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Changes in brain activity related to eating chocolate: From pleasure to aversion
Abstract
We performed successive H(2)(15)O-PET scans on volunteers as they ate chocolate to beyond satiety. Thus, the sensory stimulus and act (eating) were held constant while the reward value of the chocolate and motivation of the subject to eat were manipulated by feeding. Non-specific effects of satiety (such as feelings of fullness and autonomic changes) were also present and probably contributed to the modulation of brain activity. After eating each piece of chocolate, subjects gave ratings of how pleasant/unpleasant the chocolate was and of how much they did or did not want another piece of chocolate. Regional cerebral blood flow was then regressed against subjects' ratings. Different groups of structures were recruited selectively depending on whether subjects were eating chocolate when they were highly motivated to eat and rated the chocolate as very pleasant [subcallosal region, caudomedial orbitofrontal cortex (OFC), insula/operculum, striatum and midbrain] or whether they ate chocolate despite being satiated (parahippocampal gyrus, caudolateral OFC and prefrontal regions). As predicted, modulation was observed in cortical chemosensory areas, including the insula and caudomedial and caudolateral OFC, suggesting that the reward value of food is represented here. Of particular interest, the medial and lateral caudal OFC showed opposite patterns of activity. This pattern of activity indicates that there may be a functional segregation of the neural representation of reward and punishment within this region. The only brain region that was active during both positive and negative compared with neutral conditions was the posterior cingulate cortex. Therefore, these results support the hypothesis that there are two separate motivational systems: one orchestrating approach and another avoidance behaviours.
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“Similarly, ventral striatal activity is initially high in response to palatable food but diminishes as individuals consume beyond satiety225.”
From Neural mechanisms of social homeostasis (2019) · cites this paper as [225]
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“Several neuroimaging studies examining the effects of hunger and satiety on activation to chemosensory stimuli have reported consistent activationwithin the insular cortex (Tataranni et al., 1999;Del Parigi et al., 2002b; Kringelbach et al., 2003; Uher et al., 2006), OFC; (Small et al., 2001;Del Parigi et al., 2002a;…”
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Brain activity in hunger and satiety: an exploratory visually stimulated fMRI study
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Effortful control, explicit processing, and the regulation of human evolved predispositions.
MacDonald, K. B. (2008) · Psychological Review · doi:10.1037/a0013327 · Cited by 238
Cherubino, P., Martinez-Levy, A. C., Caratù, M., Cartocci, G., Flumeri, G. D., Modica, E., Rossi, D., Mancini, M., & Trettel, A. (2019) · Computational Intelligence and Neuroscience · doi:10.1155/2019/1976847 · Cited by 260
“Several studies imply that unpleasantness of taste correlates with brain activity in the lateral OFC and left dorsal anterior insula/operculum [185, 186].”
BackgroundNeuropsychology of prefrontal cortex
Goyal, N., Siddiqui, S. V., Chatterjee, U., Kumar, D., & Siddiqui, A. (2008) · Indian Journal of Psychiatry · doi:10.4103/0019-5545.43634 · Cited by 248
Contributions of the Amygdala to Reward Expectancy and Choice Signals in Human Prefrontal Cortex
Hampton, A. N., Adolphs, R., Tyszka, J. M., & O'Doherty, J. P. (2007) · Neuron · doi:10.1016/j.neuron.2007.07.022 · Cited by 213
“When comparing responses to receipt of rewarding outcomes compared with punishing ones, in our control subjects we found significant activity relating to receipt of reward in medial PFC and medial OFC (Figure 6A), consistent with previous reports (Anderson et al., 2003; Knutson et al., 2001; O’Doherty et al., 2001, 20…”
Role of addiction and stress neurobiology on food intake and obesity
Sinha, R. (2018) · Biological Psychology · doi:10.1016/j.biopsycho.2017.05.001 · Cited by 211
Parigi, A. D., Gautier, J., Chen, K., Salbe, A. D., Ravussin, É., Reiman, E. M., & Tataranni, P. A. (2002) · PubMed · Cited by 206
Regional cerebral blood flow changes associated with clitorally induced orgasm in healthy women
Georgiadis, J. R., Kortekaas, R., Kuipers, R., Nieuwenburg, A., Pruim, J., Reinders, A. A. T. S., & Holstege, G. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05206.x · Cited by 205
“This cell group plays a crucial role in a wide range of rewarding behaviours (McBride et al., 1999), including euphoric states induced by drugs of abuse (Breiter et al., 1997; Sell et al., 1999), pleasurable music (Blood & Zatorre, 2001) and even eating chocolate (Small et al., 2001).”
BackgroundOpioid and orexin hedonic hotspots in rat orbitofrontal cortex and insula
Castro, D. C., & Berridge, K. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1705753114 · Cited by 214
The neurobiology of punishment
Seymour, B., Singer, T., & Dolan, R. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2119 · Cited by 240
Ellingsen, D., Leknes, S., Løseth, G. E., Wessberg, J., & Olausson, H. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01986 · Cited by 214
“When being touched by another individual, inferences about the identity, physical characteristics, and the intentions of the toucher, conveyed through visual and auditory stimuli, gives useful information about the importance of the touch and how preferable it is (Suvilehto et al., 2015).”
BackgroundCools, R., & Arnsten, A. F. T. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01100-8 · Cited by 216
“, the changing reward value of chocolate or other palatable foods as one eats to satiation [20, 21].”
BackgroundAmygdala damage impairs emotion recognition from music
Gosselin, N., Peretz, I., Johnsen, E., & Adolphs, R. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.07.012 · Cited by 198
Individual Differences in the Subjective Experience of Pain: New Insights Into Mechanisms and Models
Coghill, R. C. (2010) · Headache The Journal of Head and Face Pain · doi:10.1111/j.1526-4610.2010.01763.x · Cited by 216
O’Doherty, J. P. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1401.036 · Cited by 206
Biswas, D., & Szocs, C. (2019) · Journal of Marketing Research · doi:10.1177/0022243718820585 · Cited by 205
“These are the types of foods that satisfy the “reward center” of the brain (Menzies 2012; Small et al. 2001; Volkow, Wang, and Baler 2011).”
BackgroundHedonic-Specific Activity in Piriform Cortex During Odor Imagery Mimics That During Odor Perception
Bensafi, M., Sobel, N., & Khan, R. M. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00349.2007 · Cited by 217
“…that OFC activity is modulated by a considerable variety of factors, such as sensory-specific satiety (O'Doherty et al. 2000), motivation (Small et al. 2001), and lexical knowledge (de Araujo et al. 2005), the differences between our results and those of previous studies may be the…”
Hunger and satiety in anorexia nervosa: fMRI during cognitive processing of food pictures
Santel, S., Baving, L., Krauel, K., Münte, T. F., & Rotte, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.045 · Cited by 194
Identification of human gustatory cortex by activation likelihood estimation
Veldhuizen, M. G., Albrecht, J., Zelano, C., Boesveldt, S., Breslin, P. A. S., & Lundström, J. N. (2011) · Human Brain Mapping · doi:10.1002/hbm.21188 · Cited by 195
“…right hemisphere for pleasant stimuli, [Small et al., 2003; Zald and Pardo, 2000]), and (2) motivation to consume chemosensory stimuli (with activity in the medial and lateral OFC associated with increased and decreased motivation for consumption [Kringelbach et al., 2003; Small et al., 2001a]).”
BackgroundThe 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
“Functional magnetic resonance imaging (fMRI) provided initial evidence that hunger and satiety already affect stimulus perception (Uher et al., 2006; Cheng et al., 2007; Delparigi et al., 2005; Kringelbach et al., 2003; Tataranni et al., 1999; Small et al., 2001; LaBar et al., 2001; Morris and Dolan, 2001).”
BackgroundPersistence of abnormal neural responses to a meal in postobese individuals
DelParigi, A., Chen, K., Salbe, A. D., Hill, J. O., Wing, R. R., Reiman, E. M., & Tataranni, P. A. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802558 · Cited by 189
May, J. C., Delgado, M. R., Dahl, R. E., Stenger, V. A., Ryan, N. D., Fiez, J. A., & Carter, C. S. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.11.008 · Cited by 193
“Once ROIs were identified, MNI coordinates were transformed (http://www.mrc-cbu.cam.ac.uk/Imaging/mnispace .html) to standard Talairach coordinates (Talairach and Tournoux 1988) and inspected with Analysis of Functional NeuroImages software (Cox 1996).”
MethodParigi, A. D., Gautier, J., CHEN, K., Salbe, A. D., Ravussin, É., Reiman, E. M., & Tataranni, P. A. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04294.x · Cited by 192
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 203
Separable Substrates for Anticipatory and Consummatory Food Chemosensation
Small, D. M., Veldhuizen, M. G., Felsted, J. A., Mak, Y. E., & McGlone, F. P. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.021 · Cited by 190
Self-citationNeural Mechanisms Underlying Hyperphagia in Prader‐Willi Syndrome
Holsen, L. M., Zarcone, J. R., Brooks, W. M., Butler, M. G., Thompson, T. I., Ahluwalia, J. S., Nollen, N. L., & Savage, C. R. (2006) · Obesity · doi:10.1038/oby.2006.118 · Cited by 189
Eres, R., Decety, J., Louis, W. R., & Molenberghs, P. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.05.038 · Cited by 207
“…greater activation in the anterior insula occurs when observing videos of people with disgusted faces (Wicker et al., 2006) as well as when vicariously observing others experience unpleasant food (Jabbi et al., 2007), and in response to positive emotions such as pleasure (Small et al, 2001).”
BackgroundEnhanced affective brain representations of chocolate in cravers vs. non‐cravers
Rolls, E. T., & McCabe, C. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05724.x · Cited by 188
“Previous investigations in which brain responses to chocolate were measured did not include a comparison between cravers and noncravers (Small et al., 2001; Kringelbach et al., 2003), and indeed we”
BackgroundInfluentialObesity: Current and potential pharmacotherapeutics and targets
Narayanaswami, V., & Dwoskin, L. P. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.10.015 · Cited by 188
“Insula is involved in processing and evaluation of food cues and in craving for food (Small et al., 2001; Pelchat et al., 2004).”
Kringelbach, M. L., & Berridge, K. C. (2017) · Emotion Review · doi:10.1177/1754073916684558 · Cited by 199
Garavan, H. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0259-8 · Cited by 181
Andrews, M. M., Meda, S. A., Thomas, A. D., Potenza, M. N., Krystal, J. H., Worhunsky, P., Stevens, M. C., O'Malley, S., Book, G. A., Reynolds, B., et al. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.049 · Cited by 181
Metadata
- Authors
- Small, D. M.
- Affiliations
- Northwestern University (US)
- Corresponding author
- Small, D. M.
- ORCID
- Small, D. M.
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2001-09-01
- Volume
- 124
- Issue
- 9
- Pages
- 1720-1733
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W2243948722
- Cited by
- 1,179
- References
- 91
- Citations by year
- 2026: 14 · 2025: 30 · 2024: 19 · 2023: 39 · 2022: 22 · 2021: 37 · 2020: 71 · 2019: 40 · 2018: 40 · 2017: 54 · 2016: 56 · 2015: 52 · 2014: 55 · 2013: 55 · 2012: 77
- FWCI
- 10.96
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- chocolate consumption, food reward, satiety, food aversion, insula, striatum, midbrain, parahippocampal gyrus, posterior cingulate cortex, approach-avoidance motivation, regional cerebral blood flow, chemosensory processing
- MeSH terms
- Avoidance Learning, Brain, Cacao, Cerebrovascular Circulation, Feeding Behavior, Female, Humans, Male, Reward, Satiety Response, Taste, Tomography, Emission-Computed
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