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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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InfluentialNeural Correlates of Tasting Concentrated Quinine and Sugar Solutions
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“Brain imaging studies in humans have also reported a consistent pattern of MRS co-activation in response to various rewards, including food (Small et al., 2001), money (Knutson et al., 2001), humorous cartoons (Mobbs et al., 2003), music (Koelsch et al., 2006; Menon and Levitin, 2005), and pleasant…”
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“…signals in anterior OFC (Howard et al., 2015), as well as with studies showing that anterior OFC tracks satiety-related changes in reward value (Small et al., 2001; Gottfried et al., 2003), raising the possibility that anterior and posterior OFC differentially contribute to goal-directed…”
Reward Region Responsivity Predicts Future Weight Gain and Moderating Effects of the TaqIA Allele
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“…aversive-valuation signals residing in some of the same regions that we observe, namely in the lateral OFC and genual ACC (O’Doherty et al., 2001; Small et al., 2001; Beyond the striatum’s adaptive coding of value, its more general role in pain processing has been hotly debated (Leknes and…”
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de Araújo, I. E., Gutiérrez, R., Oliveira-Maia, A. J., Pereira, A., Nicolelis, M. A. L., & Simon, S. A. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.009 · Cited by 136
Stice, E. M., Yokum, S., Burger, K., Epstein, L. H., & Smolen, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1506-12.2012 · Cited by 136
“The pallidum, which is a part of the basal ganglia neighboring the dorsal striatum has a similar synaptic composition and encodes receipt of palatable food (Small et al., 2001; Bohon et al., 2009; Smeets et al., 2011).”
BackgroundMechanisms of the portion size effect. What is known and where do we go from here?
English, L., Lasschuijt, M. P., & Keller, K. (2014) · Appetite · doi:10.1016/j.appet.2014.11.004 · Cited by 134
Georgiadis, J. R., Reinders, A. A. T. S., Paans, A. M. J., Renken, R. J., & Kortekaas, R. (2009) · Human Brain Mapping · doi:10.1002/hbm.20733 · Cited by 134
“, 2006, 2007], primarily because of its role in urge suppression and behavioral release [Beauregard et al., 2001; Dougherty et al., 1999; Small et al., 2001], but the more medial areas have received less attention.”
BackgroundMethodPhysiological mechanisms by which non-nutritive sweeteners may impact body weight and metabolism
Burke, M. V., & Small, D. M. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.05.036 · Cited by 132
Self-citationPhysiology of women's sexual function: basic knowledge and new findings.
Salonia, A., Giraldi, A., Chivers, M. L., Georgiadis, J. R., Levin, R., Maravilla, K. R., & McCarthy, M. M. (2010) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2010.01810.x · Cited by 132
Le, D. S. N. T., Pannacciulli, N., Chen, K., Salbe, A. D., Hill, J. O., Wing, R. R., Reiman, E. M., & Krakoff, J. A. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.3.573 · Cited by 134
Homeostatic and non-homeostatic controls of feeding behavior: Distinct vs. common neural systems
Liu, C. M., & Kanoski, S. E. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.02.011 · Cited by 131
Marchand, W. R. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0280-y · Cited by 137
Neuroimaging in bulimia nervosa and binge eating disorder: A systematic review
Donnelly, B., Touyz, S., Hay, P., Burton, A., Russell, J., & Caterson, I. (2018) · Journal of Eating Disorders · doi:10.1186/s40337-018-0187-1 · Cited by 132
“The precentral gyrus is the site of the primary motor cortex while the insula has a central role in gustatory and hedonic taste processing and alongside the middle frontal gyrus, it is activated in response to pleasurable taste [58, 60, 61].”
BackgroundFunctional neuroimaging: a new generation of human brain studies in obesity research
Tataranni, P. A., & DelParigi, A. (2003) · Obesity Reviews · doi:10.1046/j.1467-789x.2003.00111.x · Cited by 132
Medial orbitofrontal cortex codes relative rather than absolute value of financial rewards in humans
Elliott, R., Agnew, Z. K., & Deakin, J. F. W. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06202.x · Cited by 128
“satiated), indicating that incentive, or value, properties of stimuli are coded in this region (O’Doherty et al., 2000; Small et al., 2001; Gottfried et al., 2002; Kringelbach et al., 2003).”
BackgroundInfluentialVBM signatures of abnormal eating behaviours in frontotemporal lobar degeneration
Whitwell, J. L., Sampson, E. L., Loy, C. T., Warren, J. E., Rossor, M. N., Fox, N. C., & Warren, J. D. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.12.006 · Cited by 130
Perfumers' expertise induces structural reorganization in olfactory brain regions
Delon‐Martin, C., Plailly, J., Fonlupt, P., Veyrac, A., & Royet, J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.11.044 · Cited by 138
Reduced frontal white matter integrity in Early-Onset schizophrenia: a preliminary study
Kumra, S., Ashtari, M., McMeniman, M., Vogel, J., Augustin, R., Becker, D. E., Nakayama, E. Y., Gyato, K., Kane, J. M., Lim, K. O., et al. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.02.025 · Cited by 128
Regional grey matter volume abnormalities in bulimia nervosa and binge-eating disorder
Schäfer, A., Vaitl, D., & Schienle, A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.063 · Cited by 122
“The elevated OFC reactivity has been interpreted to reflect altered reward processing as this region represents the hedonic value of food stimuli (Kringelbach and Rolls, 2004) and is activated during the experience and anticipation of pleasant taste (O'Doherty et al., 2002; Small et al., 2001; De Araujo et al., 2001;…”
Brain structures associated with executive functions during everyday events in a non-clinical sample
Takeuchi, H., Taki, Y., Sassa, Y., Hashizume, H., Sekiguchi, A., Fukushima, A., & Kawashima, R. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0444-z · Cited by 146
“2008), pleasantness felt when eating chocolate (Small et al. 2001) and seeing the face of the person we love (Xu et al.”
BackgroundElliott, R., Newman, J. L., Longe, O. A., & Deakin, J. F. W. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.10.010 · Cited by 134
Griffiths, K. R., Morris, R. W., & Balleine, B. W. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00101 · Cited by 118
“…when humans were presented with food outcomes, the degree of hunger and pleasantness caused graded OFC/vmPFC BOLD activity (Morris and Dolan, 2001; Kringelbach et al., 2003) that was reduced after satiation with the presented food (O’doherty et al., 2000; Small et al., 2001; Valentin et al., 2007).”
BackgroundReber, J., Feinstein, J. S., O’Doherty, J. P., Liljeholm, M., Adolphs, R., & Tranel, D. (2017) · Brain · doi:10.1093/brain/awx105 · Cited by 134
“These results are of considerable importance because functional MRI studies in humans (O’Doherty et al., 2000; Small et al., 2001; Kringelbach et al., 2003; Rolls et al., 2003) and electrophysiology studies in non-human primates (Critchley and Rolls, 1996) frequently report the presence of neural…”
ResultHarrar, V., & Spence, C. (2013) · Flavour · doi:10.1186/2044-7248-2-21 · Cited by 124
“The effect of colour (or colour contrast) on flavour perception and consumption behaviour might be mediated by emotion [22,23], especially since thoughts of food and emotions activate similar brain areas [24,25].”
BackgroundResting-state functional connectivity of the human hypothalamus
Kullmann, S., Heni, M., Linder, K., Zipfel, S., Häring, H., Veit, R., Fritsche, A., & Preissl, H. T. (2014) · Human Brain Mapping · doi:10.1002/hbm.22607 · Cited by 127
“Furthermore, several studies have illustrated that the OFC is involved in the integration of different food modalities and in reward evaluation [Kringelbach and Rolls, 2004; Rolls and Baylis, 1994; Small et al., 2001].”
BackgroundNeural correlates of sexual arousal in homosexual and heterosexual men.
Safron, A., Barch, B., Bailey, J. M., Gitelman, D. R., Parrish, T. B., & Reber, P. J. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.2.237 · Cited by 128
The neural circuitry of reward and its relevance to psychiatric disorders
Chau, D. T., Roth, R. M., & Green, A. I. (2004) · Current Psychiatry Reports · doi:10.1007/s11920-004-0026-8 · Cited by 123
“Positron emission tomography and fMRI studies also have shown that brain reward circuitry in healthy humans is activated to various primary and secondary rewards including food such as chocolate [ 61 ], listening to enjoyable music [62], looking at beautiful faces [63] or humorous cartoons [64], and sexual activity [6…”
BackgroundSelective involvement by the medial orbitofrontal cortex in biasing risky, but not impulsive, choice
Stopper, C. M., Green, E. B., & Floresco, S. B. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhs297 · Cited by 117
“Early studies pointed to mOFC activity correlating with positive outcomes or the reward (O’Doherty et al. 2001; Small et al. 2001; Gottfried et al. 2002; Anderson et al. 2003; Rolls et al. 2003; Ursu and Carter, 2005; Kim et al. 2006).”
BackgroundWindmann, S., Kirsch, P., Mier, D. U., Stark, R. M., Walter, B., Güntürkün, O., & Vaitl, D. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.7.1198 · Cited by 127
“…primary reinforcers such as food and smell might activate these lateral regions not because they elicit aversive experiences, but because of their ambiguous and transient motivational qualities that call for regulation of consummatory behavior (Gottfried et al., 2003; Small et al., 2000).”
BackgroundWu, Q., Lemus, M. B., Stark, R., Bayliss, J. A., Reichenbach, A., Lockie, S. H., & Andrews, Z. B. (2014) · Endocrinology · doi:10.1210/en.2013-1831 · Cited by 124
Addicted to Love: What Is Love Addiction and When Should It Be Treated?
Earp, B. D., Wudarczyk, O. A., Foddy, B., & Savulescu, J. (2017) · Philosophy, psychiatry & psychology · doi:10.1353/ppp.2017.0011 · Cited by 123
Burger, K. S., & Stice, E. (2012) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.027003 · Cited by 122
The appreciation of wine by sommeliers: a functional magnetic resonance study of sensory integration
Castriota-Scanderbeg, A., Hagberg, G. E., Cerasa, A., Committeri, G., Galati, G., Patria, F., Pitzalis, S., Caltagirone, C., & Frackowiak, R. S. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.11.045 · Cited by 121
Pain relief as an opponent process: a psychophysical investigation
Leknes, S., Brooks, J. C. W., Wiech, K., & Tracey, I. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06380.x · Cited by 124
“For instance, food tastes better when it relieves hunger (Small et al., 2001; Kringelbach et al., 2003).”
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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