Cited by 1,179Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesRegulation of Appetite and Obesity

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Changes in brain activity related to eating chocolate: From pleasure to aversion

Small, D. M.·2001·Brain

DOI 10.1093/brain/124.9.1720

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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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BackgroundMethodInfluential
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Murray, E. A., & Rudebeck, P. H. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00112 · Cited by 38
“A number of investigations have started to uncover the neural substrates of satiety and devaluation effects in humans (O’Doherty et al., 2000; Small et al., 2001; Gottfried et al., 2003; Kringelbach et al., 2003).”
Background
FTO gene variant modulates the neural correlates of visual food perception
Kühn, A. B., Feis, D., Schilbach, L., Kracht, L., Hess, M. E., Mauer, J., Brüning, J. C., & Tittgemeyer, M. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2015.12.049 · Cited by 38
“In addition, increased neural responses of middle and inferior frontal areas were associated to hedonic eating (Small et al., 2001).”
Background
Emotional eating and Pavlovian learning: evidence for conditioned appetitive responding to negative emotional states
Bongers, P., & Jansen, A. T. M. (2015) · Cognition & Emotion · doi:10.1080/02699931.2015.1108903 · Cited by 38
Neural Correlates of the Perception of Spoiled Food Stimuli
Becker, C. A., Flaisch, T., Renner, B., & Schupp, H. T. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00302 · Cited by 44
Why Symbolic Processing of Affect Can Disrupt Negative Affect
Lieberman, M. D. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195316872.003.0013 · Cited by 39
Implications from addiction research towards the understanding and treatment of obesity
Grosshans, M., Loeber, S., & Kiefer, F. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2010.00300.x · Cited by 38
EVOLUTIONARY MISMATCH, NEURAL REWARD CIRCUITS, AND PATHOLOGICAL GAMBLING
Spinella, M. (2003) · International Journal of Neuroscience · doi:10.1080/00207450390162254 · Cited by 38
“Similar activations occur in these structures with many other forms of pleasurable activity, including drug-induced euphoria, listening to enjoyable music, and eating appetizing food (Kilts et al., 2001; Blood & Zatorre, 2001; Small et al., 2001).”
Background
Forebrain circuits and control of feeding by learned cues
Petrovich, G. D. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.10.003 · Cited by 37
From Perception to Pleasure
Zatorre, R. J. (2023) · doi:10.1093/oso/9780197558287.001.0001 · Cited by 43
Chocolate craving among children: Implications for disordered eating patterns
Cartwright, F., Stritzke, W. G. K., Durkin, K., Houghton, S. J., Burke, V., & Beilin, L. J. (2006) · Appetite · doi:10.1016/j.appet.2006.07.081 · Cited by 37
The Craving Stops Before You Feel It: Neural Correlates of Chocolate Craving During Cue Exposure with Response Prevention
Frankort, A., Roefs, A., Siep, N., Roebroeck, A. F., Havermans, R. C., & Jansen, A. T. M. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht016 · Cited by 37
Activity of frontal pole cortex reflecting hedonic tone of food and drink: fNIRS study in humans
Minematsu, Y., Ueji, K., & Yamamoto, T. (2018) · Scientific Reports · doi:10.1038/s41598-018-34690-3 · Cited by 39
Multistage Valuation Signals and Common Neural Currencies
Platt, M. L., & Plaßmann, H. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-416008-8.00013-9 · Cited by 38
Neuroimaging and Sexual Behavior: Identification of Regional and Functional Differences
Cheng, J., Secondary, J., Burke, W. H., Fedoroff, J. P., & Dwyer, R. G. (2015) · Current Psychiatry Reports · doi:10.1007/s11920-015-0593-x · Cited by 38
Rebuilding reality: A phenomenology of aspects of chronic schizophrenia
SCHWARTZ, M. A., Wiggins, O. P., Naudin, J., & Spitzer, M. (2005) · Phenomenology and the Cognitive Sciences · doi:10.1007/s11097-005-4738-y · Cited by 37
“More recent investigations demonstrate that the same system is activated in normal human beings after eating chocolate ( Small et al. 2001 ), hearing nice music (Blood and Zatorre 2001), winning ag ame (Koepp et al. 1998), and even looking at an attractive face (Aharon et al. 2001).”
Background
Sensory-specific satiety: Added insights from autonomic nervous system responses and facial expressions
He, W., Boesveldt, S., Delplanque, S., de Graaf, C., & de Wijk, R. A. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.12.012 · Cited by 36
Effects of distraction on taste-related neural processing: a cross-sectional fMRI study
Duif, I., Wegman, J., Mars, M., de Graaf, C., Smeets, P. A. M., & Aarts, E. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa032 · Cited by 36
Limbic responses to reward cues correlate with antisocial trait density in heavy drinkers
Oberlin, B. G., Dzemidzic, M., Bragulat, V., Lehigh, C. A., Talavage, T., O'Connor, S. J., & Kareken, D. A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.043 · Cited by 35
“This idea is supported by human PET studies showing dopamine release in dorsal, but not ventral striatum in response to feeding (Small et al., 2001, 2003).”
Tasting calories differentially affects brain activation during hunger and satiety
van Rijn, I., de Graaf, C., & Smeets, P. A. M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.11.019 · Cited by 37
The Neural Correlates of Desire
Kawabata, H., & Zeki, S. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003027 · Cited by 35
“, [6,7]), beauty [27], and love [37,38].”
Physical exercise and brain responses to images of high-calorie food
Killgore, W. D. S., Kipman, M., Schwab, Z. J., Tkachenko, O. N., Preer, L. A., Gogel, H., Bark, J. S., Mundy, E. A., Olson, E. A., & Weber, M. (2013) · Neuroreport · doi:10.1097/wnr.0000000000000029 · Cited by 34
Structure–function relationships in the processing of regret in the orbitofrontal cortex
Sommer, T., Peters, J., Gläscher, J. P., & Büchel, C. (2009) · Brain Structure and Function · doi:10.1007/s00429-009-0222-8 · Cited by 35
“In one elegant study, the valuation of a primary reinforcer (chocolate) changed due to feeding to satiety which was accompanied by decreasing activity in medial and increasing activity in lateral OFC (Small et al. 2001).”
Background
Review
Stamatakis, E. A., & Hetherington, M. M. (2003) · Nutritional Neuroscience · doi:10.1080/10284150310001640338 · Cited by 34
“Motivational features of brain activity in relation to food intake were investigated by Small et al. (2001) who scanned nine subjects using PET after eating squares of chocolate to satiety.”
Background
Activation of the mesostriatal reward pathway with exposure to ultraviolet radiation (UVR) vs. sham UVR in frequent tanners: a pilot study
Harrington, C. R., Beswick, T. C., Graves, M., Jacobe, H. T., Harris, T. S., Kourosh, S., Devous Sr, M. D., & Adinoff, B. (2012) · Addiction Biology · doi:10.1111/j.1369-1600.2010.00312.x · Cited by 81
“…the evaluative, experiential or expressive aspects of internally generated emotions (Reiman et al. 1997; Craig 2003) and anterior/middle insular activation has been observed during the ingestion of chocolate in ‘chocolate lovers’ (Small et al. 2001) and cocaine administration (Kufahl et al. 2005).”
Background
The sensory valuation account of aesthetic experience
Nadal, M., & Skov, M. (2024) · Nature Reviews Psychology · doi:10.1038/s44159-024-00385-y · Cited by 42
“As people eat or drink to satiation, they find food and drinks increasingly less pleasurable and activity in their nucleus accumbens, insula and orbitofrontal cortex decreases 149,150,172 .”
Regulation of Energy Balance and Body Weight by the Brain: A Distributed System Prone to Disruption
Faulconbridge, L. F., & Hayes, M. R. (2011) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2011.08.008 · Cited by 34
Altered neural inhibition responses to food cues after Roux-en-Y Gastric Bypass
Zoon, H. F. A., de Bruijn, S. E. M., Jager, G., Smeets, P. A. M., de Graaf, C., Janssen, I. M. C., Schijns, W., Deden, L. N., & Boesveldt, S. (2018) · Biological Psychology · doi:10.1016/j.biopsycho.2018.06.005 · Cited by 33
“Increased activation in the parahippocampal gyrus during exposure to taste and smell of food was associated with decreasing reward value in healthy (Small et al., 2001) and obese subjects (Bragulat et al., 2010).”
Orbitofrontal cortex: a ‘non-rewarding’ new treatment target in depression?
Downar, J. (2019) · Current Biology · doi:10.1016/j.cub.2018.11.057 · Cited by 31
Multiple Systems for the Motivational Control of Behavior and Associated Neural Substrates in Humans
O’Doherty, J. P. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_386 · Cited by 33
Can age-related CNS taste differences be detected as early as middle age? Evidence from fMRI
Green, E., Jacobson, A., Haase, L., & Murphy, C. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.027 · Cited by 32
Consumption of a highly palatable food induces a lasting place-conditioning memory in marmoset monkeys
Duarte, R. B., Patrono, E., Borges, A. C., César, A., Tomaz, C. A. B., Ventura, R., Gasbarri, A., Puglisi‐Allegra, S., & Barros, M. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.08.021 · Cited by 32
Food-Evoked Changes in Humans
Walla, P., Richter, M., Farber, S., Leodolter, U., & Bauer, H. (2010) · Journal of Psychophysiology · doi:10.1027/0269-8803/a000003 · Cited by 32
Thermal taster status: Evidence of cross-modal integration
Hort, J., Ford, R. A., Eldeghaidy, S., & Francis, S. (2016) · Human Brain Mapping · doi:10.1002/hbm.23171 · Cited by 32
“Previous studies have reported DLFPC activation to food-related studies [Small et al., 2001; Tataranni et al., 1999], and Kringelbach et al. [2004] showed DLFPC activation to unimodal taste and multimodal flavour stimuli in the human brain.”
Background
From Thirst to Satiety: The Anterior Mid-Cingulate Cortex and Right Posterior Insula Indicate Dynamic Changes in Incentive Value
Becker, C. A., Flaisch, T., Renner, B., & Schupp, H. T. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00234 · Cited by 35
“Similarly, a further study investigated changes in brain activity related to eating chocolate to satiety, tracking the hedonic experience of chocolate from being highly pleasurable to being highly aversive (Small et al., 2001).”
Background
Deep brain stimulation of the orbitofrontal cortex prevents the development and reinstatement of morphine place preference
Fakhrieh‐Asl, G., Sadr, S. S., Karimian, S. M., & Riahi, E. (2019) · Addiction Biology · doi:10.1111/adb.12780 · Cited by 30
“Electrode‐implanted rats were examined postmortem for precise electrode placement in the OFC.”
BackgroundInfluential
Food Addiction and Tobacco Use Disorder: Common Liability and Shared Mechanisms
Zawertailo, L. A., Attwells, S., deRuiter, W. K., Le, T. L., Dawson, D., & Selby, P. L. (2020) · Nutrients · doi:10.3390/nu12123834 · Cited by 37
“PET studies demonstrated a positive association of food cravings and increased dorsal caudate and putamen regional cerebral blood flow [53], as well as an association of DA ligand binding within the dorsal striatum and feeding [54].”
Background

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
DOI: 10.1093/brain/124.9.1720
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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Changes in brain activity related to eating chocolate: From pleasure to aversion

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