Cited by 679Regulation of Appetite and ObesityEating Disorders and BehaviorsNeurotransmitter Receptor Influence on Behavior

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Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals

Rothemund, Yvonne, Preuschhof, Claudia, Bohner, Georg, Bauknecht, Hans-Christian, Klingebiel, Randolf, Flor, Herta, Klapp, Burghard F.·2007·NeuroImage

DOI 10.1016/j.neuroimage.2007.05.008

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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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Background
Brain Responses to High-Calorie Visual Food Cues in Individuals with Normal-Weight or Obesity: An Activation Likelihood Estimation Meta-Analysis
Yang, Y., Wu, Q., & Morys, F. (2021) · Brain Sciences · doi:10.3390/brainsci11121587 · Cited by 45
“14 Overweight At least 2 High-calorie food commercials Non-food commercials Passive viewing 5 p 0.05, FWE corrected Rothemund et al., 2007 [83] 13 (100”
Influential
How Does the Brain Implement Adaptive Decision Making to Eat?
Compan, V., Walsh, B. T., Kaye, W. H., & Geliebter, A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2602-15.2015 · Cited by 45
“Greater putamen activation in obese versus lean women in response to high-ED compared with low-ED visual stimuli were also noted in another fMRI study (Rothemund et al., 2007).”
Result
Abdominal fat is associated with a greater brain reward response to high‐calorie food cues in hispanic women
LUO, S. H., Romero, A., Adam, T. C., Hu, P., Monterosso, J. R., & Page, K. A. (2013) · Obesity · doi:10.1002/oby.20344 · Cited by 42
“in brain regions involved in reward and motivation [3-8], and obese”
Background
Obesity and Brain Addiction Circuitry
Taghva, A. S., Corrigan, J. D., & Rezai, A. R. (2012) · Neurosurgery · doi:10.1227/neu.0b013e31825972ab · Cited by 44
Increased Brain Reward Responsivity to Food‐Related Odors in Obesity
Han, P., Roitzsch, C., Horstmann, A., Poessel, M., & Hummel, T. R. (2021) · Obesity · doi:10.1002/oby.23170 · Cited by 46
“These regions have been well documented as key areas involved in food reward processing of food odors and flavors (26) and have been shown with increased activation among people with obesity during highcalorie versus lowcalorie visual food cue processing (27,28).”
Background
Role of orexin/hypocretin in conditioned sucrose-seeking in female rats
Cason, A. M., & Aston‐Jones, G. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.07.007 · Cited by 43
“Recent clinical studies have linked increased visual attention bias to food related cues and increased neuronal activation of reward centers in anticipation of food reward to obesity (Castellanos et al., 2009; Nijs et al., 2010; Rothemund et al., 2007; Stice et al., 2008).”
Altered monetary loss processing and reinforcement-based learning in individuals with obesity
Kube, J., Mathar, D., Horstmann, A., Kotz, S. A., Villringer, A., & Neumann, J. (2017) · Brain Imaging and Behavior · doi:10.1007/s11682-017-9786-8 · Cited by 42
A systematic and meta-analytic review on the neural correlates of viewing high- and low-calorie foods among normal-weight adults
Zheng, L., Miao, M., & Gan, Y. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104721 · Cited by 41
Diabetes mellitus and Parkinson’s disease: dangerous liaisons between insulin and dopamine
de Iuliis, A., Montinaro, E., Fatati, G., Plebani, M., & Colosimo, C. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.320965 · Cited by 37
Sexually dimorphic functional connectivity in response to high vs. low energy-dense food cues in obese humans: An fMRI study
Atalayer, D., Pantazatos, S. P., Gibson, C. D., McOuatt, H., Puma, L. M., Astbury, N. M., & Geliebter, A. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.05.054 · Cited by 42
“Moreover, it has been shown that fMRI signals in response to high-calorie food items are BMI-dependent (Rothemund et al., 2007) and baseline fMRI signals before a diet correlate with the subsequent weight loss (Weygandt et al., 2013).”
Background
Early adversity promotes binge-like eating habits by remodeling a leptin-responsive lateral hypothalamus–brainstem pathway
Shin, S., You, I., Jeong, M., Bae, Y., Wang, X., Cawley, M. L., Han, A., & Lim, B. K. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01208-0 · Cited by 42
Association between the seven-repeat allele of the dopamine-4 receptor gene (DRD4) and spontaneous food intake in pre-school children
Silveira, P. P., Portella, A. K., Kennedy, J. L., Gaudreau, H., Davis, C. A., Steiner, M. S., Soares, C. N., Matthews, S. G., Sokolowski, M. B., Dubé, L., et al. (2013) · Appetite · doi:10.1016/j.appet.2013.10.004 · Cited by 40
“Food-related cues activate brain areas that are either involved in the synthesis and release of dopamine or are targets for dopamine projections (Killgore et al., 2003, Rothemund et al., 2007).”
Background
Pregnancy eating attributes study (PEAS): a cohort study examining behavioral and environmental influences on diet and weight change in pregnancy and postpartum
Nansel, T. R., Lipsky, L. M., Siega‐Riz, A. M., Burger, K. S., Faith, M. S., & Liu, A. (2016) · BMC Nutrition · doi:10.1186/s40795-016-0083-5 · Cited by 40
“versus normal weight subjects [62], and predicts subsequent weight gain over 6–12 months [61].”
Background
Taste at first (person) sight: Visual perspective modulates brain activity implicitly associated with viewing unhealthy but not healthy foods
Bassó, F., Petit, O., Bellu, S. L., Lahlou, S., Cancel, A., & Anton, J. (2018) · Appetite · doi:10.1016/j.appet.2018.06.009 · Cited by 43
Improvement in Uncontrolled Eating Behavior after Laparoscopic Sleeve Gastrectomy Is Associated with Alterations in the Brain–Gut–Microbiome Axis in Obese Women
Dong, T. S., Gupta, A., Jacobs, J. P., Lagishetty, V., Gallagher, E., Bhatt, R. R., Vora, P. P., Osadchiy, V., Stains, J., Balioukova, A., et al. (2020) · Nutrients · doi:10.3390/nu12102924 · Cited by 41
“In imaging studies, the putamen and the amygdala display higher reactivity to high-calorie food cues among obese subjects than among lean subjects [59,60].”
Background
Resting activity of the hippocampus and amygdala in obese individuals predicts their response to food cues
Li, G., Hu, Y., Zhang, W., Ding, Y., Wang, Y., Wang, J., He, Y., Lv, G., von Deneen, K. M., Zhao, Y., et al. (2020) · Addiction Biology · doi:10.1111/adb.12974 · Cited by 40
GLP-1 and hunger modulate incentive motivation depending on insulin sensitivity in humans
Hanßen, R., Kretschmer, A. C., Rigoux, L., Albus, K., Thanarajah, S. E., Sitnikow, T., Melzer, C., Cornely, O. A., Brüning, J. C., & Tittgemeyer, M. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101163 · Cited by 42
Functional Neuroimaging in Craniopharyngioma: A Useful Tool to Better Understand Hypothalamic Obesity?
Roth, C. L., Aylward, E., Liang, O., Kleinhans, N. M., Pauley, G., & Schur, E. A. (2012) · Obesity Facts · doi:10.1159/000338695 · Cited by 40
Polycystic Ovary Syndrome and Brain: An Update on Structural and Functional Studies
Saydam, B. Ö., & Yıldız, B. O. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa843 · Cited by 39
Intrinsic brain subsystem associated with dietary restraint, disinhibition and hunger: an fMRI study
Zhao, J., Li, M., Zhang, Y., Song, H., von Deneen, K. M., Shi, Y., Liu, Y., & He, D. (2016) · Brain Imaging and Behavior · doi:10.1007/s11682-015-9491-4 · Cited by 37
Assessing the psychometric properties of two food addiction scales
Lemeshow, A. R., Gearhardt, A. N., Genkinger, J. M., & Corbin, W. R. (2016) · Eating Behaviors · doi:10.1016/j.eatbeh.2016.08.005 · Cited by 39
Bariatric Surgery and Brain Health—A Longitudinal Observational Study Investigating the Effect of Surgery on Cognitive Function and Gray Matter Volume
Prehn, K., Profitlich, T., Rangus, I., Heßler, S., Witte, A. V., Grittner, U., Ordemann, J., & Flöel, A. (2020) · Nutrients · doi:10.3390/nu12010127 · Cited by 39
“Eating fewer calories overall, and smaller portions, reduces the chronically enhanced neural activity in these brain regions [63,64], which will translate into a decrease of volume over time.”
Background
Differences in brain responses between lean and obese women to a sweetened drink
Connolly, L., Coveleskie, K., Kilpatrick, L. A., Labus, J. S., Ebrat, B., Stains, J., Jiang, Z., Tillisch, K., Raybould, H. E., & Mayer, E. A. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12125 · Cited by 38
Gaining New Insights into Food Reward with Functional Neuroimaging
Neary, M. T., & Batterham, R. L. (2009) · Forum of nutrition/Bibliotheca Nutritio et dieta · doi:10.1159/000264403 · Cited by 38
Eating-related behaviors and appetite during energy imbalance in obese-prone and obese-resistant individuals
Thomas, E. A., Bechtell, J. L., Vestal, B. E., Johnson, S. L., Bessesen, D. H., Tregellas, J. R., & Cornier, M. (2013) · Appetite · doi:10.1016/j.appet.2013.01.015 · Cited by 41
Rationale and consequences of reclassifying obesity as an addictive disorder: Neurobiology, food environment and social policy perspectives
Allen, P. J., Batra, P. J., Geiger, B. M., Wommack, T., Gilhooly, C. H., & Pothos, E. N. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.05.005 · Cited by 39
Habituation to the pleasure elicited by sweetness in lean and obese women
Pepino, M. Y., & Mennella, J. A. (2012) · Appetite · doi:10.1016/j.appet.2012.01.026 · Cited by 39
“…to lean individuals, obese individuals showed increased activation of brain areas associated with food reward when tasting or viewing a picture of a palatable, high-calorie meal (DelParigi et al., 2004; Rothemund et al., 2007; Stice, Spoor, Bohon, Veldhuizen, & Small, 2008; Stoeckel et al., 2008).”
Distinct and overlapping fusiform activation to faces and food
Adamson, K. M., & Troiani, V. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.02.064 · Cited by 36
White matter integrity disparities between normal-weight and overweight/obese adolescents: an automated fiber quantification tractography study
Carbine, K. A., Duraccio, K. M., Hedges‐Muncy, A., Barnett, K. A., Kirwan, C. B., & Jensen, C. D. (2019) · Brain Imaging and Behavior · doi:10.1007/s11682-019-00036-4 · Cited by 39
Implications from addiction research towards the understanding and treatment of obesity
Grosshans, M., Loeber, S., & Kiefer, F. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2010.00300.x · Cited by 38
“However, only recently, Rothermund et al. (2007) were able to demonstrate that not only food but also visual stimuli of high caloric food induce striatal activation in obese patients.”
Background
The Craving Stops Before You Feel It: Neural Correlates of Chocolate Craving During Cue Exposure with Response Prevention
Frankort, A., Roefs, A., Siep, N., Roebroeck, A. F., Havermans, R. C., & Jansen, A. T. M. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht016 · Cited by 37
“Further, there was a region in the left striate cortex (Rothemund et al. 2007; Führer et al. 2008; Malik et al. 2008; Tang et al. 2012), as well as 2 regions in the extrastriate cortex (Rothemund et al.”
BackgroundInfluential
Listen, Learn, Like! Dorsolateral Prefrontal Cortex Involved in the Mere Exposure Effect in Music
Green, A. C., Bærentsen, K. B., Stødkilde‐Jørgensen, H., Roepstorff, A., & Vuust, P. (2012) · Neurology Research International · doi:10.1155/2012/846270 · Cited by 41
“The dorsal striatum has also been implicated in reward processing of various types of stimuli, especially food and drink, for example [25, 32, 33].”
Background
Dynamic fMRI networks predict success in a behavioral weight loss program among older adults
Mokhtari, F., Rejeski, W. J., Zhu, Y., Guorong Wu, A., Simpson, S. L., Burdette, J. H., & Laurienti, P. J. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.02.025 · Cited by 36
Brain response to food brands correlates with increased intake from branded meals in children: an fMRI study
Masterson, T. D., Stein, W. M., Beidler, E., Bermúdez, M. A., English, L., & Keller, K. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9919-8 · Cited by 36
Appetite, Satiety, and Food Reward in Obese Individuals: A Behavioral Phenotype Approach
Dalton, M., Finlayson, G., Esdaile, E. K., & King, N. A. (2013) · Current Nutrition Reports · doi:10.1007/s13668-013-0060-4 · Cited by 42
Neural correlates of pediatric obesity
Bruce, A. S., Martin, L. E., & Savage, C. R. (2011) · Preventive Medicine · doi:10.1016/j.ypmed.2011.01.018 · Cited by 37
Impaired Cross-Talk between Mesolimbic Food Reward Processing and Metabolic Signaling Predicts Body Mass Index
Simon, J. J., Skunde, M., Sinno, M. H., Brockmeyer, T., Herpertz, S. C., Bendszus, M., Herzog, W., & Friederich, H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00359 · Cited by 35
“…value (Balleine et al., 2007), increased activity in the DS, and a concurrent decrease in brain regions subserving inhibitory control (mainly the dorsolateral prefrontal cortex) have been found in obese individuals during anticipatory food reward (Rothemund et al., 2007; Nummenmaa et al., 2012).”
Background
Neural processing of food cues in pre‐pubertal children
LUO, S. H., Alves, J. M., Hardy, K., Wang, X., Monterosso, J. R., Xiang, A. H., & Page, K. A. (2018) · Pediatric Obesity · doi:10.1111/ijpo.12435 · Cited by 35
Bariatric Surgery and the Central Nervous System
Rao, R. S. (2012) · Obesity Surgery · doi:10.1007/s11695-012-0649-5 · Cited by 35
“Another study found greater activation of dorsal striatum and certain other brain areas in response to pictures of high calorie foods in overweight women using functional MRI when compared to normal weight women [9].”
Background
Correlation Between Ventromedial Prefrontal Cortex Activation to Food Aromas and Cue-Driven Eating: An fMRI Study
Eiler, W. J. A., Džemidžić, M., Case, K. R., Considine, R. V., & Kareken, D. A. (2012) · Chemosensory Perception · doi:10.1007/s12078-011-9112-6 · Cited by 36
“Rothemund and colleagues (Rothemund et al., 2007) observed increased neuronal activation within the dorsal striatum, anterior and posterior cingulate cortices and lateral OFC following the presentation of high-calorie food images, suggesting an increased role for brain areas associated with reward…”
Independent functional connectivity networks underpin food and monetary reward sensitivity in excess weight
Verdejo‐Román, J., Fornito, A., Soriano‐Mas, C., Vilar‐López, R., & Verdejo‐García, A. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.11.011 · Cited by 36

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
ORCID: Preuschhof, Claudia
Bauknecht, Hans-Christian
Klingebiel, Randolf
Flor, Herta
Venue: NeuroImage
Publisher: Elsevier BV
Published: 2007-08
Volume: 37
Issue: 2
Pages: 410-421
ISSN: 1053-8119 (ISSN-L)
DOI: 10.1016/j.neuroimage.2007.05.008
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
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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Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals

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