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

Small, D. M.

doi:10.1093/brain/124.9.1720

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

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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Crossref · 10.1093/brain/124.9.1720

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Ventral striatal activity is initially high in response to palatable food but diminishes as individuals consume beyond satiety.
“Similarly, ventral striatal activity is initially high in response to palatable food but diminishes as individuals consume beyond satiety225.”
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Untitled work
Worsley (1996) · doi:10.1002/(sici)1097-0193(1996)4:1
Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys
Carmichael, S. T., & Price, J. L. (1996) · Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960722)371:2

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How do you feel — now? The anterior insula and human awareness
(Bud) Craig, A. D. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2555 · Cited by 6,657 · see citing works
An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance
Aston-Jones, G., & Cohen, J. D. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135709 · Cited by 4,472 · see citing works
Does Rejection Hurt? An fMRI Study of Social Exclusion
Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003) · Science · doi:10.1126/science.1089134 · Cited by 3,849 · see citing works
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
“…particular (Aharon et al , 2001; Anderson et al , 2003; Blood and Zatorre, 2001; Breiter et al , 1997; Elliott et al , 2000b; Knutson et al , 2000; Kunig et al , 2000; Martin-Solch et al , 2001; O’Doherty et al , 2001; Rogers et al , 1999; Rolls et al , 2003; Small et al , 2001; Thut et al , 1997).”
Background
Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion
Blood, A. J., & Zatorre, R. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191355898 · Cited by 2,814 · see citing works
A framework for studying the neurobiology of value-based decision making
Rangel, A., Camerer, C., & Montague, P. R. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2357 · Cited by 2,184 · see citing works
“Moreover, the activity in the medial OFC parallels the reduction in outcome value that one would expect after a subject is fed to satiatio”
Background
The human orbitofrontal cortex: linking reward to hedonic experience
Kringelbach, M. L. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1747 · Cited by 2,180 · see citing works
The functional neuroanatomy of the human orbitofrontal cortex: Evidence from neuroimaging and neuropsychology
KRINGELBACH, M. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.03.006 · Cited by 1,977 · see citing works
“…Verbal memory Schnider et al., 2000 PET 8 8 0 Learning of new memories Small et al., 1997 PET 10 5 5 All smell-odourless Small et al., 1999 PET – – – Review Small et al., 2001 PET 9 5 4 Chocolate “beyond” satiety Sobel et al., 1998 fMRI 12 6 6 Odour sniffing and smelling Thut et al., 1997 PET 10…”
BackgroundInfluential
Pleasure Systems in the Brain
Berridge, K. C., & Kringelbach, M. L. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.018 · Cited by 1,730 · see citing works
“…the OFC or insula would be important and possibly relevant to the orbitofrontal mid-anterior site mentioned earlier that especially tracks the subjective pleasure of foods in humans (Georgiadis et al., 2012; Kringelbach, 2005; Kringelbach et al., 2003; Small et al., 2001; Veldhuizen et al., 2010).”
Background
Liking, wanting, and the incentive-sensitization theory of addiction
Berridge, K. C., & Robinson, T. E. (2016) · American Psychologist · doi:10.1037/amp0000059 · Cited by 1,440 · see citing works
What does the retrosplenial cortex do?
Vann, S. D., Aggleton, J. P., & Maguire, E. A. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2733 · Cited by 1,409 · see citing works
Functional imaging of neural responses to expectancy and experience of monetary gains and losses
Breiter, H. C., Aharon, I., Kahneman, D., Dale, A., & Shizgal, P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00303-8 · Cited by 1,404 · see citing works
Affective neuroscience of pleasure: reward in humans and animals
Berridge, K. C., & Kringelbach, M. L. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1099-6 · Cited by 1,254 · see citing works
“…and Robbins 2005; Kringelbach 2004, 2005; Kringelbach and Berridge 2008; Kringelbach et al. 2004; Levine et al. 2003; Menon and Levitin 2005; O’Doherty et al. 2002; Pelchat et al. 2004; Rolls 2005; Schultz 2006; Small et al. 2001; Volkow et al. 2002; Wang et al. 2004; Watson et al. 2006; Figs.”
BackgroundMethod
“Liking” and “wanting” food rewards: Brain substrates and roles in eating disorders
Berridge, K. C. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.02.044 · Cited by 1,147 · see citing works
“The orbitofrontal cortex in particular has been suggested to code the pleasure of food stimuli in humans, especially along its medial edge and in a mid-anterior site that tracks changes in food pleasure during alliesthesia of hunger or satiety [28,34,35,38].”
Background
Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex
Gottfried, J. A., O'Doherty, J., & Dolan, R. J. (2003) · Science · doi:10.1126/science.1087919 · Cited by 1,165 · see citing works
The Need to Feed
Saper, C. B., Chou, T. C., & Elmquist, J. K. (2002) · Neuron · doi:10.1016/s0896-6273(02)00969-8 · Cited by 1,120 · see citing works
Disgust as a disease-avoidance mechanism.
Oaten, M., Stevenson, R. J., & Case, T. I. (2009) · Psychological Bulletin · doi:10.1037/a0014823 · Cited by 1,120 · see citing works
Mental fatigue: Costs and benefits
Boksem, M. A. S., & Tops, M. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.07.001 · Cited by 1,142 · see citing works
“People high on neuroticism have been shown to outperform their lowneurotic counterparts when a high level of effort has to be invested (Smillie et al., 2006; Tamir, 2005), possibly sacrificing immediate pleasure or well being to optimise task performance (Tamir, 2005).”
Background
Beautiful Faces Have Variable Reward Value
Aharon, I., Etcoff, N., Ariely, D., Chabris, C. F., O'Connor, E., & Breiter, H. C. (2001) · Neuron · doi:10.1016/s0896-6273(01)00491-3 · Cited by 1,087 · see citing works
The human amygdala and the emotional evaluation of sensory stimuli
Zald, D. H. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00248-5 · Cited by 1,062 · see citing works
The rewards of music listening: Response and physiological connectivity of the mesolimbic system
Menon, V., & Levitin, D. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.05.053 · Cited by 1,059 · see citing works
“The few extant studies of positive emotion have tended to use drugs of addiction to induce those positive emotions artificially (Berridge, 2003), and only recently have more naturalistic and ecologically valid studies of positive emotion been conducted (Kringelbach et al., 2003; Small et al., 2001).”
Background
The neurochemistry of music
Chanda, M. L., & Levitin, D. J. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.02.007 · Cited by 1,136 · see citing works
The dopamine motive system: implications for drug and food addiction
Volkow, N. D., Wise, R. A., & Baler, R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.130 · Cited by 939 · see citing works
Reward, Motivation, and Emotion Systems Associated With Early-Stage Intense Romantic Love
Aron, A., Fisher, H., Mashek, D. J., Strong, G., Li, H., & Brown, L. L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00838.2004 · Cited by 963 · see citing works
Positive emotion dispositions differentially associated with Big Five personality and attachment style
Shiota, M. N., Keltner, D. J., & John, O. P. (2006) · The Journal of Positive Psychology · doi:10.1080/17439760500510833 · Cited by 918 · see citing works
Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness
O’Doherty, J., Winston, J., Critchley, H., Perrett, D., Burt, D. M., & Dolan, R. J. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00145-8 · Cited by 898 · see citing works
“However, dissociable responses have been reported in these regions over time as food was eaten to satiety in a meal in which the food changed from being pleasant to aversive [52].”
Background
The tempted brain eats: Pleasure and desire circuits in obesity and eating disorders
Berridge, K. C., Ho, C.-Y., Richard, J. M., & DiFeliceantonio, A. G. (2010) · Brain Research · doi:10.1016/j.brainres.2010.04.003 · Cited by 873 · see citing works
“…the anterior cingulate cortex and the anterior insula cortex (de Araujo et al., 2003; Kringelbach, 2004; Kringelbach, 2005; Kringelbach, 2010; O'Doherty et al., 2001; Petrovich and Gallagher, 2007; Rolls, 2006; Rolls et al., 2003; Small and Veldhuizen, 2010; Small et al., 2001; Small et al., 2003).”
Influential
Widespread reward-system activation in obese women in response to pictures of high-calorie foods
Stoeckel, L. E., Weller, R. E., Cook, E. W., Twieg, D. B., Knowlton, R. C., & Cox, J. E. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.02.031 · Cited by 857 · see citing works
“…et al., 2003; Killgore and Yurgelun-Todd, 2005; Kinomura et al., 1994; Kringelbach at al., 2003; LaBar et al., 2001; O'Doherty et al., 2002; Porubska et al., 2006; Rothemund et al., 2007; Simmons et al., 2005; Small et al., 1999, 2001; St-Onge et al., 2005; Uher et al., 2006; Wang et al., 2004a).”
The cingulate cortex and limbic systems for emotion, action, and memory
Rolls, E. T. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01945-2 · Cited by 859 · see citing works
Sensory expectations based on product-extrinsic food cues: An interdisciplinary review of the empirical evidence and theoretical accounts
Piqueras-Fiszman, B., & Spence, C. (2015) · Food Quality and Preference · doi:10.1016/j.foodqual.2014.09.013 · Cited by 855 · see citing works
New insights into symptoms and neurocircuit function of anorexia nervosa
Kaye, W. H., Fudge, J. L., & Paulus, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2682 · Cited by 843 · see citing works
“Indeed, brain imaging studies have consistently shown that food deprivation (compared to having been fed) in healthy individuals activates the insula and the oFC 117,127–130 .”
Activation of the Human Orbitofrontal Cortex to a Liquid Food Stimulus is Correlated with its Subjective Pleasantness
Kringelbach, M. L. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.10.1064 · Cited by 824 · see citing works
Processing of primary and secondary rewards: A quantitative meta-analysis and review of human functional neuroimaging studies
Sescousse, G., Caldú, X., Segura, B., & Dreher, J.-C. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.002 · Cited by 782 · see citing works
“For instance, vmPFC activity decreases with satiety (O’Doherty et al., 2000; Small et al., 2001) and increases with personal preferences based on brand or price (Plassmann et al.”
The orbitofrontal cortex and beyond: From affect to decision-making
Rolls, E. T., & Fabian Grabenhorst, B. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.09.001 · Cited by 808 · see citing works
“…et al., 2003c, 2005; Francis et al., 1999; Gottfried et al., 2006; McCabe and Rolls, 2007; O'Doherty et al., 2000; Rolls et al., 2003a; Rolls and McCabe, 2007; Small et al., 2001, 2005), and that the activations correlate with ratings of pleasantness (Kringelbach and Rolls, 2004; Rolls, 2005).”
Background
Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation
Small, D. M., Gregory, M. D., Mak, Y. E., Gitelman, D. R., Mesulam, M. M., & Parrish, T. B. (2003) · Neuron · doi:10.1016/s0896-6273(03)00467-7 · Cited by 789 · see citing works
Self-citation
Relation Between Obesity and Blunted Striatal Response to Food Is Moderated by <i>Taq</i> IA A1 Allele
Stice, E., Spoor, S., Bohon, C., & Small, D. M. (2008) · Science · doi:10.1126/science.1161550 · Cited by 786 · see citing works
Self-citation
Relation of reward from food intake and anticipated food intake to obesity: A functional magnetic resonance imaging study.
Stice, E., Spoor, S., Bohon, C., Veldhuizen, M. G., & Small, D. M. (2008) · Journal of Abnormal Psychology · doi:10.1037/a0013600 · Cited by 779 · see citing works
“Third, activation in regions representing anticipatory and consummatory food reward (LaBar et al., 2001; O’Doherty et al., 2002; Small et al., 2001) in response to anticipation and receipt of milkshake in this fMRI paradigm correlated (r .”
Self-citation
A common neurobiology for pain and pleasure
Leknes, S., & Tracey, I. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2333 · Cited by 784 · see citing works
Odor/taste integration and the perception of flavor
Small, D. M., & Prescott, J. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-2376-9 · Cited by 712 · see citing works
“…1999; O’Doherty et al. 2000; Savic et al. 2000; O’Doherty et al. 2001; Poellinger et al. 2001), and the anterior cingulate cortex (Zald and Pardo 1997; Zald et al. 1998; O’Doherty et al. 2000; Savic et al. 2000; Small et al. 2001; de Araujo et al. 2003; Royet et al. 2003; Small et al. 2003) (Fig.”
BackgroundSelf-citation
Neural correlates of food addiction
Gearhardt, A. N. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.32 · Cited by 707 · see citing works
“We performed small volume correction analyses using peaks with the highest volumes (millimeters cubed) and z values identified previously in the cue-induced craving and drug administration literature(9,34,35) as well as in food cue/food administration studies.(15,36,37) To test our hypothesis that participants exhibit…”
Ghrelin Modulates Brain Activity in Areas that Control Appetitive Behavior
Malik, S., McGlone, F., Bedrossian, D., & Dagher, A. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.03.007 · Cited by 677 · see citing works
Images of desire: food-craving activation during fMRI
Pelchat, M. L., Johnson, A., Chan, R., Valdez, J., & Ragland, J. D. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.08.023 · Cited by 667 · see citing works
“…cortex (O'Doherty et al., 2000; Small et al., 2001; Wang et al., 2004), amygdala (LaBar et al., 2001), parahippocampal gyrus (LaBar et al., 2001; Small et al., 2001), anterior fusiform gyrus (LaBar et al., 2001), insula (Gordon et al., 2000; Small et al., 2001; Wang et al., 2004), striatum…”
Influential
Neural Correlates of Beauty
Kawabata, H., & Zeki, S. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00696.2003 · Cited by 880 · see citing works
Taste‐olfactory convergence, and the representation of the pleasantness of flavour, in the human brain
De Araujo, I. E. T., Rolls, E. T., Kringelbach, M. L., McGlone, F., & Phillips, N. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02915.x · Cited by 642 · see citing works
Neurobiology of anorexia and bulimia nervosa
Kaye, W. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.037 · Cited by 625 · see citing works
Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers
Small, D. M., Jones-Gotman, M., & Dagher, A. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00253-2 · Cited by 632 · see citing works
“…striatum in feeding, our current findings are also consistent with our previous human PET study, where we reported that regional cerebral blood flow measured while eating chocolate correlated with pleasantness ratings in the dorsal caudate and putamen, but not in the NAc (Small et al., 2001).”
ResultSelf-citation
Adaptive gain and the role of the locus coeruleus–norepinephrine system in optimal performance
Aston‐Jones, G., & Cohen, J. D. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20723 · Cited by 630 · see citing works
Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices
O'Doherty, J., Critchley, H., Deichmann, R., & Dolan, R. J. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07931.2003 · Cited by 611 · see citing works
“Other studies have also found medial–lateral dissociations for rewarding versus punishing stimuli (Small et al., 2001; Gottfried et al., 2002; O’Doherty et al., 2003).”
Result
The sentient self
Craig, A. D. (. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0248-y · Cited by 600 · see citing works
Carbohydrate sensing in the human mouth: effects on exercise performance and brain activity
Chambers, E. S., Bridge, M., & Jones, D. A. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.164285 · Cited by 598 · see citing works
“…oral carbohydrate stimulus during subsequent exercise as it is likely that the activation of brain regions associated with feeding and reward, such as the orbitofrontal cortex and striatum, are modulated by homeostatic regulation and the current physiological state of the body (Small et al. 2001).”
BackgroundInfluential
Branding the brain: A critical review and outlook
Plaßmann, H., Ramsøy, T. Z., & Milosavljevic, M. (2012) · Journal of Consumer Psychology · doi:10.1016/j.jcps.2011.11.010 · Cited by 628 · see citing works
Individual Differences in Reward Drive Predict Neural Responses to Images of Food
Beaver, J. D., Lawrence, A. D., van Ditzhuijzen, J., Davis, M. H., Woods, A., & Calder, A. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0350-06.2006 · Cited by 594 · see citing works
“Similarly, human functional imaging investigations have used hunger/satiety manipulations to demonstrate that motivational state can influence reward-related activations in homologous areas (LaBar et al., 2001; Morris and Dolan, 2001; Small et al., 2001; Gottfried et al., 2003; Hinton et al., 2004; Wang et al., 2004).”
Background
Anatomy of a decision: Striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal.
Frank, M. J., & Claus, E. D. (2006) · Psychological Review · doi:10.1037/0033-295x.113.2.300 · Cited by 578 · see citing works
“In one of these studies, medial OFC activity was observed when participants began eating chocolate, but as a sated state was reached, the lateral OFC became more active (Small et al., 2001).”
Background
Disclosing information about the self is intrinsically rewarding
Tamir, D. I., & Mitchell, J. P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202129109 · Cited by 563 · see citing works
Risky business: the neuroeconomics of decision making under uncertainty
Platt, M. L., & Huettel, S. A. (2008) · Nature Neuroscience · doi:10.1038/nn2062 · Cited by 556 · see citing works
Brain Organization for Music Processing
Peretz, I., & Zatorre, R. J. (2005) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070225 · Cited by 863 · see citing works
Evolution and Cognition
Kamil, A. C. (2001) · Evolution and Human Behavior · doi:10.1016/s1090-5138(01)00068-x · Cited by 548 · see citing works
Facial expressions, their communicatory functions and neuro–cognitive substrates
Blair, J. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1220 · Cited by 537 · see citing works
“Experimental investigations in macaques have shown that there is a primary taste cortical region in the anterior insula (Rolls 1997) and neuro-imaging studies in humans have also shown the insula to be involved in the representation of taste (O'Doherty et al. 2001b; Small et al. 2001).”
Background
Body mass correlates inversely with inhibitory control in response to food among adolescent girls: An fMRI study
Batterink, L. J., Yokum, S., & Stice, E. M. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.05.059 · Cited by 527 · see citing works
Towards a functional neuroanatomy of pleasure and happiness
Kringelbach, M. L., & Berridge, K. C. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.08.006 · Cited by 528 · see citing works
Brain abnormalities in human obesity: A voxel-based morphometric study
Pannacciulli, N., Del Parigi, A., Chen, K., Le, D. S. N. T., Reiman, E. M., & Tataranni, P. A. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.01.047 · Cited by 523 · see citing works
Biomarkers of satiation and satiety
de Graaf, C., Blom, W. A. M., Smeets, P. A. M., Stafleu, A., & Hendriks, H. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/79.6.946 · Cited by 523 · see citing works
“A PET study on brain activity changes in subjects who had eaten chocolate beyond satiety showed that the medial orbitofrontal cortex was activated when the chocolate was liked, whereas the lateral orbitofrontal cortex was activated when the consumption of chocolate became aversive (42).”
Background
The neurobiology of positive emotions
Burgdorf, J., & Panksepp, J. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.001 · Cited by 677 · see citing works
From emotion perception to emotion experience: Emotions evoked by pictures and classical music
Baumgärtner, T., Esslen, M., & Jäncke, L. (2005) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.04.007 · Cited by 517 · see citing works
“These brain structures are known to be active in response to other euphoria-inducing stimuli, such as food, sex, and drugs of abuse (e.g. Small et al., 2001).”
Background
Learning, reward, and decision making
O'Doherty, J. P., Cockburn, J., & Pauli, W. M. (2017) · Annual Review of Psychology · doi:10.1146/annurev-psych-010416-044216 · Cited by 475 · see citing works
Stress as a Common Risk Factor for Obesity and Addiction
Sinha, R., & Jastreboff, A. M. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.032 · Cited by 611 · see citing works
PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans
Batterham, R. L., Ffytche, D. H., Rosenthal, J., Zelaya, F. O., Barker, G. J., Withers, D. J., & Williams, S. (2007) · Nature · doi:10.1038/nature06212 · Cited by 474 · see citing works
Compulsive overeating as an addiction disorder. A review of theory and evidence
Davis, C. A., & Carter, J. C. (2009) · Appetite · doi:10.1016/j.appet.2009.05.018 · Cited by 479 · see citing works
Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging
Gottfried, J. A., O’Doherty, J. P., & Dolan, R. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10829.2002 · Cited by 474 · see citing works
“Recent neuroimaging studies indicate that the neural substrates of reward and punishment may be functionally compartmentalized within medial and lateral OFC, respectively (O’Doherty et al., 2001, 2003; Small et al., 2001).”
Background
Heart rate variability reflects self-regulatory strength, effort, and fatigue
Segerstrom, S. C., & Nes, L. S. (2007) · Psychological Science · doi:10.1111/j.1467-9280.2007.01888.x · Cited by 606 · see citing works
“Selfregulatory tasks are associated with activation of prefrontal cortex, and self-regulatory fatigue adversely and selectively affects performance on cognitive tasks that are considered to be frontal or executive (Schmeichel, Vohs, & Baumeister, 2003; Small, Zatorre, Dagher, Evans, & Jones-Gotman, 2001 ).”
Background
Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans
Small, D. M., Gerber, J. C., Mak, Y. E., & Hummel, T. (2005) · Neuron · doi:10.1016/j.neuron.2005.07.022 · Cited by 463 · see citing works
“Support for a role for these regions in encoding the receipt of food reward and food liking comes from Small and colleagues, who demonstrated a very strong correlation between decreases in the pleasantness of chocolate as it is eaten beyond satiety and decreases in activity in a region that encompassed the perigenual…”
InfluentialSelf-citation
Food and drug cues activate similar brain regions: A meta-analysis of functional MRI studies
Tang, D., Fellows, L. K., Small, D. M., & Dagher, A. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.03.009 · Cited by 457 · see citing works
“The insula is also implicated in the devaluation of food cues when eating to satiety [64,69].”
BackgroundSelf-citation
Is Avoiding an Aversive Outcome Rewarding? Neural Substrates of Avoidance Learning in the Human Brain
Kim, H., Shinsuke Shimojo, A., & O’Doherty, J. P. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040233 · Cited by 447 · see citing works
Binge-Eating Disorder: Reward Sensitivity and Brain Activation to Images of Food
Schienle, A., Schäfer, A., Hermann, A., & Vaitl, D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.09.028 · Cited by 447 · see citing works
Processing emotional pictures and words: Effects of valence and arousal
KENSINGER, E. A., & SCHACTER, D. L. (2006) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.6.2.110 · Cited by 442 · see citing works
“The results were generally consistent with those in prior studies demonstrating that lateral PFC regions respond to aversive stimuli, whereas medial PFC regions respond to positive stimuli (e.g., O’Doherty et al., 2001; Small et al., 2001).”
Result
Hedonic Hot Spots in the Brain
Peciña, S., Smith, K. S., & Berridge, K. C. (2006) · The Neuroscientist · doi:10.1177/1073858406293154 · Cited by 441 · see citing works
A functional MRI study of happy and sad affective states induced by classical music
Mitterschiffthaler, M. T., Fu, C. H. Y., Dalton, J. A., Andrew, C. M., & Williams, S. (2007) · Human Brain Mapping · doi:10.1002/hbm.20337 · Cited by 445 · see citing works
“…structures has also been observed during mating/copulation in rodents [Pfaus et al., 1995], in humans in association with stimulants such as food [Small et al., 2001], recreational drugs [Breiter et al., 1997] and while viewing pleasant pictures or facial images [Aharon et al., 2001; Lane et…”
Background
Neuroimaging and neuromodulation approaches to study eating behavior and prevent and treat eating disorders and obesity
Val‐Laillet, D., Aarts, E., Weber, B., Ferrari, M., Quaresima, V., Stoeckel, L. E., Alonso‐Alonso, M., Audette, M. A., Malbert, C., & Stice, E. M. (2015) · NeuroImage Clinical · doi:10.1016/j.nicl.2015.03.016 · Cited by 443 · see citing works
“…implicated in reward in both humans and other animals, including the ventral and dorsal striatum, midbrain, amygdala, and orbitofrontal cortex (OFC: Small et al., 2001; Avena et al., 2006; Berridge, 2009; Stice et al., 2013) and causes dopamine (DA) release in the dorsal striatum, with the amount…”
The effect of carbohydrate mouth rinse on 1-h cycle time trial performance
CARTER, J. M., JEUKENDRUP, A. E., & JONES, D. A. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000147585.65709.6f · Cited by 437 · see citing works
Opponent appetitive-aversive neural processes underlie predictive learning of pain relief
Seymour, B., O'Doherty, J. P., Koltzenburg, M., Wiech, K., Frackowiak, R., Friston, K., & Dolan, R. (2005) · Nature Neuroscience · doi:10.1038/nn1527 · Cited by 439 · see citing works
GLP-1 Receptor Activation Modulates Appetite- and Reward-Related Brain Areas in Humans
van Bloemendaal, L., IJzerman, R. G., ten Kulve, J. S., Barkhof, F., Konrad, R. J., Drent, M. L., Veltman, D. J., & Diamant, M. (2014) · Diabetes · doi:10.2337/db14-0849 · Cited by 427 · see citing works
“The insula is involved in the processing of food-cues and craving for food (31) and has been implicated in the devaluation of food-cues when eating to satiety (32).”
BackgroundInfluential
Limbic systems for emotion and for memory, but no single limbic system
Rolls, E. T. (2013) · Cortex · doi:10.1016/j.cortex.2013.12.005 · Cited by 428 · see citing works
A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats
Capriles, N., Rodaros, D., Sorge, R. E., & Stewart, J. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1283-z · Cited by 414 · see citing works
“The OFC, however, is known to be involved in the appetitive and aversive motivational control of goal-directed behavior (O’Doherty et al. 2001; Small et al. 2001 ), modulating decisions about expected outcomes (Bechara et al. 2000; Hollerman et al. 2000).”
Background
Adolescents' Performance on the Iowa Gambling Task: Implications for the Development of Decision Making and Ventromedial Prefrontal Cortex.
Hooper, C. J., Luciana, M., Conklin, H. M., & Yarger, R. S. (2004) · Developmental Psychology · doi:10.1037/0012-1649.40.6.1148 · Cited by 412 · see citing works
Neural representations of subjective reward value
Peters, J., & Büchel, C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.04.031 · Cited by 405 · see citing works
The Orbitofrontal Oracle: Cortical Mechanisms for the Prediction and Evaluation of Specific Behavioral Outcomes
Rudebeck, P. H., & Murray, E. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.049 · Cited by 405 · see citing works
Weight Gain Is Associated with Reduced Striatal Response to Palatable Food
Stice, E., Yokum, S., Blum, K., & Bohon, C. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2105-10.2010 · Cited by 401 · see citing works
“The dorsal striatum responds to ingestion of chocolate in lean humans and is sensitive to its devaluation by feeding beyond satiety (Small et al., 2001).”
The human sexual response cycle: Brain imaging evidence linking sex to other pleasures
Georgiadis, J. R., & Kringelbach, M. L. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.05.004 · Cited by 399 · see citing works
“…mid-anterior subregion of the OFC is interesting, since previous research has shown that activity correlates with the subjective pleasure of different rewards, e.g. food (Kringelbach et al., 2003), drugs (Vollm et al., 2004), chocolate (Small et al., 2001), and even music (Blood and Zatorre, 2001).”
BackgroundInfluential
Experience-dependent neural integration of taste and smell in the human brain
Small, D. M., Voss, J., Mak, Y. E., Simmons, K. B., Parrish, T., & Gitelman, D. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00050.2004 · Cited by 398 · see citing works
Self-citation
Olfactory disorders and their consequences for quality of life
Hummel, T. R., & Nordin, S. (2004) · Acta Oto-Laryngologica · doi:10.1080/00016480410022787 · Cited by 398 · see citing works
“Examples of the ability of olfaction to generate strong associations include food aversions and nausea induced by an odor [22,23].”
Background
Attentional Bias to Food Images Associated With Elevated Weight and Future Weight Gain: An fMRI Study
Yokum, S., Ng, J., & Stice, E. M. (2011) · Obesity · doi:10.1038/oby.2011.168 · Cited by 396 · see citing works
Contextual modulation of amygdala responsivity to surprised faces
Kim, H., Somerville, L. H., Johnstone, T., Polis, S., Alexander, A. L., Shin, L. M., & Whalen, P. J. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042947865 · Cited by 389 · see citing works
Common cellular and molecular mechanisms in obesity and drug addiction
Kenny, P. J. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3105 · Cited by 382 · see citing works
Modulation of aesthetic value by semantic context: An fMRI study
Kirk, U., Skov, M., Hulme, O., Christensen, M. S., & Zeki, S. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.009 · Cited by 381 · see citing works
“…suggests that this region represents attributed hedonic values from a variety of sensory modalities, including gustatory (O'Doherty et al., 2001a; Small et al., 2001, 2003), olfactory (Anderson et al., 2003; Gottfried et al., 2002; Rolls et al., 2003a), somatosensory (Rolls et al., 2003b),…”
Hunger is the best spice: An fMRI study of the effects of attention, hunger and calorie content on food reward processing in the amygdala and orbitofrontal cortex
Siep, N., Roefs, A., Roebroeck, A., Havermans, R., Bonte, M. L., & Jansen, A. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.10.035 · Cited by 375 · see citing works
The nature of music from a biological perspective
Peretz, I. (2006) · Cognition · doi:10.1016/j.cognition.2005.11.004 · Cited by 384 · see citing works
Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways
Page, K. A., Chan, O., Arora, J., Belfort-DeAguiar, R., Dzuira, J., Roehmholdt, B., Cline, G. W., Naik, S., Sinha, R., Constable, R. T., et al. (2013) · JAMA · doi:10.1001/jama.2012.116975 · Cited by 379 · see citing works
“tivation occur when initially hungry individuals reach satiety.(23,26) Of note, fructose ingestion reduced CBF in the hippocampus.”
Background
Naturalizing aesthetics: Brain areas for aesthetic appraisal across sensory modalities
Brown, S., Gao, X., Tisdelle, L., Eickhoff, S. B., & Liotti, M. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.06.012 · Cited by 376 · see citing works
“For example, Small et al. (2001) had subjects eat chocolate to beyond satiety.”
Liking vs. wanting food: Importance for human appetite control and weight regulation
Finlayson, G., King, N. A., & Blundell, J. E. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.03.004 · Cited by 376 · see citing works
“One neuroimaging study (Small et al. 2001) used consecutive PET scans to track changes in brain activity as subjects consumed chocolate to beyond satiety.”
BackgroundMethodInfluential
Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants
Nitschke, J. B., Nelson, E. E., Rusch, B. D., Fox, A. S., Oakes, T. R., & Davidson, R. J. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.10.005 · Cited by 371 · see citing works
“…with humans have activated different sectors of the OFC using taste (Berns et al., 2001; McClure et al., 2003; O'Doherty et al., 2001b, 2002, 2003a; Small et al., 2001), smell (Anderson et al., 2003; O'Doherty et al., 2000), money (Breiter et al., 2001; Elliott et al., 2000, 2003; Knutson et al.,…”

Please, no more!
Russell, T. A. (2001) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01811-8
Enhanced 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 · see citing works
Spatiotemporal dynamics of the hedonic processing of chocolate images in individuals with and without trait chocolate craving
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 51 · see citing works
Differential Orbitofrontal Cortex Responses to Chocolate Images While Performing an Approach–Avoidance Task in the MRI Environment
Lender, A., Wirtz, J., Kronbichler, M., Kahveci, S., Kühn, S., & Jens Blechert, A. (2023) · Nutrients · doi:10.3390/nu15010244 · Cited by 8 · see citing works
An fMRI study of the effect of satiation on reward and aversion
Thomas, J. M., Hansen, P., Harmer, C. J., Dourish, C. T., Higgs, S., & McCabe, C. (2012) · Appetite · doi:10.1016/j.appet.2012.05.102

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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