Skip to main content
Log in

Correlation Between Ventromedial Prefrontal Cortex Activation to Food Aromas and Cue-Driven Eating: An fMRI Study

  • Published:
Chemosensory Perception

Abstract

Food aromas are signals associated with both food's availability and pleasure. Previous research from this laboratory has shown that food aromas under fasting conditions evoke robust activation of medial prefrontal brain regions thought to reflect reward value (Bragulat et al., Obesity (Silver Spring), 18(8): 1566–1571, 2010). In the current study, 18 women (11 normal weight and 7 obese) underwent a 2-day imaging study (one after being fed and one while fasting). All were imaged on a 3T Siemens Trio-Tim scanner while sniffing two food (F; pasta and beef) odors, one non-food (NF; Douglas fir) odor, and an odorless control (CO). Prior to imaging, participants rated hunger and perceived odor qualities and completed the Dutch Eating Behavior Questionnaire (DEBQ) to assess "externality" (the extent to which eating is driven by external food cues). Across all participants, both food and non-food odors (compared to CO) elicited large blood oxygenation level dependent (BOLD) responses in olfactory and reward-related areas, including the medial prefrontal and anterior cingulate cortex, bilateral orbitofrontal cortex, and bilateral piriform cortex, amygdala, and hippocampus. However, food odors produced greater activation of medial prefrontal cortex, left lateral orbitofrontal cortex, and inferior insula than non-food odors. Moreover, there was a significant correlation between the (F > CO) BOLD response in ventromedial prefrontal cortex and “externality” sub-scale scores of the DEBQ, but only under the fed condition; no such correlation was present with the (NF > CO) response. This suggests that in those with high externality, ventromedial prefrontal cortex may inappropriately valuate external food cues in the absence of internal hunger.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

3D-PACE:

Three-dimensional prospective acquisition correction

ACC:

Anterior cingulate cortex

BMI:

Body mass index

BOLD:

Blood oxygenation level dependent

CO:

Control odorless sniffing

CRC:

Clinical Research Center

DEBQ:

Dutch Eating Behavior Questionnaire

F :

Food odors

FA:

Flip angle

FDR:

False discovery rate

fMRI:

Functional magnetic resonance imaging

FOV:

Field of view

LMS:

Labeled magnitude scale

MNI:

Montreal Neurological Institute

mPFC:

Medial prefrontal cortex

MPRAGE:

Magnetization prepared rapid gradient echo

MRI:

Magnetic resonance imaging

NF:

Non-food odor

OFC:

Orbitofrontal cortex

ROI:

Region of interest

SD:

Standard deviation

TR:

Repetition time

TE:

Echo Time

VAS:

Visual Analog Scale

vmPFC:

Ventromedial prefrontal cortex

References

  • Arana FS, Parkinson JA, Hinton E, Holland AJ, Owen AM, Roberts AC (2003) Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection. J Neurosci 23(29):9632–9638

    CAS  Google Scholar 

  • Bellisle F, Louis-Sylvestre J, Demozay F, Blazy D, Le Magnen J (1985) Cephalic phase of insulin secretion and food stimulation in humans: a new perspective. Am J Physiol 249(6 Pt 1):E639–E645

    CAS  Google Scholar 

  • Berridge KC (2007) The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacol Berl 191(3):391–431

    Article  CAS  Google Scholar 

  • Berridge KC, Ho CY, Richard JM, DiFeliceantonio AG (2010) The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res 1350:43–64

    Article  CAS  Google Scholar 

  • Berthoud HR (2006) Homeostatic and non-homeostatic pathways involved in the control of food intake and energy balance. Obes Silver Spring 14 Suppl 5:197S–200S

    Article  Google Scholar 

  • Bragulat V, Dzemidzic M, Talavage T, Davidson D, O'Connor SJ, Kareken DA (2008) Alcohol sensitizes cerebral responses to the odors of alcoholic drinks: an fMRI study. Alcohol Clin Exp Res 32(7):1124–1134

    Article  Google Scholar 

  • Bragulat V, Dzemidzic M, Bruno C, Cox CA, Talavage T, Considine RV, Kareken DA (2010) Food-related odor probes of brain reward circuits during hunger: a pilot FMRI study. Obes Silver Spring 18(8):1566–1571

    Article  Google Scholar 

  • Bray S, Shimojo S, O'Doherty JP (2010) Human medial orbitofrontal cortex is recruited during experience of imagined and real rewards. J Neurophysiol 103(5):2506–2512

    Article  Google Scholar 

  • Brett, M., Anton, J., Valabregue, R., & Poline, J. (2002). Region of interest analysis using an SPM toolbox. Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan

  • Cardello AV, Schutz HG, Lesher LL, Merrill E (2005) Development and testing of a labeled magnitude scale of perceived satiety. Appetite 44(1):1–13

    Article  Google Scholar 

  • Carnell S, Wardle J (2008) Appetite and adiposity in children: evidence for a behavioral susceptibility theory of obesity. Am J Clin Nutr 88(1):22–29

    CAS  Google Scholar 

  • Castellanos EH, Charboneau E, Dietrich MS, Park S, Bradley BP, Mogg K, Cowan RL (2009) Obese adults have visual attention bias for food cue images: evidence for altered reward system function. Int J Obes Lond 33(9):1063–1073

    Article  CAS  Google Scholar 

  • Chib VS, Rangel A, Shimojo S, O'Doherty JP (2009) Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. J Neurosci 29(39):12315–12320

    Article  CAS  Google Scholar 

  • Cornier MA, Salzberg AK, Endly DC, Bessesen DH, Rojas DC, Tregellas JR (2009) The effects of overfeeding on the neuronal response to visual food cues in thin and reduced-obese individuals. PLoS One 4(7):e6310

    Article  Google Scholar 

  • Davidson TL, Jarrard LE (1993) A role for hippocampus in the utilization of hunger signals. Behav Neural Biol 59(2):167–171

    Article  CAS  Google Scholar 

  • Davidson TL, Kanoski SE, Schier LA, Clegg DJ, Benoit SC (2007) A potential role for the hippocampus in energy intake and body weight regulation. Curr Opin Pharmacol 7(6):613–616

    Article  CAS  Google Scholar 

  • de Wijk RA, Polet IA, Engelen L, van Doorn RM, Prinz JF (2004) Amount of ingested custard dessert as affected by its color, odor, and texture. Physiol Behav 82(2–3):397–403

    Google Scholar 

  • Doty RL (1995) The smell identification testTM: administration manual, 3rd edn. Sensonics, Hadon Heights

    Google Scholar 

  • Fedoroff IC, Polivy J, Herman CP (1997) The effect of pre-exposure to food cues on the eating behavior of restrained and unrestrained eaters. Appetite 28(1):33–47

    Article  CAS  Google Scholar 

  • Fedoroff I, Polivy J, Herman CP (2003) The specificity of restrained versus unrestrained eaters' responses to food cues: general desire to eat, or craving for the cued food? Appetite 41(1):7–13

    Article  Google Scholar 

  • Filbey FM, Claus E, Audette AR, Niculescu M, Banich MT, Tanabe J, Hutchison KE (2008) Exposure to the taste of alcohol elicits activation of the mesocorticolimbic neurocircuitry. Neuropsychopharmacology 33(6):1391–1401

    Article  CAS  Google Scholar 

  • Flegal KM (2005) Epidemiologic aspects of overweight and obesity in the United States. Physiol Behav 86(5):599–602

    Article  CAS  Google Scholar 

  • Flegal KM, Carroll MD, Kuczmarski RJ, Johnson CL (1998) Overweight and obesity in the United States: prevalence and trends, 1960–1994. Int J Obes Relat Metab Disord 22(1):39–47

    Article  CAS  Google Scholar 

  • Gautier JF, Chen K, Uecker A, Bandy D, Frost J, Salbe AD, Tataranni PA (1999) Regions of the human brain affected during a liquid-meal taste perception in the fasting state: a positron emission tomography study. Am J Clin Nutr 70(5):806–810

    CAS  Google Scholar 

  • Gearhardt AN, Yokum S, Orr PT, Stice E, Corbin WR, Brownell KD (2011) Neural correlates of food addiction. Arch Gen Psychiatry 68(8):808–816

    Article  Google Scholar 

  • Green BG, Dalton P, Cowart B, Shaffer G, Rankin K, Higgins J (1996) Evaluating the 'Labeled Magnitude Scale' for measuring sensations of taste and smell. Chem Senses 21(3):323–334

    Article  CAS  Google Scholar 

  • Hare TA, O'Doherty J, Camerer CF, Schultz W, Rangel A (2008) Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors. J Neurosci 28(22):5623–5630

    Article  CAS  Google Scholar 

  • Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324(5927):646–648

    Article  CAS  Google Scholar 

  • Hare TA, Camerer CF, Knoepfle DT, Rangel A (2010) Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J Neurosci 30(2):583–590

    Article  CAS  Google Scholar 

  • Hare TA, Malmaud J, Rangel A (2011) Focusing attention on the health aspects of foods changes value signals in vmPFC and improves dietary choice. J Neurosci 31(30):11077–11087

    Article  CAS  Google Scholar 

  • Hebben N, Corkin S, Eichenbaum H, Shedlack K (1985) Diminished ability to interpret and report internal states after bilateral medial temporal resection: case H.M. Behav Neurosci 99(6):1031–1039

    Article  CAS  Google Scholar 

  • Herman CP, Polivy J (1980) Restrained eating. In: Stunkard AJ (ed) Obesity. Saunders, Philadelphia, pp 208–225

    Google Scholar 

  • Hock BJ Jr, Bunsey MD (1998) Differential effects of dorsal and ventral hippocampal lesions. J Neurosci 18(17):7027–7032

    CAS  Google Scholar 

  • Jansen A, Theunissen N, Slechten K, Nederkoorn C, Boon B, Mulkens S, Roefs A (2003) Overweight children overeat after exposure to food cues. Eat Behav 4(2):197–209

    Article  Google Scholar 

  • Kable JW, Glimcher PW (2007) The neural correlates of subjective value during intertemporal choice. Nat Neurosci 10(12):1625–1633

    Article  CAS  Google Scholar 

  • Kareken DA, Claus ED, Sabri M, Dzemidzic M, Kosobud AE, Radnovich AJ, Li TK (2004) Alcohol-related olfactory cues activate the nucleus accumbens and ventral tegmental area in high-risk drinkers: preliminary findings. Alcohol Clin Exp Res 28(4):550–557

    Article  Google Scholar 

  • Kareken DA, Bragulat V, Dzemidzic M, Cox C, Talavage T, Davidson D, O'Connor SJ (2010a) Family history of alcoholism mediates the frontal response to alcoholic drink odors and alcohol in at-risk drinkers. NeuroImage 50(1):267–276

    Article  Google Scholar 

  • Kareken DA, Liang T, Wetherill L, Dzemidzic M, Bragulat V, Cox C, Foroud T (2010b) A polymorphism in GABRA2 is associated with the medial frontal response to alcohol cues in an fMRI study. Alcohol Clin Exp Res 34(12):2169–2178

    Article  Google Scholar 

  • Kareken, D. A., Grahame, N., Dzemidzic, M., Walker, M. J., Lehigh, C. A., & O'Connor, S. J. (2011). fMRI of the brain's response to stimuli experimentally paired with alcohol intoxication. Psychopharmacology (Berl) (in press)

  • LaBar KS, Gitelman DR, Parrish TB, Kim YH, Nobre AC, Mesulam MM (2001) Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behav Neurosci 115(2):493–500

    Article  CAS  Google Scholar 

  • Martin LE, Holsen LM, Chambers RJ, Bruce AS, Brooks WM, Zarcone JR, Savage CR (2010) Neural mechanisms associated with food motivation in obese and healthy weight adults. Obes Silver Spring 18(2):254–260

    Article  Google Scholar 

  • Mela DJ (2006) Novel food technologies: enhancing appetite control in liquid meal replacers. Obes Silver Spring 14 Suppl 4:179S–181S

    Article  Google Scholar 

  • Mozell MM, Smith BP, Smith PE, Sullivan RL Jr, Swender P (1969) Nasal chemoreception in flavor identification. Arch Otolaryngol 90(3):367–373

    Article  CAS  Google Scholar 

  • Murphy C, Cain WS, Bartoshuk LM (1977) Mutual action of taste and olfaction. Sens Proc 1(3):204–211

    CAS  Google Scholar 

  • Myrick H, Anton RF, Li X, Henderson S, Randall PK, Voronin K (2008) Effect of naltrexone and ondansetron on alcohol cue-induced activation of the ventral striatum in alcohol-dependent people. Arch Gen Psychiatry 65(4):466–475

    Article  CAS  Google Scholar 

  • Noonan MP, Mars RB, Rushworth MF (2011) Distinct roles of three frontal cortical areas in reward-guided behavior. J Neurosci 31(40):14399–14412

    Article  CAS  Google Scholar 

  • O’Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F, Kobal G, Renner B, Ahne G. (2000) Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11(4):893–897

    Google Scholar 

  • Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM (2006) Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 295(13):1549–1555

    Article  CAS  Google Scholar 

  • Paulus MP, Frank LR (2003) Ventromedial prefrontal cortex activation is critical for preference judgments. Neuroreport 14(10):1311–1315

    Google Scholar 

  • Pelchat ML, Johnson A, Chan R, Valdez J, Ragland JD (2004) Images of desire: food-craving activation during fMRI. NeuroImage 23(4):1486–1493

    Article  Google Scholar 

  • Plassmann H, O'Doherty JP, Rangel A (2010) Appetitive and aversive goal values are encoded in the medial orbitofrontal cortex at the time of decision making. J Neurosci 30(32):10799–10808

    Article  CAS  Google Scholar 

  • Polivy J, Herman CP (1983) Breaking the diet habit: the natural weight alternative. Basic Books, New York

    Google Scholar 

  • Rothemund Y, Preuschhof C, Bohner G, Bauknecht HC, Klingebiel R, Flor H, Klapp BF (2007) Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. NeuroImage 37(2):410–421

    Article  Google Scholar 

  • Schachter S, Goldman R, Gordon A (1968) Effects of fear, food deprivation, and obesity on eating. J Pers Soc Psychol 10(2):91–97

    Article  CAS  Google Scholar 

  • Shepherd GM (2006) Smell images and the flavour system in the human brain. Nature 444(7117):316–321

    Article  CAS  Google Scholar 

  • Stoeckel LE, Weller RE, Cook EW 3rd, Twieg DB, Knowlton RC, Cox JE (2008) Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage 41(2):636–647

    Article  Google Scholar 

  • Thesen S, Heid O, Mueller E, Schad LR (2000) Prospective acquisition correction for head motion with image-based tracking for real-time fMRI. Magn Reson Med 44(3):457–465

    Article  CAS  Google Scholar 

  • Tracy AL, Jarrard LE, Davidson TL (2001) The hippocampus and motivation revisited: appetite and activity. Behav Brain Res 127(1–2):13–23

    Article  CAS  Google Scholar 

  • van Strien T, Frijters JE, Bergers GP, Defares PB (1986) Dutch eating behavior questionnaire for assessment of restrained, emotional and external eating behaviour. Int J Eat Disord 5(2):21

    Google Scholar 

  • Volkow ND, Wise RA (2005) How can drug addiction help us understand obesity? Nat Neurosci 8(5):555–560

    Article  CAS  Google Scholar 

  • Yeomans MR (2006) Olfactory influences on appetite and satiety in humans. Physiol Behav 87(4):800–804

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Supported by the National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases to RVC and DAK (R01 DK089070) and the Indiana CTSI, Indiana Clinical Research Center, UL RR025761. Special thanks to MR technologists Michele Beal and Courtney Robbins. We also thank Richard Mattes, MPH, Ph.D., R.D. (Purdue University) for his advice and assistance; Cheryl Armstrong, Ph.D., M.B.A., R.D. for her help with meal planning, preparation, and caloric intake measures; Stephen Warrenburg, Ph.D. at International Flavors and Fragrances for the donation of odorant stimuli; and Kieren Mather, M.D. for his medical support.

Financial Disclosures

The authors report no competing or conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David A. Kareken.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eiler, W.J.A., Dzemidzic, M., Case, K.R. et al. Correlation Between Ventromedial Prefrontal Cortex Activation to Food Aromas and Cue-Driven Eating: An fMRI Study. Chem. Percept. 5, 27–36 (2012). https://doi.org/10.1007/s12078-011-9112-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12078-011-9112-6

Keywords

Navigation