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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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Egecioglu, E., Skibicka, K. P., Hansson, C., Álvarez-Crespo, M., Friberg, P. A., Jerlhag, E., Engel, J. A., & Dickson, S. L. (2011) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-011-9166-4 · Cited by 192
“Obese individuals have a greater striatal response to visual food cues relative to lean individuals (64-66).”
BackgroundNijs, I. M. T., Franken, I. H. A., & Muris, P. (2010) · Eating Behaviors · doi:10.1016/j.eatbeh.2010.07.002 · Cited by 186
“Neuroimaging studies have yielded more knowledge about the brain substrates that seem to play a role in food-related cue-responsivity (e.g., Rothemund et al., 2007; Stoeckel, Kim, Weller, & Cox, 2009; Stoeckel et al., 2008).”
BackgroundSchur, E. A., Kleinhans, N. M., Goldberg, J. H., Buchwald, D., Schwartz, M. W., & Maravilla, K. R. (2009) · International Journal of Obesity · doi:10.1038/ijo.2009.56 · Cited by 173
Standardized food images: A photographing protocol and image database
Charbonnier, L., van Meer, F., van der Laan, L. N., Viergever, M. A., & Smeets, P. A. M. (2015) · Appetite · doi:10.1016/j.appet.2015.08.041 · Cited by 168
“…often poor in lighting; other 63 studies used images from commercial stock photograph websites (Killgore et al., 2003; 64 Killgore and Yurgelun‐Todd, 2005; Rothemund et al., 2007; Siep et al., 2009), which are of 65 high photographic quality but highly diverse in portion size and presentation.”
Individual variation in resisting temptation: Implications for addiction
Saunders, B. T., & Robinson, T. E. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.008 · Cited by 177
Functional brain imaging of appetite
Dagher, A. (2012) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.02.009 · Cited by 171
McCaffery, J. M., Haley, A. P., Sweet, L. H., Phelan, S., Raynor, H. A., Del Parigi, A., Cohen, R., & Wing, R. R. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27924 · Cited by 161
Neural Responses to Visual Food Cues: Insights from Functional Magnetic Resonance Imaging
García‐García, I., Narberhaus, A., Marqués‐Iturria, I., Garolera, M., Rădoi, A., Segura, B., Pueyo, R., Ariza, M., & Jurado, M. Á. (2013) · European Eating Disorders Review · doi:10.1002/erv.2216 · Cited by 166
Obesity: Is it a mental disorder?
Marcus, M. D., & Wildes, J. E. (2009) · International Journal of Eating Disorders · doi:10.1002/eat.20725 · Cited by 166
“Similarly, Rothemund et al.(116) reported that obese women had greater activation in the dorsal striatum, anterior insula, hippocampus, and parietal lobule than did lean women in response to viewing pictures of highcalorie foods.”
BackgroundStice, E., Burger, K., & Yokum, S. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.11.028 · Cited by 162
Oussaada, S. M., van Galen, K. A., Cooiman, M. I., Kleinendorst, L., Hazebroek, E. J., van Haelst, M. M., ter Horst, K. W., & Serlie, M. J. (2019) · Metabolism · doi:10.1016/j.metabol.2018.12.012 · Cited by 180
Milton, A. L., Lee, J. L. C., & Everitt, B. J. (2008) · Learning & Memory · doi:10.1101/lm.825008 · Cited by 163
“…to depend upon common underlying neurobiological and psychological mechanisms (Wang et al. 2004; Kelley et al. 2005; Volkow and Wise 2005; Rothemund et al. 2007), this may suggest that a reconsolidation-based treatment using propranolol could also be useful in reducing cueinduced craving…”
BackgroundBohon, C., & Stice, E. (2011) · International Journal of Eating Disorders · doi:10.1002/eat.20869 · Cited by 153
“Interestingly, fMRI studies indicate that obese versus lean individuals show greater activation in reward areas, including the insula, frontal operculum, orbitofrontal cortex, amygdala, and striatum in response to pictures of palatable foods (38-40) and anticipated receipt of palatable food (20).”
BackgroundSaad, G., & Stenstrom, E. P. (2012) · Journal of Consumer Psychology · doi:10.1016/j.jcps.2011.10.001 · Cited by 159
Siep, N., Roefs, A., Roebroeck, A. F., Havermans, R. C., Bonte, M. L., & Jansen, A. T. M. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.067 · Cited by 163
“There is now considerable support that obese people show abnormalities in the mesocorticolimbic circuitry, which – as some researchers believe – may cause them to overeat (Rothemund et al., 2007; Stice et al., 2008; Stoeckel et al., 2008; Volkow and Wise, 2005; Wang et al., 2001).”
Obesity-Related Differences between Women and Men in Brain Structure and Goal-Directed Behavior
Horstmann, A., Busse, F. P., Mathar, D., Müller, K., Lepsien, J., Schlögl, H., Kabisch, S., Kratzsch, J., Neumann, J., Stümvoll, M., et al. (2011) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2011.00058 · Cited by 170
Dimitropoulos, A., Tkach, J., Ho, A., & Kennedy, J. (2012) · Appetite · doi:10.1016/j.appet.2011.10.014 · Cited by 151
“The lateral OFC plays an important role in food-related neural circuitry and responds preferentially to high-calorie food cues (Goldstone et al., 2009; Rothemund et al., 2007; Stoeckel et al., 2008).”
BackgroundInfluentialLoeber, S., Grosshans, M., Korucuoglu, O., Vollmert, C., Vollstädt-Klein, S., Schneider, S., Wiers, R., Mann, K., & Kiefer, F. (2012) · International Journal of Obesity · doi:10.1038/ijo.2011.184 · Cited by 163
Aerobic exercise reduces neuronal responses in food reward brain regions
Evero, N., Hackett, L. C., Clark, R. D., Phelan, S., & Hagobian, T. A. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01365.2011 · Cited by 150
“Acute exercise, relative to no-exercise, resulted in significantly reduced neuronal responses in the left and right insula, right putamen, right rolandic operculum, and orbitofrontal cortex, all of which are consistent with reduced food reward (13, 48, 52).”
BackgroundRelation of obesity to neural activation in response to food commercials
Gearhardt, A. N., Yokum, S., Stice, E. M., Harris, J. L., & Brownell, K. D. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst059 · Cited by 153
“…memory (e.g., hippocampus), cognition (e.g, temporal lobe), and somatosensory processing (e.g., postcentral gyrus) in response to food cues (Bruce et al., 2010; Carnell & Wardle, 2007; Martin et al., 2009; Rothemund et al., 2007; Stice, Yokum, Bohon, Marti, & Smolen, 2010; Stoeckel et al., 2008).”
BackgroundResultYokum, S., & Stice, E. M. (2013) · International Journal of Obesity · doi:10.1038/ijo.2013.39 · Cited by 148
“Therefore, an alternative explanation is that because obese versus lean individuals show greater reward region response to palatable food images/cues (4, 7, 10), the former may need more intensive training to effectively inhibit reward region activation in response to palatable food images/cues.”
Devoto, F., Zapparoli, L., Bonandrini, R., Berlingeri, M., Ferrulli, A., Luzi, L., Banfi, G., & Paulesu, E. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.017 · Cited by 140
Effective connectivity of a reward network in obese women
Stoeckel, L. E., Kim, J., Weller, R. E., Cox, J. E., Cook, E. W., & Horwitz, B. (2009) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2009.05.016 · Cited by 147
“Other studies exposing obese individuals or those with higher BMI’s to food stimuli also found abnormal patterns of activation in these regions ([22], [23], [28], [43], [68]), as well as others ([40], [68]).”
Sun, X., Kroemer, N. B., Veldhuizen, M. G., Babbs, A. E., de Araújo, I. E., Gitelman, D. R., Sherwin, R. S., Sinha, R., & Small, D. M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3884-14.2015 · Cited by 147
“, 2013) and increased caudate response to food pictures (Rothemund et al., 2007; Stoeckel et al., 2008; Nummenmaa et al., 2012).”
BackgroundIndividual differences in the neurophysiology of reward and the obesity epidemic
Small, D. M. (2009) · International Journal of Obesity · doi:10.1038/ijo.2009.71 · Cited by 144
A core eating network and its modulations underlie diverse eating phenomena
Chen, J., Papies, E. K., & Barsalou, L. W. (2016) · Brain and Cognition · doi:10.1016/j.bandc.2016.04.004 · Cited by 144
“Rothemund et al. (2007) reported similar results for female adults, with BMI again predicting neural activity to high-calorie food pictures in taste and reward areas (anterior insula, striatum, posterior cingulate, OFC).”
Obesity and the Neurocognitive Basis of Food Reward and the Control of Intake
Ziauddeen, H., Alonso‐Alonso, M., Hill, J. O., Kelley, M. J., & Khan, N. A. (2015) · Advances in Nutrition · doi:10.3945/an.115.008268 · Cited by 158
Variety, palatability, and obesity
Johnson, F., & Wardle, J. (2014) · Advances in Nutrition · doi:10.3945/an.114.007120 · Cited by 138
Pharmacological management of appetite expression in obesity
Halford, J. C. G., Boyland, E. J., Blundell, J. E., Kirkham, T. C., & Harrold, J. A. (2010) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2010.19 · Cited by 142
“Moreover, in the obese, the effect of food cues on motivational systems seems to be resistant to the normal inhibitory consequences of ingestion”
Ng, J., Stice, E. M., Yokum, S., & Bohon, C. (2011) · Appetite · doi:10.1016/j.appet.2011.03.017 · Cited by 144
“We performed small volume correction (SVC) analyses with a radius of 10 mm based on peaks from prior studies examining food reward processing (Grabenhorst & Rolls, 2009; Plassman, O'Doherty, Shiv, & Rangel, 2008; Rothemund et al., 2007; Small, Zatorre, Dagher, Evans, & Jones-Gotman, 2001; Stice et al., 2008b) and we t…”
BackgroundMethodInfluentialFood Addiction: Implications for the Diagnosis and Treatment of Overeating
Adams, R. C., Sedgmond, J., Maizey, L., Chambers, C., & Lawrence, N. (2019) · Nutrients · doi:10.3390/nu11092086 · Cited by 158
“Increased activation of this reward system has also been shown in human participants during the presentation of food cues and meal consumption (Lawrence et al., 2012; Rothemund et al., 2007; Small, Jones-Gotman, & Dagher, 2003; Volkow et al., 2002; Volkow et al., 2003b).”
BackgroundEffects of dietary glycemic index on brain regions related to reward and craving in men
Lennerz, B. S., Alsop, D. C., Holsen, L. M., Stern, E., Rojas, R., Ebbeling, C. B., Goldstein, J. M., & Ludwig, D. S. (2013) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.064113 · Cited by 140
Burger, K. S., & Stice, E. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.12.009 · Cited by 138
“…the hedonic value and reward value of foods, including the insula, frontal operculum, parietal operculum, Rolandic operculum, lateral orbitofrontal cortex (OFC), amygdala, and striatum in response to pictures of palatable foods (Rothemund et al., 2007; Stoeckel et al., 2008; Stice et al., 2010b).”
Variability in Reward Responsivity and Obesity: Evidence from Brain Imaging Studies
Burger, K. S., & Stice, E. M. (2011) · Current Drug Abuse Reviews · doi:10.2174/1874473711104030182 · Cited by 138
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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