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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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Self-face evaluation and self-esteem in young females: An fMRI study using contrast effect
Oikawa, H., Sugiura, M., Sekiguchi, A., Tsukiura, T., Miyauchi, C. M., Hashimoto, T., Takano‐Yamamoto, T., & Kawashima, R. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.098 · Cited by 59
“…(e.g., ventral tegmental area (VTA), orbitofrontal cortex (OFC), and ventral striatum) responds not only to primary rewards (Berns et al., 2001; Small et al., 2001), but also to abstract and social rewards such as being liked (Davey et al., 2010) or having a good reputation (Izuma et al.,…”
Motivational Salience Modulates Early Visual Cortex Responses across Task Sets
Rossi, V., Vanlessen, N., Bayer, M., Graß, A., Pourtois, G., & Schacht, A. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01093 · Cited by 56
The human posterior cingulate and the stress-response benefits of viewing green urban landscapes
Chang, D. H. F., Jiang, B., Wong, N., Wong, J. J., Webster, C. J., & Lee, T. M. C. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117555 · Cited by 57
“…b t t 2 n a u e s g n c o a a s a t r l t q t s r g s – u i u e a p a H fi o t t a a 2 i d m i m t t m m f s e A o K U o A W s r Papez, 1937 ), although it has also been implicated in motivation, re- ard, and valuation, activating with changes in subjective motivational tate ( Small et al., 2001 ).”
BackgroundInforming others is associated with behavioral and neural signatures of value.
Tamir, D., Zaki, J., & Mitchell, J. P. (2015) · Journal of Experimental Psychology General · doi:10.1037/xge0000122 · Cited by 59
Whitwell, J. L., Jack, C. R., Senjem, M. L., Parisi, J. E., Boeve, B. F., Knopman, D. S., Dickson, D. W., Petersen, R. C., & Josephs, K. A. (2009) · Neurodegenerative Diseases · doi:10.1159/000209507 · Cited by 53
Viviani, R. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00123 · Cited by 54
Winter, S. R., Yokum, S., Stice, E. M., Osipowicz, K. Z., & Lowe, M. R. (2017) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.141143 · Cited by 56
“In healthy individuals, greater insula activity has been observed in response to milkshake receipt in frequent milkshake consumers (24) as well as to passive viewing of appetitive food images (25, 26), thereby suggesting that this region is related to the motivational salience of palatable foods.”
BackgroundModality general and modality specific coding of hedonic valence
Miskovic, V., & Anderson, A. K. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.12.012 · Cited by 55
The Role of the Parabrachial Nucleus in Taste Processing and Feeding
Scott, T. R., & Small, D. M. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.03906.x · Cited by 52
Self-citationYanagisawa, K., Masui, K., Furutani, K., Nomura, M., Ura, M., & Yoshida, H. (2010) · Social Neuroscience · doi:10.1080/17470919.2010.506139 · Cited by 53
Altered functional brain networks in Prader–Willi syndrome
Zhang, Y., Zhao, H., Qiu, S., Tian, J., Wen, X., Miller, J. L., von Deneen, K. M., Zhou, Z., Gold, M. S., & Liu, Y. (2013) · NMR in Biomedicine · doi:10.1002/nbm.2900 · Cited by 50
Asmaro, D., Jaspers‐Fayer, F., Sramko, V., Taake, I., Carolan, P. L., & Mario Liotti, A. (2012) · Appetite · doi:10.1016/j.appet.2012.01.030 · Cited by 56
“High motivation toward chocolate was associated with blood flow changes in medial OFC, insula, ventral striatum and midbrain (Small et al., 2001).”
Neuroimaging in Eating Disorders and Obesity: Implications for Research
den Eynde, F. V., & Treasure, J. L. (2008) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2008.07.016 · Cited by 53
Access conditions affect binge-type shortening consumption in rats
Wojnicki, F. H. E., Johnson, D. S., & Corwin, R. L. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.09.017 · Cited by 51
Cortico-limbic responsiveness to high-calorie food images predicts weight status among women
Killgore, W. D. S., Weber, M., Schwab, Z. J., Kipman, M., DelDonno, S. R., Webb, C. A., & Rauch, S. L. (2013) · International Journal of Obesity · doi:10.1038/ijo.2013.26 · Cited by 49
Value of freedom to choose encoded by the human brain
Fujiwara, J., Usui, N., Park, S. Q., Williams, T., Iijima, T., Taira, M., Tsutsui, K., & Tobler, P. N. (2013) · Journal of Neurophysiology · doi:10.1152/jn.01057.2012 · Cited by 56
“…food), and social rewards (e.g., beautiful faces, being evaluated positively by others) (e.g., Aharon et al. 2001; Goldstone et al. 2009; Gregorios-Pippas et al. 2009; Izuma et al. 2008; Kable and Glimcher 2007; McClure et al. 2003; Oyama et al. 2010; Small et al. 2001; Tobler et al. 2009).”
BackgroundReed, D. D., Naudé, G. P., Gelino, B. W., & Amlung, M. T. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108632591.011 · Cited by 48
Lasschuijt, M. P., de Graaf, K. C., & Mars, M. (2021) · Nutrients · doi:10.3390/nu13051391 · Cited by 55
“internal state modulates the activation of the insula and that this is associated with a reduction in affective value or pleasantness of the taste stimuli, specific satiation [63,67,69].”
BackgroundInfluentialHuman amygdala activations during nasal chemoreception
Patin, A., & Pause, B. M. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.10.009 · Cited by 59
Orbitofrontal Cortex Contributions to Food Selection and Decision Making
Zald, D. H. (2009) · Annals of Behavioral Medicine · doi:10.1007/s12160-009-9117-4 · Cited by 48
Nees, F., & Becker, S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.08.051 · Cited by 49
“For example, food tastes better when one is hungry (Small et al., 2001; Kringelbach et al., 2003) and heat feels pleasant when someone is cold but unpleasant when being warm (Cabanac et al.”
Appetite for destruction: Counterintuitive effects of attractive faces on people's food choices
Otterbring, T. (2019) · Psychology and Marketing · doi:10.1002/mar.21257 · Cited by 49
Disgust: Sensory affect or primary emotional system?
Toronchuk, J. A., & Ellis, G. (2007) · Cognition & Emotion · doi:10.1080/02699930701298515 · Cited by 48
“Human neuroimaging studies show that AI is involved in coding taste sensation, olfaction, the reward value of taste (Royet, Plailly, Delon-Martin, Kareken, & Segebarth, 2003; Small et al, 2003 ; Small, Zatorre, Dagher, Evans, & Jones-Gotman, 2001 ), and participates in more comprehensive mapping of other aspects of in…”
BackgroundRudenga, K. J., & Small, D. M. (2013) · Chemical Senses · doi:10.1093/chemse/bjt029 · Cited by 52
“This is an important consideration because vmPFC response to food has been associated with internal state (Small et al. 2001).”
BackgroundSelf-citationGreen, S., Ralph, M. A. L., Moll, J., Stamatakis, E. A., Grafman, J. H., & Zahn, R. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.05.038 · Cited by 47
The Feeling of Excellent Functioning: Hedonic and Eudaimonic Emotions
Vittersø, J. (2016) · International handbooks of quality-of-life · doi:10.1007/978-3-319-42445-3_17 · Cited by 54
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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