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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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Individual differences in risk preference predict neural responses during financial decision-making
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“The PCC, on the other hand, has been implicated in emotional processing (e.g. Chandrasekhar et al., 2008; Maddock et al., 2003; Small et al., 2001; Vogt et al., 2003; for reviews see Maddock (1999) and Vogt et al. (2006)), selfreflection and self-imagery (Johnson et al., 2002; Kircher et al., 2001,…”
BackgroundA scarcity mindset alters neural processing underlying consumer decision making
Huijsmans, I., Ma, I., Micheli, L., Civai, C., Stallen, M., & Sanfey, A. G. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1818572116 · Cited by 103
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Trace elements in cocoa solids and chocolate: An ICPMS study
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“In an H2(15)O-PET study in healthy self-proclaimed “chocolate-lovers” (Small et al., 2001), it was also found that rCBF in the dorsal striatum decreased along with decreased motivation to eat, providing further evidence for its role in the initiation of feeding behavior.”
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“Rewarding stimuli activate certain emotional regions of the brain, and the regions of the brain activated by rewards versus punishments are different (e.g., Blood and Zatorre 2001; Damasio 1999; Damasio et al. 2000; Small et al. 2001).”
BackgroundUnderstanding the human parental brain: A critical role of the orbitofrontal cortex
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“Results: Animal and human data combined to show a core aversion-related network, consisting of similar cortical (i.e. MCC, PCC, AI, DMPFC, RTG, SMA, VLOFC; see results section or abbreviation section for full names) and subcortical (i.e. Amyg, BNST, DS, Hab, Hipp/Parahipp, Hyp, NAc, NTS, PAG, PBN, raphe, septal nuclei…”
BackgroundInfluentialSubregions of the ventral striatum show preferential coding of reward magnitude and probability
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BackgroundThe value of identity: olfactory notes on orbitofrontal cortex function
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“Specifically, resection of the amygdala for the treatment of pharmacologically intractable epilepsy results in increases in taste intensity perception (Small et al., 2001b,c).”
BackgroundSelf-citationCartwright, F., & Stritzke, W. G. K. (2007) · Eating Behaviors · doi:10.1016/j.eatbeh.2007.01.006 · Cited by 86
Thomas, J. M., Higgs, S., Dourish, C. T., Hansen, P., Harmer, C. J., & McCabe, C. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.097543 · Cited by 87
Kawamoto, T., Onoda, K., Nakashima, K., Nittono, H., Yamaguchi, S., & Ura, M. (2012) · Frontiers in Evolutionary Neuroscience · doi:10.3389/fnevo.2012.00011 · Cited by 85
“Activation in this region is associated with the regulation or inhabitation of negative affect (Hariri et al., 2000; Small et al., 2001; Petrovic et al., 2002) as well as pain-induced distress (Eisenberger et al.”
BackgroundRybnicek, R., Bergner, S., & Gutschelhofer, A. (2017) · Review of Managerial Science · doi:10.1007/s11846-017-0252-1 · Cited by 133
“Kohls et al. (2013), for instance, R. Rybnicek et al. found activations in the putamen and thalamus when social approval was anticipated, whereas Smith et al. (2010) reported activations in these two brain areas when research participants felt rewarded after looking at attractive faces.”
ResultSeparating subjective emotion from the perception of emotion-inducing stimuli: An fMRI study
Garrett, A. S., & Maddock, R. J. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.05.024 · Cited by 82
“…making judgments that require reflecting on subjective feelings, including value judgments {Zysset, 2002 #85}, feelings of sadness (Levesque et al., 2003), enjoyment while eating chocolate (Small et al., 2001), pleasant and painful touch (Rolls et al., 2003), and taste (Kringelbach et al., 2003).”
BackgroundGenetically Determined Differences in Brain Response to a Primary Food Reward: Figure 1.
Felsted, J. A., Ren, X., Chouinard-Decorte, F., & Small, D. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5483-09.2010 · Cited by 84
“source and target regions that are also known to play a role in food reward, including the midbrain, striatum, thalamus, OFC, insula, and amygdala (Small et al., 2001; Sánchez-González et al., 2005; GarcíaCabezas et al., 2007, 2009).”
BackgroundInfluentialSelf-citationSerotonin shapes risky decision making in monkeys
Long, A., Kuhn, C. M., & Platt, M. L. (2009) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsp020 · Cited by 89
“Since calculations of both time and probability-weighted value contribute to time-sensitive decision making (Kacelnik and Bateson, 1996; Evenden, 1999a; Hayden and Platt, 2007), as does the context within which choices are made (Kahneman and Tversky, 1979; Small et al., 2001; Huettel et al., 2005), impulsive behavior…”
BackgroundKühn, S., Müller, B. C. N., van Baaren, R. B., Wietzker, A., Dijksterhuis, A., & Braß, M. (2010) · Social Neuroscience · doi:10.1080/17470911003633750 · Cited by 88
“Interestingly, this network is very similar to brain networks activated when we receive primary reward (e.g., while eating chocolate; Small et al., 2001).”
BackgroundOvereating Behavior and Striatal Dopamine with 6--Fluoro-L--Tyrosine PET
Wilcox, C. E., Braskie, M. N., Kluth, J. T., & Jagust, W. J. (2010) · Journal of Obesity · doi:10.1155/2010/909348 · Cited by 82
“Increased fMRI activation, increased regional cerebral blood flow, and increased dopamine release in the dorsal striatum are associated with food administration but appear to decrease as motivation to eat decreases [17, 30, 31].”
BackgroundCentral Gustatory Processing in Humans
Small, D. M. (2006) · KARGER eBooks · doi:10.1159/000093761 · Cited by 82
Self-citationVocks, S., Herpertz, S., Rosenberger, C., Senf, W., & Gizewski, E. R. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2010.07.012 · Cited by 82
Wright, H., Li, X., Fallon, N. B., Crookall, R., Giesbrecht, T., Thomas, A. K., Halford, J. C. G., Harrold, J. A., & Stančák, A. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13182 · Cited by 84
“While research has demonstrated the involvement of the mid-insula in feeding behaviour (Small et al., 2001; Li et al., 2012a), and some association between DMN activity and obesity (Tregellas et al., 2011; Kullmann et al., 2012; McFadden et al., 2013), it is likely in the context of the current…”
BackgroundFeed-forward mechanisms: Addiction-like behavioral and molecular adaptations in overeating
Alsiö, J., Olszewski, P. K., Levine, A. S., & Schiöth, H. B. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.01.002 · Cited by 81
“Brain imaging studies have identified neuroanatomical structures activated during food craving, including the caudal and medial orbitofrontal cortex, amygdala, striatum and midbrain [147,164,192].”
Processing of pictorial food stimuli in patients with eating disorders—A systematic review
Giel, K. E., Teufel, M., Friederich, H., Hautzinger, M., Enck, P., & Zipfel, S. (2010) · International Journal of Eating Disorders · doi:10.1002/eat.20785 · Cited by 80
Learning networks in health and Parkinson's disease: Reproducibility and treatment effects
Carbon, M., Ghilardi, M. F., Feigin, A., Fukuda, M., Silvestri, G., Mentis, M. J., Ghez, C. P., Moeller, J. R., & Eidelberg, D. (2003) · Human Brain Mapping · doi:10.1002/hbm.10115 · Cited by 81
Making claims: functional foods for managing appetite and weight
Blundell, J. E. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.224 · Cited by 80
“However, in recent years the use of brain imaging procedures such as PET and functional MRI has enabled activity in different brain regions to be correlated with states of high and low hunge”
The Hedonic Brain: A Functional Neuroanatomy of Human Pleasure
Kringelbach, M. L. (2009) · Oxford University Press eBooks · doi:10.1093/oso/9780195331028.003.0014 · Cited by 80
Cytoarchitecture and probability maps of the human medial orbitofrontal cortex
Henssen, A. G., Zilles, K., Palomero‐Gallagher, N., Schleicher, A., Mohlberg, H., Gerboga, F., Eickhoff, S. B., Bludau, S., & Amunts, K. (2015) · Cortex · doi:10.1016/j.cortex.2015.11.006 · Cited by 79
The Influence of Consumer Distractions on the Effectiveness of Food-Sampling Programs
Nowlis, S. M., & Shiv, B. (2005) · Journal of Marketing Research · doi:10.1509/jmkr.42.2.157.62287 · Cited by 79
Evidence of increased activation underlying cognitive control in ecstasy and cannabis users
Roberts, G. M. P., & Garavan, H. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.192 · Cited by 83
Siessmeier, T. (2003) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.74.7.922 · Cited by 79
Neurobiological features of binge eating disorder
Balodis, I. M., Grilo, C. M., & Potenza, M. N. (2015) · CNS Spectrums · doi:10.1017/s1092852915000814 · Cited by 79
Zamorano, A. M., Cifré, I., Montoya, P., Riquelme, I., & Kleber, B. (2017) · Human Brain Mapping · doi:10.1002/hbm.23682 · Cited by 81
The role of hedonics in the Human Affectome
Becker, S., Bräscher, A., Bannister, S., Bensafi, M., Calma‐Birling, D., Chan, R. C. K., Eerola, T., Ellingsen, D., Ferdenzi, C., Hanson, J. L., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.003 · Cited by 93
Amygdala response to sucrose consumption is inversely related to artificial sweetener use
Rudenga, K. J., & Small, D. M. (2011) · Appetite · doi:10.1016/j.appet.2011.12.001 · Cited by 78
Self-citationOkamoto, M., & Dan, I. (2012) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2012.11.001 · Cited by 78
Food neophobia and its relation with olfaction
Demattè, M. L., Endrizzi, I., & Gasperi, F. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00127 · Cited by 77
“MINI REVIEW ARTICLE published: 17 February 2014 doi: 10.3389/fpsyg.2014.00127 Food neophobia and its relation with olfaction”
BackgroundInfluentialOlfactory dysfunction in the pathophysiological continuum of dementia
Bathini, P., Brai, E., & Auber, L. A. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.100956 · Cited by 77
“The valence-dependent medio-lateral pattern of the OFC is conserved for other sensory modalities (Gottfried, 2006; Small et al., 2001; OöDoherty et al., 2003).”
BackgroundGraded Encoding of Food Odor Value in theDrosophilaBrain
Beshel, J., & Zhong, Y. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2605-13.2013 · Cited by 79
“In humans, evidence suggests that there may be significant overlap in areas activated by food odors and areas responsible for processing the hedonic value of chemosensory stimuli (Small et al., 2001; O’Doherty et al., 2002).”
BackgroundNusslock, R., Young, C. B., & Damme, K. S. F. (2014) · Behaviour Research and Therapy · doi:10.1016/j.brat.2014.08.011 · Cited by 83
“Several neuroimaging studies indicate that sensory and abstract rewards recruit the OFC (Blood& Zatorre, 2001; Knutson, Westdorp, Kaiser, & Hommer, 2000; Small et al., 2001).”
Background
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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