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 using BOLD fMRI have shown selective overactivity in the nucleus accumbens and related brain areas in obese compared with lean individuals when shown images of highly palatable food.
“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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BackgroundReinert, K. R. S., Po'e, E. K., & Barkin, S. L. (2013) · Journal of Obesity · doi:10.1155/2013/820956 · Cited by 344 · see citing works
Smith, D. G., & Robbins, T. W. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.026 · Cited by 348 · see citing works
“striatal circuitry activation during anticipation of high-caloric foods as compared with lean control subjects (10,74,75).”
Murdaugh, D. L., Cox, J. E., Cook, E. W., & Weller, R. E. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.071 · Cited by 341 · see citing works
“Indeed, our results are congruent with those of other neuroimaging experiments providing evidence for an “orexigenic network” that encompasses such regions as the insula, VTA, NAc, and ACC, which are more active during hunger and fasting and are thought to motivate one to consume calorically-dense foods (e.g., Del Par…”
BackgroundResultInfluentialIs food addiction a valid and useful concept?
Ziauddeen, H., & Fletcher, P. C. (2012) · Obesity Reviews · doi:10.1111/j.1467-789x.2012.01046.x · Cited by 334 · see citing works
“Different predictions from the addiction model have been borne out in some of these studies such as increased striatal and orbitofrontal activation on viewing food images (59,60) or in anticipation of actual food rewards (61), decreased consummatory reward activation (62) and decreased prefrontal metabolism (63) in ob…”
BackgroundStice, E. M., Yokum, S., Bohon, C., Marti, N., & Smolen, A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.01.081 · Cited by 333 · see citing works
Diekhof, E. K., Kaps, L., Falkai, P., & Gruber, O. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.02.007 · Cited by 332 · see citing works
McElroy, S. L., Hudson, J. I., Mitchell, J. E., Wilfley, D., Ferreira-Cornwell, M. C., Gao, J., Wang, J., Whitaker, T., Jonas, J., & Gasior, M. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2014.2162 · Cited by 322 · see citing works
Taste representation in the human insula
Small, D. M. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0266-9 · Cited by 300 · see citing works
“high calorie foods (Rothemund et al. 2007) and to the anticipated as well as actual ingestion of milkshake (Stice et al.”
BackgroundThe Prefrontal Cortex and Obesity: A Health Neuroscience Perspective
Lowe, C. J., Reichelt, A. C., & Hall, P. A. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.01.005 · Cited by 295 · see citing works
Relation of obesity to consummatory and anticipatory food reward
Stice, E. M., Spoor, S. T. P., Ng, J., & Zald, D. H. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.03.020 · Cited by 289 · see citing works
“Rothemund [113] found greater dorsal striatum responses to pictures of high-calorie foods in obese verse lean adults and that BMI”
BackgroundMorris, M. J., Beilharz, J. E., Maniam, J., Reichelt, A. C., & Westbrook, R. F. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.002 · Cited by 285 · see citing works
Bruce, A. S., Holsen, L. M., Chambers, R. J., Martin, L. E., Brooks, W. M., Zarcone, J. R., Butler, M. G., & Savage, C. R. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.84 · Cited by 282 · see citing works
Neural Mechanisms Associated With Food Motivation in Obese and Healthy Weight Adults
Martin, L. E., Holsen, L. M., Chambers, R. J., Bruce, A. S., Brooks, W. M., Zarcone, J. R., Butler, M. G., & Savage, C. R. (2009) · Obesity · doi:10.1038/oby.2009.220 · Cited by 278 · see citing works
“Results of the current study are, however, consistent with previous studies, which examined only female participants (7,26,27).”
BackgroundResultInfluentialThe contribution of brain reward circuits to the obesity epidemic
Stice, E., Figlewicz, D. P., Gosnell, B. A., Levine, A. S., & Pratt, W. E. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.12.001 · Cited by 274 · see citing works
“…regions (ventral lateral prefrontal cortex [vlPFC]); and in somatosensory regions, in response to high-fat/high-sugar food images relative to control images (e.g., Bruce et al. 2010; Martin et al., 2009; Nummenmaa et al., 2012; Rothemund et al., 2007; Stoeckel et al., 2008; Stice et al., 2010).”
BackgroundKullmann, S., Heni, M., Veit, R., Ketterer, C., Schick, F., Häring, H., Fritsche, A., & Preissl, H. T. (2011) · Human Brain Mapping · doi:10.1002/hbm.21268 · Cited by 273 · see citing works
“…reduced dopamine D2 receptor availability in obese individuals [Wang et al., 2001] and exhibited greater activation to high caloric food stimuli [Rothemund et al., 2007; Stoeckel et al., 2008], but less activation in response to food consumption in obese individuals [Stice et al., 2008].”
BackgroundBrooks, S. J., Cedernaes, J., & Schiöth, H. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060393 · Cited by 269 · see citing works
Hormonal and neural mechanisms of food reward, eating behaviour and obesity
Murray, S. M., Tulloch, A. J., Gold, M. S., & Avena, N. M. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.91 · Cited by 267 · see citing works
Regulation of dietary choice by the decision-making circuitry
Rangel, A. (2013) · Nature Neuroscience · doi:10.1038/nn.3561 · Cited by 246 · see citing works
Wang, G.-J., Volkow, N. D., Telang, F., Jayne, M., Ma, Y., Pradhan, K., Zhu, W., Wong, C. T., Thanos, P. K., Geliebter, A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807423106 · Cited by 242 · see citing works
“Indeed a recent fMRI study using the blood oxygen level dependent (BOLD) signal showed obese subjects activated striatum and OFC as well as insula (brain region involved with interoception for food signals that is also innervated by DA terminals) while viewing pictures of high-caloric food (7).”
BackgroundLawrence, N. S., Hinton, E. C., Parkinson, J. A., & Lawrence, A. D. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.06.070 · Cited by 242 · see citing works
“These data are also consistent with findings in obese individuals, who show increased striatal activation to food cues (Rothemund et al., 2007; Stoeckel et al., 2008) that is predictive of weight gain (Murdaugh et al., 2012), in addition to reduced self-control (Nederkoorn et al., 2006a,b).”
Effect of combined naltrexone and bupropion therapy on the brain’s reactivity to food cues
Wang, G.-J., Tomasi, D. G., Volkow, N. D., Wang, R., Telang, F., Caparelli, E. C., & Dunayevich, E. (2013) · International Journal of Obesity · doi:10.1038/ijo.2013.145 · Cited by 242 · see citing works
Pursey, K. M., Stanwell, P., Callister, R. J., Brain, K., Collins, C. E., & Burrows, T. L. (2014) · Frontiers in Nutrition · doi:10.3389/fnut.2014.00007 · Cited by 239 · see citing works
“Additionally, obese individuals displayed greater activation to food cues in areas involved in motor learning and coordination such as hand-to-mouth movements and swallowing [insula (26, 33, 41, 43, 47), putamen (28, 41, 47), thalamus (33, 41), caudate (28, 45, 47)] as well as risk aversion [inferior frontal gyrus (41…”
BackgroundIncreased neural processing of rewarding and aversive food stimuli in recovered anorexia nervosa
Cowdrey, F. A., Park, R. J., Harmer, C. J., & McCabe, C. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.028 · Cited by 233 · see citing works
Striatocortical pathway dysfunction in addiction and obesity: differences and similarities
Tomasi, D. G., & Volkow, N. D. (2012) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2012.735642 · Cited by 232 · see citing works
“Brain activation in dorsal and ventral striatum, insula, hippocampus, OFC, amygdala, medial PFC and ACC elicited by visual exposures to high caloric foods was higher for obese than for control women (Rothemund et al., 2007; Stoeckel et al., 2008).”
BackgroundNummenmaa, L., Hirvonen, J., Hannukainen, J. C., Immonen, H., Lindroos, M. M., Salminen, P., & Nuutila, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031089 · Cited by 220 · see citing works
“However, it should also be noted that some prior studies [19] have reported elevated frontal responses to food pictures in obese versus normal-weight individuals.”
BackgroundInfluentialThe brain tracks the energetic value in food images
Toepel, U., Knebel, J., Hudry, J., le Coutre, J., & Murray, M. M. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.005 · Cited by 223 · see citing works
“…(Wang et al., 2004), and multisensory combinations (Gottfried et al., 2003; Small et al., 2004; Geliebter et al., 2006), but also to solely viewing food images (Killgore et al., 2003; Simmons et al., 2005; Beaver et al., 2006; Santel et al., 2006; Rothemund et al., 2007; Stoeckel et al., 2008).”
BackgroundInfluentialIs Food Addictive? A Review of the Science
Gearhardt, A. N., & LaFata, E. M. (2021) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-110420-111710 · Cited by 222 · see citing works
Homeostasis Meets Motivation in the Battle to Control Food Intake
Ferrario, C. R., Labouèbe, G., Liu, S., Nieh, E. H., Routh, V. H., Xu, S., & O’Connor, E. C. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2338-16.2016 · Cited by 213 · see citing works
“Obese and overweight individuals also show enhanced striatal activation in response to food-predictive cues (Rothemund et al., 2007; Stoeckel et al., 2008; Demos et al., 2012), but reduced striatal activation following palatable food receipt (Stice et al.”
BackgroundMonetary Reward Processing in Obese Individuals With and Without Binge Eating Disorder
Balodis, I. M., Hedy Kober, A., Worhunsky, P. D., White, M. A., Stevens, M. C. G., Pearlson, G. D., Sinha, R., Grilo, C. M., & Potenza, M. N. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.014 · Cited by 210 · see citing works
“Striatal activity is associated with reward processing tasks (15–18,26,27), and altered striatal responses are associated with obesity and weight gain; however, although some studies demonstrate diminished activity after palatable food intake in obese individuals, others report increased striatal responding (6,22,28,2…”
Hendrikse, J. J., Cachia, R. L., Kothe, E. J., McPhie, S., Skouteris, H., & Hayden, M. J. (2015) · Obesity Reviews · doi:10.1111/obr.12265 · Cited by 206 · see citing works
“The neuroimaging literature reported altered reward circuitry interactions (19) and variable strengths of cortical connectivity (18,20,25,26,31,34) between obese and healthy weight individuals in response to food stimuli.”
BackgroundNeural Correlates of Stress- and Food Cue–Induced Food Craving in Obesity
Jastreboff, A. M., Sinha, R., Lacadie, C., Small, D. M., Sherwin, R. S., & Potenza, M. N. (2013) · Diabetes Care · doi:10.2337/dc12-1112 · Cited by 204 · see citing works
Sex differences in neural responses to stress and alcohol context cues
Seo, D., Jia, Z., Lacadie, C., Tsou, K. A., Bergquist, K. L., & Sinha, R. (2010) · Human Brain Mapping · doi:10.1002/hbm.21165 · Cited by 199 · see citing works
Alterations of the salience network in obesity: A resting‐state fMRI study
García‐García, I., Jurado, M. Á., Garolera, M., Segura, B., Sala‐Llonch, R., Marqués‐Iturria, I., Pueyo, R., Sender‐Palacios, M. J., Vernet‐Vernet, M., Narberhaus, A., et al. (2013) · Human Brain Mapping · doi:10.1002/hbm.22104 · Cited by 200 · see citing works
Yokum, S., Ng, J., & Stice, E. M. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.175 · Cited by 197 · see citing works
The impact of hunger on food cue processing: An event-related brain potential study
Stockburger, J., Schmälzle, R., Flaisch, T., Bublatzky, F., & Schupp, H. T. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.04.071 · Cited by 191 · see citing works
“Furthermore, fMRI studies observed different activation patterns in higher order visual associative regions for food pictures, as compared to various control stimuli (e.g., tools, household objects or buildings; LaBar et al., 2001; Morris and Dolan, 2001; Simmons et al., 2005; Rothemund et al., 2007; Stoeckel et al.,…”
BackgroundCentral nervous system regulation of eating: Insights from human brain imaging
Farr, O. M., Li, C. R., & Mantzoros, C. S. (2016) · Metabolism · doi:10.1016/j.metabol.2016.02.002 · Cited by 191 · see citing works
“[109] Rothemund Y, Preuschhof C, Bohner G, Bauknecht HC, Klingebiel R, Flor H, et al.”
The role of reward circuitry and food addiction in the obesity epidemic: An update
Leigh, S.-J., & Morris, M. J. (2018) · Biological Psychology · doi:10.1016/j.biopsycho.2016.12.013 · Cited by 191 · see citing works
Frascella, J., Potenza, M. N., Brown, L. L., & Childress, A. R. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05420.x · Cited by 191 · see citing works
Obesity: Pathophysiology and Intervention
Zhang, Y., Liu, J., Yao, J., Ji, G., Qian, L., Wang, J., Zhang, G., Tian, J., Nie, Y., Zhang, Y., et al. (2014) · Nutrients · doi:10.3390/nu6115153 · Cited by 191 · see citing works
“DA release in the dorsal striatum can directly impact food ingestion, and the magnitude of the release correlates with ratings of meal pleasantness [99].”
BackgroundHigh-fat food biases hypothalamic and mesolimbic expression of consummatory drives
Mazzone, C. M., Liang-Guallpa, J., Li, C., Wolcott, N. S., Boone, M. H., Southern, M., Kobzar, N. P., Salgado, I. D. A., Reddy, D., Sun, F., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0684-9 · Cited by 179 · see citing works
Garavan, H. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0259-8 · Cited by 181 · see citing works
Robinson, M. J. F., Burghardt, P. R., Patterson, C. M., Nobile, C. W., Akil, H., Watson, S. J., Berridge, K. C., & Ferrario, C. R. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.71 · Cited by 185 · see citing works
Food related processes in the insular cortex
Frank, S., Kullmann, S., & Veit, R. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00499 · Cited by 182 · see citing works
Reward processing in obesity, substance addiction and non‐substance addiction
García‐García, I., Horstmann, A., Jurado, M. Á., Garolera, M., Chaudhry, S. J., Margulies, D. S., Villringer, A., & Neumann, J. (2014) · Obesity Reviews · doi:10.1111/obr.12221 · Cited by 177 · see citing works
Neural vulnerability factors that increase risk for future weight gain
Stice, E., & Yokum, S. (2016) · Psychological Bulletin · doi:10.1037/bul0000044 · Cited by 179 · see citing works
“Apparently consistent with the incentive sensitization theory, obese versus lean humans show greater responsivity of brain regions associated with reward and motivation (striatum, amygdala, OFC) to pictures of high-calorie foods versus low-calorie foods and control images (e.g., Bruce et al. 2010; Dimitropoulos, Tkach…”
BackgroundHedonic and incentive signals for body weight control
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 173 · see citing works
“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 172 · see citing works
“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 170 · see citing works
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 · see citing works
“…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 165 · see citing works
Functional brain imaging of appetite
Dagher, A. (2012) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.02.009 · Cited by 164 · see citing works
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 · see citing works
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 · see citing works
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 163 · see citing works
“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 · see citing works
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 · see citing works
Milton, A. L., Lee, J. L. C., & Everitt, B. J. (2008) · Learning & Memory · doi:10.1101/lm.825008 · Cited by 161 · see citing works
“…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 · see citing works
“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 156 · see citing works
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 155 · see citing works
“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 155 · see citing works
Dimitropoulos, A., Tkach, J., Ho, A., & Kennedy, J. (2012) · Appetite · doi:10.1016/j.appet.2011.10.014 · Cited by 151 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
“…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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
“, 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 · see citing works
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 · see citing works
“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 144 · see citing works
Variety, palatability, and obesity
Johnson, F., & Wardle, J. (2014) · Advances in Nutrition · doi:10.3945/an.114.007120 · Cited by 138 · see citing works
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 · see citing works
“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 141 · see citing works
“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 143 · see citing works
“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 · see citing works
Burger, K. S., & Stice, E. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.12.009 · Cited by 138 · see citing works
“…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 · see citing works
- 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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