Food‐Related Odor Probes of Brain Reward Circuits During Hunger: A Pilot fMRI Study
Open accessAbstract
Food aromas can be powerful appetitive cues in the natural environment. Although several studies have examined the cerebral responses to food images, none have used naturalistic food aromas to study obesity. Ten individuals (five normal‐weight and five obese) were recruited to undergo 24 h of food deprivation. Subjects were then imaged on a 3T Siemens Trio‐Tim scanner (Siemens, Erlangen, Germany) while smelling four food‐related odors (FRO; two sweet odors and two fat‐related) and four “nonappetitive odors” (NApO; e.g., Douglas fir). Before the imaging session, subjects rated their desire to eat each type of food to determine their most preferred (P‐FRO). Across all 10 subjects, P‐FRO elicited a greater blood oxygenation level dependent (BOLD) response than the NApO in limbic and reward‐related areas, including the bilateral insula and opercular (gustatory) cortex, the anterior and posterior cingulate, and ventral striatum. Obese subjects showed greater activation in the bilateral hippocampus/parahippocampal gyrus, but lean controls showed more activation in the posterior insula. Brain areas activated by food odors are similar to those elicited by cues of addictive substances, such as alcohol. Food odors are highly naturalistic stimuli, and may be effective probes of reward‐related networks in the context of hunger and obesity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Responses to food cues depend on nutrition status, highlighting the role of the homeostatic network in controlling the reward network, which is also influenced by stress-processing pathways.
“The dependence of the responses to food cues on the nutrition status (60,61) highlights the role of the homeostatic network in the control of the reward network, which in turn is also influenced by neuronal pathways that process stress.”
From Obesity and addiction: Neurobiological overlaps (2013) · cites this paper as [60]
Cites
Overweight and obesity in the United States: prevalence and trends, 1960–1994
Flegal, K., Carroll, M., Kuczmarski, R., & Johnson, C. (1998) · International Journal of Obesity · doi:10.1038/sj.ijo.0800541 · Cited by 3,045 · see citing works
The debate over dopamine’s role in reward: the case for incentive salience
Berridge, K. C. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0578-x · Cited by 2,347 · see citing works
Environmental Contributions to the Obesity Epidemic
Hill, J. O., & Peters, J. C. (1998) · Science · doi:10.1126/science.280.5368.1371 · Cited by 2,206 · see citing works
Self-Control in Decision-Making Involves Modulation of the vmPFC Valuation System
Hare, T. A., Camerer, C. F., & Rangel, A. (2009) · Science · doi:10.1126/science.1168450 · Cited by 1,928 · see citing works
The neural correlates of subjective value during intertemporal choice
Kable, J. W., & Glimcher, P. W. (2007) · Nature Neuroscience · doi:10.1038/nn2007 · Cited by 1,916 · see citing works
Damage to the insula disrupts addiction to cigarette smoking
Naqvi, N. H., Rudrauf, D., Damasio, H., & Bechara, A. (2007) · Science · doi:10.1126/science.1135926 · Cited by 1,245 · see citing works
Architectonic subdivision of the human orbital and medial prefrontal cortex
Öngür, D., Ferry, A. T., & Price, J. L. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10609 · Cited by 944 · see citing works
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
Hare, T. A., O'Doherty, J., Camerer, C. F., Schultz, W., & Rangel, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1309-08.2008 · Cited by 792 · see citing works
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
Haber, S. N., Kim, K.-S., Mailly, P., & Calzavara, R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0271-06.2006 · Cited by 686 · see citing works
Rothemund, Y., Preuschhof, C., Bohner, G., Bauknecht, H.-C., Klingebiel, R., Flor, H., & Klapp, B. F. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.05.008 · Cited by 679 · cited 1× · see citing works
“(16) in their study of normal-weight and obese women described as neither hungry nor satiated, and of those reported by Stoeckel et al.”
BackgroundImages 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
Trends in Energy Intake in U.S. between 1977 and 1996: Similar Shifts Seen across Age Groups
Nielsen, S. J., Siega‐Riz, A. M., & Popkin, B. M. (2002) · Obesity Research · doi:10.1038/oby.2002.51 · Cited by 634 · see citing works
The Hormonal Control of Food Intake
Coll, A. P., Farooqi, I. S., & O’Rahilly, S. (2007) · Cell · doi:10.1016/j.cell.2007.04.001 · Cited by 605 · see citing works
Widespread origin of the primate mesofrontal dopamine system.
Williams, S. M., & Goldman-Rakic, P. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.4.321 · Cited by 481 · see citing works
The Effect of Pre-exposure to Food Cues on the Eating Behavior of Restrained and Unrestrained Eaters
Fedoroff, I. C., Polivy, J., & Herman, C. P. (1997) · Appetite · doi:10.1006/appe.1996.0057 · Cited by 471 · see citing works
Central Control of Body Weight and Appetite
Woods, S. C., & D’Alessio, D. A. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1630 · Cited by 460 · see citing works
Hunger selectively modulates corticolimbic activation to food stimuli in humans
LaBar, K. S., Gitelman, D. R., Parrish, T. B., Kim, Y.-H., Nobre, A. C., & Mesulam, M. M. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.2.493 · Cited by 444 · see citing works
Gut Hormones and Appetite Control
Wren, A., & Bloom, S. R. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.03.048 · Cited by 434 · see citing works
Fedoroff, I. C., Polivy, J., & Herman, C. P. (2003) · Appetite · doi:10.1016/s0195-6663(03)00026-6 · Cited by 359 · see citing works
Central and Peripheral Regulation of Food Intake and Physical Activity: Pathways and Genes
Lenard, N. R., & Berthoud, H. (2008) · Obesity · doi:10.1038/oby.2008.511 · Cited by 338 · see citing works
Caloric imbalance and public health policy.
Koplan, J. P., & Dietz, W. (1999) · Journal of the American Medical Association (JAMA) · doi:10.1001/jama.282.16.1579 · Cited by 337 · see citing works
Overweight children overeat after exposure to food cues
Jansen, A. T. M., Theunissen, N. C. M., Slechten, K., Nederkoorn, C., Boon, B. J. F., Mulkens, S., & Roefs, A. (2003) · Eating Behaviors · doi:10.1016/s1471-0153(03)00011-4 · Cited by 336 · see citing works
Chiba, T., Kayahara, T., & Nakano, K. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03013-4 · Cited by 290 · see citing works
Differential brain responses to satiation in obese and lean men.
Gautier, J., Chen, K., Salbe, A. D., Bandy, D. J., Pratley, R. E., Heiman, M. L., Ravussin, É., Reiman, E. M., & Tataranni, P. A. (2000) · Diabetes · doi:10.2337/diabetes.49.5.838 · Cited by 283 · see citing works
Neural Mechanisms Associated With Food Motivation in Obese and Healthy Weight Adults
Martin, L. E., Holsen, L. M., Chambers, R. J., Bruce, A. S., Brooks, W. M., Zarcone, J. R., Butler, M. G., & Savage, C. R. (2009) · Obesity · doi:10.1038/oby.2009.220 · Cited by 278 · see citing works
Lathe, R. (2001) · Journal of Endocrinology · doi:10.1677/joe.0.1690205 · Cited by 272 · see citing works
Exposure to the Taste of Alcohol Elicits Activation of the Mesocorticolimbic Neurocircuitry
Filbey, F. M., Claus, E., Audette, A. R., Niculescu, M., Banich, M. T., Tanabe, J., Du, Y. P., & Hutchison, K. E. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301513 · Cited by 270 · see citing works
Myrick, H., Anton, R. F., Li, X., Henderson, S., Randall, P. K., & Voronin, K. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.4.466 · Cited by 258 · see citing works
A role for hippocampus in the utilization of hunger signals
Davidson, T. L., & Jarrard, L. E. (1993) · Behavioral and Neural Biology · doi:10.1016/0163-1047(93)90925-8 · Cited by 216 · see citing works
A potential role for the hippocampus in energy intake and body weight regulation
Davidson, T. L., Kanoski, S. E., Schier, L. A., Clegg, D. J., & Benoit, S. C. (2007) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.10.008 · Cited by 178 · see citing works
Shelley, B. P., & Trimble, M. (2004) · The World Journal of Biological Psychiatry · doi:10.1080/15622970410029933 · Cited by 168 · see citing works
Davids, S., Lauffer, H., Thoms, K., Jagdhuhn, M., Hirschfeld, H., Domín, M., Hamm, A. O., & Lotze, M. (2009) · International Journal of Obesity · doi:10.1038/ijo.2009.193 · Cited by 162 · see citing works
McCaffery, J. M., Haley, A. P., Sweet, L. H., Phelan, S., Raynor, H. A., Del Parigi, A., Cohen, R., & Wing, R. R. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27924 · Cited by 161 · see citing works
Olfactory influences on appetite and satiety in humans
Yeomans, M. R. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.04.010 · Cited by 160 · see citing works
Cornier, M., Salzberg, A. K., Endly, D. C., Bessesen, D. H., Rojas, D. C., & Tregellas, J. R. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006310 · Cited by 154 · see citing works
The hippocampus and motivation revisited: appetite and activity
Tracy, A. L., Jarrard, L. E., & Davidson, T. L. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00364-3 · Cited by 148 · see citing works
Kareken, D. A., Claus, E. D., Sabri, M., Džemidžić, M., Kosobud, A., Radnovich, A. J., Hector, D. H., Ramchandani, V. A., O’Connor, S., Lowe, M. J., et al. (2004) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000122764.60626.af · Cited by 122 · see citing works
Self-citationPetrovich, G. D., Ross, C. A., Holland, P. C., & Gallagher, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5001-06.2007 · Cited by 118 · see citing works
Regional cerebral blood flow during food exposure in obese and normal- weight women
Karhunen, L. J. (1997) · Brain · doi:10.1093/brain/120.9.1675 · Cited by 107 · see citing works
Individual differences in food-cue reactivity. The role of BMI and everyday portion-size selections
Tetley, A., Brunstrom, J., & Griffiths, P. (2009) · Appetite · doi:10.1016/j.appet.2009.02.005 · Cited by 103 · see citing works
Little and often: Ingestive behavior patterns following hippocampal lesions in rats.
Clifton, P. G., Vickers, S. P., & Somerville, E. M. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.3.502 · Cited by 100 · see citing works
Little and often: Ingestive behavior patterns following hippocampal lesions in rats.
Clifton, P. G., Vickers, S. P., & Somerville, E. M. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.3.502 · Cited by 92 · see citing works
Gautier, J., Chen, K., Uecker, A., Bandy, D. J., Frost, J., Salbe, A. D., Pratley, R. E., Lawson, M. A., Ravussin, É., Reiman, E. M., et al. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/70.5.806 · Cited by 82 · see citing works
Kareken, D. A., Bragulat, V., Džemidžić, M., Cox, C., Talavage, T. M., Davidson, D., & O’Connor, S. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.11.076 · Cited by 78 · see citing works
Self-citationAlcohol Sensitizes Cerebral Responses to the Odors of Alcoholic Drinks: An fMRI Study
Bragulat, V., Džemidžić, M., Talavage, T. M., Davidson, D., O’Connor, S., & Kareken, D. A. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2008.00693.x · Cited by 66 · see citing works
Self-citationMental phenomena induced by stimulation in the limbic system.
Halgren, E. (1982) · PubMed · Cited by 54 · see citing works
Amount of ingested custard dessert as affected by its color, odor, and texture
DEWIJK, R., Polet, I. A., Engelen, L., et al. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.04.053 · Cited by 52 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Reward, dopamine and the control of food intake: implications for obesity
Volkow, N. D., Wang, G.-J., & Baler, R. D. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.11.001 · Cited by 1,400 · see citing works
Obesity and addiction: Neurobiological overlaps
Volkow, N. D., Wang, G. ‐., Tomasi, D., & Baler, R. D. (2013) · Obesity Reviews · doi:10.1111/j.1467-789x.2012.01031.x · Cited by 800 · see citing works
Reward mechanisms in obesity: new insights and future directions
Kenny, P. J. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.016 · Cited by 748 · see citing works
Neural correlates of long-term intense romantic love
Acevedo, B. P., Aron, A., Fisher, H. E., & Brown, L. L. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq092 · Cited by 441 · see citing works
“Although little is known about the posterior hippocampal region, some studies have shown increased activation in this area in association with hunger and food craving (LaBar et al., 2001; Pelchat et al., 2004), with particularly greater activity shown in obese individuals (Bragulat et al., 2010).”
BackgroundNeuroimaging and obesity: current knowledge and future directions
Carnell, S., Gibson, C., Benson, L., Ochner, C. N., & Geliebter, A. (2012) · Obesity Reviews · doi:10.1111/j.1467-789x.2011.00927.x · Cited by 441 · see citing works
Pursey, K. M., Stanwell, P., Callister, R. J., Brain, K., Collins, C. E., & Burrows, T. L. (2014) · Frontiers in Nutrition · doi:10.3389/fnut.2014.00007 · Cited by 239 · see citing works
Sleep restriction increases the neuronal response to unhealthy food in normal-weight individuals
St-Onge, M.-P., Wolfe, S., Sy, M., Shechter, A., & Hirsch, J. (2014) · International Journal of Obesity · doi:10.1038/ijo.2013.114 · Cited by 229 · see citing works
Dimitropoulos, A., Tkach, J., Ho, A., & Kennedy, J. (2012) · Appetite · doi:10.1016/j.appet.2011.10.014 · Cited by 151 · see citing works
Bhargava, A., Arnold, A. P., Bangasser, D. A., Denton, K. M., Gupta, A., Hilliard Krause, L. M., Mayer, E. A., McCarthy, M., Miller, W. L., Raznahan, A., et al. (2021) · Endocrine Reviews · doi:10.1210/endrev/bnaa034 · Cited by 130 · see citing works
- Authors
- Bragulat, V., Dzemidzic, M., Bruno, C., Cox, C. A., Talavage, T., Considine, R. V., & Kareken, D. A.
- Affiliations
- Indiana University Indianapolis (US)
- Indiana University School of Medicine (US)
- Purdue University West Lafayette (US)
- Corresponding author
- Considine, Robert V.
- Kareken, David A.
- Venue
- Obesity
- Publisher
- Wiley
- Published
- 2010-08
- Volume
- 18
- Issue
- 8
- Pages
- 1566-1571
- ISSN
- 1930-7381 (ISSN-L)
- 1930-739X
- OpenAlex
- W2140940174
- Cited by
- 128
- References
- 49
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 3 · 2023: 6 · 2022: 3 · 2021: 15 · 2020: 9 · 2019: 8 · 2018: 8 · 2017: 9 · 2016: 10 · 2015: 6 · 2014: 11 · 2013: 11 · 2012: 9
- FWCI
- 5.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Obesity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Alcohol Abuse and Alcoholism (R01AA014605)
- National Center for Research Resources (M01RR000750)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- food aroma, hunger, brain reward circuits, food deprivation, appetite, insula, ventral striatum, cingulate cortex, hippocampus, gustatory cortex, naturalistic stimuli, food cues
- MeSH terms
- Adult, Brain, Brain Mapping, Cues, Female, Food, Food Deprivation, Food Preferences, Humans, Hunger, Magnetic Resonance Imaging, Odorants, Pilot Projects, Reward, Smell, Stimulation, Chemical, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review