fernández‐Santaella, M. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0114515 · Cited by 74
Stice, E. M., Yokum, S., & Burger, K. S. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.11.019 · Cited by 75
Sex-based fMRI differences in obese humans in response to high vs. low energy food cues
Geliebter, A., Pantazatos, S. P., McOuatt, H., Puma, L., Gibson, C. D., & Atalayer, D. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.12.023 · Cited by 72
Paquet, C., Daniel, M., Knaüper, B., Gauvin, L. I., Kestens, Y., & Dubé, L. (2010) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28648 · Cited by 72
Beyer, F., Masouleh, S. K., Huntenburg, J. M., Lampe, L., Luck, T., Riedel-Heller, S. G., Loeffler, M., Schroeter, M. L., Stümvoll, M., Villringer, A., et al. (2017) · Human Brain Mapping · doi:10.1002/hbm.23605 · Cited by 75
“Using task-based functional MRI (fMRI), several studies revealed differences between lean and obese participants in regional activation patterns during the processing of rewarding food and non-food stimuli [Rothemund et al., 2007; Stice et al., 2008; Stoeckel et al., 2008].”
BackgroundObesity, body weight regulation and the brain: insights from fMRI
Makaronidis, J., & Batterham, R. L. (2018) · British Journal of Radiology · doi:10.1259/bjr.20170910 · Cited by 77
Is obesity related to enhanced neural reactivity to visual food cues? A review and meta-analysis
Morys, F., García‐García, I., & Dagher, A. (2020) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsaa113 · Cited by 71
Figley, C. R., Asem, J. S. A., Levenbaum, E., & Courtney, S. M. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00234 · Cited by 70
“…as well as gustatory, limbic, and reward regions—and that these responses were disproportionately large in overweight vs. normal weight participants (Simmons et al., 2005; Porubská et al., 2006; Rothemund et al., 2007; Stoeckel et al., 2008) and reduced in anorexic patients (McFadden et al., 2014).”
BackgroundMesolimbic dopamine and its neuromodulators in obesity and binge eating
Naef, L., Pitman, K. A., & Borgland, S. L. (2015) · CNS Spectrums · doi:10.1017/s1092852915000693 · Cited by 70
Changes in brain activation to food pictures after adjustable gastric banding
Bruce, J. M., Hancock, L. M., Bruce, A. S., Lepping, R. J., Martin, L. E., Lundgren, J. D., Malley, S., Holsen, L. M., & Savage, C. R. (2011) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2011.07.006 · Cited by 70
Brain imaging studies of appetite in the context of obesity and the menstrual cycle
Vugt, D. A. V. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp051 · Cited by 72
“Greater activation was attributed to subjects being hungry at the time of the scan, whereas hungry subjects were explicitly excluded in the other study (Rothemund et al., 2007).”
BackgroundAssessing food appeal and desire to eat: the effects of portion size & energy density
Burger, K. S., Cornier, M. A., Ingebrigtsen, J. P., & Johnson, S. L. (2011) · International Journal of Behavioral Nutrition and Physical Activity · doi:10.1186/1479-5868-8-101 · Cited by 68
“These studies have reported that brain activation in reward and attention related areas is increased when individuals are shown pictures of energy dense, highly palatable foods [8] and that activation resulting from high calorie foods is positively associated with body mass index [8-10].”
Backgroundvan Bloemendaal, L., Veltman, D. J., ten Kulve, J. S., Drent, M. L., Barkhof, F., Diamant, M., & IJzerman, R. G. (2015) · Obesity · doi:10.1002/oby.21200 · Cited by 69
“We previously described that exenatide versus placebo reduces responses to food pictures in subjects with obesity and T2DM patients (in insula, amygdala, putamen and OFC), but not in lean subjects (13).”
InfluentialStimulus devaluation induced by stopping action.
Wessel, J. R., O’Doherty, J. P., Berkebile-Weinberg, M., Linderman, D., & Aron, A. R. (2014) · Journal of Experimental Psychology General · doi:10.1037/xge0000022 · Cited by 71
“, a cigarette or unhealthy food) is a core symptom of psychiatric disorders such as substance dependence (Goldstein & Volkow, 2002, 2011), unhealthy eating (Rothemund et al., 2007), and pathological gambling (Clark et al.”
BackgroundMichaelides, M., Thanos, P. K., Volkow, N. D., & Wang, G. (2012) · International Review of Psychiatry · doi:10.3109/09540261.2012.679918 · Cited by 65
“Obese subjects also show enhanced striatal and OFC BOLD signal responses to images of food, and these responses are associated with susceptibility to weight gain (Rothemund et al., 2007; Stoeckel et al., 2008; Stice et al., 2010a).”
BackgroundNeural correlates of individual differences related to appetite
Lowe, M. R., van Steenburgh, J., Ochner, C. N., & Coletta, M. C. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.04.001 · Cited by 70
“There is substantial literature indicating that obese individuals find palatable foods more rewarding [118,134–137], but it is unclear why this is so.”
BackgroundSimon, J. J., Skunde, M., Wu, M., Schnell, K., Herpertz, S. C., Bendszus, M., Herzog, W., & Friederich, H. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu162 · Cited by 66
Endogenous GLP1 and GLP1 analogue alter CNS responses to palatable food consumption
ten Kulve, J. S., Veltman, D. J., van Bloemendaal, L., Groot, P. F. C., Ruhé, H. G., Barkhof, F., Diamant, M., & IJzerman, R. G. (2016) · Journal of Endocrinology · doi:10.1530/joe-15-0461 · Cited by 65
“A priori regions of interest were determined based on the previous studies (i.e. insula, striatum, amygdala and OFC) (Rothemund et al. 2007, Stoeckel et al. 2008, Tang et al. 2012, van Bloemendaal et al.”
BackgroundMethodInfluentialMartens, M. J. I., Born, J. R., Lemmens, S. G. T., Karhunen, L. J., Heinecke, A., Goebel, R., Adam, T. C., & Westerterp‐Plantenga, M. S. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.044024 · Cited by 65
Association of Body Mass and Brain Activation during Gastric Distention: Implications for Obesity
Tomasi, D., Wang, G.-J., Wang, R., Backus, W., Geliebter, A., Telang, F., Jayne, M. C., Wong, C., Fowler, J. S., & Volkow, N. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006847 · Cited by 64
Orosensory and Homeostatic Functions of the Insular Taste Cortex
de Araújo, I. D., Geha, P., & Small, D. (2012) · Chemosensory Perception · doi:10.1007/s12078-012-9117-9 · Cited by 59
“Regarding the sensory representation of food, obese relative to lean individuals also show greater insular responses to pictures of high-calorie foods (Rothemund et al. 2007) and to the anticipated as well as actual ingestion of milkshake (Stice et al. 2008).”
BackgroundBody–Brain Connections: The Effects of Obesity and Behavioral Interventions on Neurocognitive Aging
Stillman, C. M., Weinstein, A. M., Marsland, A. L., Gianaros, P. J., & Erickson, K. I. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00115 · Cited by 69
“Notably, functional activation differences between obese and healthy-weight groups are typically largest in response to high calorie food items, and have also been shown to scale with individual differences in BMI (Rothemund et al., 2007; Grosshans et al., 2012; Martens et al., 2013).”
BackgroundDo ADHD-impulsivity and BMI have shared polygenic and neural correlates?
Barker, E. D., Ing, A., Biondo, F., Jia, T., Pingault, J., Rietz, E. D., Zhang, Y., Ruggeri, B., Banaschewski, T., Hohmann, S., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0444-y · Cited by 67
“reward areas in the medial frontal regions [54, 55].”
BackgroundCansell, C., Castel, J., Denis, R., Rouch, C., Delbes, A.-S., Martinez, S., Mestivier, D., Finan, B., Maldonado‐Avilés, J. G., Rijnsburger, M., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.31 · Cited by 69
Circulating Triglycerides Gate Dopamine-Associated Behaviors through DRD2-Expressing Neurons
Berland, C., Montalban, E., Perrin, E., Miceli, M. D., Nakamura, Y., Martinat, M., Sullivan, M., Davis, X. S., Shenasa, M. A., Martin, C., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.02.010 · Cited by 70
“Excessive consumption of energy-dense food increases the vulnerability to develop uncontrolled craving, compulsive feeding and ultimately excessive body weight gain (Kenny et al., 2013; Rothemund et al., 2007; Stice et al., 2008a; Volkow et al., 2013).”
BackgroundAttentional bias to food-related visual cues: is there a role in obesity?
Doolan, K. J., Breslin, G., Hanna, D., & Gallagher, A. M. (2014) · Proceedings of The Nutrition Society · doi:10.1017/s002966511400144x · Cited by 63
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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