Brain Imaging and Behavior

, Volume 12, Issue 3, pp 685–696 | Cite as

Conflict-related dorsomedial frontal cortex activation during healthy food decisions is associated with increased cravings for high-fat foods

  • Ryan Smith
  • Anna Alkozei
  • William D. S. Killgore
Original Research


Previous studies suggest obesity is associated with altered function within the insula and dorsomedial frontal cortex (including dorsal anterior cingulate cortex; DMFC/dACC), reflecting abnormal reward processing and reduced sensitivity to feelings of satiety. Given the proposed roles of DMFC/dACC in monitoring response conflict and reward-based decision making, the present study examined DMFC/dACC activation, and functional connectivity between the DMFC/dACC and the anterior insula (AI), during food-related decision-making. Twenty participants recruited from the general population (10 Female) performed a decision task while undergoing functional magnetic resonance imaging. They were instructed to “choose the healthier option” when simultaneously shown pairs of images of different foods. Significant DMFC/dACC activation was observed during food-related decision-making, and activation levels also positively correlated with self-reported cravings for high-fat foods (r = 0.57, p = 0.009) and self-reported desire to eat the high-fat foods depicted in the images (r = 0.48, p = 0.032). Negative functional connectivity estimates between the right AI and DMFC/dACC were also associated with self-reported control over eating (r = −0.50, p = 0.025). These results suggest that (1) more intense cravings for unhealthy foods are associated with greater response conflict when deciding between healthy and unhealthy food options, and (2) lack of eating-related control may involve a reduced influence of insula-mediated bodily signals on decision-making. This task may offer a neuroimaging-based probe for identifying individuals vulnerable to eating-related disorders and should be replicated in clinical populations.


Decision-making Obesity Food Insula Dorsomedial frontal cortex Dorsal anterior cingulate cortex 


Compliance with ethical standards


This study was funded by a USAMRAA grant to WDSK (grant number W81XWH-09-1-0730).

Conflict of interest

Ryan Smith declares that he has no conflict of interest. Anna Alkozei declares that she has no conflict of interest. W.D. “Scott” Killgore declares that he has no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.


  1. Botvinick, M., Cohen, J., & Carter, C. (2004). Conflict monitoring and anterior cingulate cortex: An update. Trends in Cognitive Sciences, 8(12), 539–546. doi: 10.1016/j.tics.2004.10.003.CrossRefPubMedGoogle Scholar
  2. Brooks, S., Cedernaes, J., & Schiöth, H. (2013). Increased prefrontal and parahippocampal activation with reduced dorsolateral prefrontal and insular cortex activation to food images in obesity: A meta-analysis of fMRI studies. PloS One, 8(4), e60393. doi: 10.1371/journal.pone.0060393.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Brown, J., & Braver, T. (2005). Learned predictions of error likelihood in the anterior cingulate cortex. Science, 307(5712), 1118–1121. doi: 10.1126/science.1105783.CrossRefPubMedGoogle Scholar
  4. Candeias, V., Armstrong, T., & Xuereb, G. (2010). Diet and physical activity in schools: Perspectives from the implementation of the WHO global strategy on diet, physical activity and health. Canadian Journal of Public Health, 101(Suppl), S28–S30.PubMedGoogle Scholar
  5. Carnell, S., Gibson, C., Benson, L., Ochner, C. N., & Geliebter, A. (2012). Neuroimaging and obesity: Current knowledge and future directions. Obesity Reviews, 13(1), 43–56. doi: 10.1111/j.1467-789X.2011.00927.x.CrossRefPubMedGoogle Scholar
  6. Craig, A. D. (2003). Interoception: The sense of the physiological condition of the body. Current Opinion in Neurobiology, 13(4), 500–505.CrossRefPubMedGoogle Scholar
  7. Craig, A. D. (2009). How do you feel--now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10(1), 59–70.CrossRefPubMedGoogle Scholar
  8. Del Rio, D., Cano, V., Martín-Ramos, M., Gómez, M., Morales, L., Del Olmo, N., & Ruiz-Gayo, M. (2015). Involvement of the dorsomedial prefrontal cortex in high-fat food conditioning in adolescent mice. Behavioural Brain Research, 283, 227–232. doi: 10.1016/j.bbr.2015.01.039.CrossRefPubMedGoogle Scholar
  9. Domenech, P., & Koechlin, E. (2015). Executive control and decision-making in the prefrontal cortex. Current Opinion in Behavioral Sciences, 1, 101–106. doi: 10.1016/j.cobeha.2014.10.007.CrossRefGoogle Scholar
  10. Dunning, D., Heath, C., & Suls, J. (2004). Flawed self-assessment: Implications for health, education, and the workplace. Psychological Science in the Public Interest, 5(3), 69–106. doi: 10.1111/j.1529-1006.2004.00018.x.CrossRefPubMedGoogle Scholar
  11. Gaykema, R., Nguyen, X.-M., Boehret, J., Lambeth, P., Joy-Gaba, J., Warthen, D., & Scott, M. (2014). Characterization of excitatory and inhibitory neuron activation in the mouse medial prefrontal cortex following palatable food ingestion and food driven exploratory behavior. Frontiers in Neuroanatomy, 8, 60. doi: 10.3389/fnana.2014.00060.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gitelman, D., Penny, W., Ashburner, J., & Friston, K. (2003). Modeling regional and psychophysiologic interactions in fMRI: The importance of hemodynamic deconvolution. NeuroImage, 19(1), 200–207. doi: 10.1016/S1053-8119(03)00058-2.CrossRefPubMedGoogle Scholar
  13. Hare, T., Camerer, C., & Rangel, A. (2009). Self-control in decision-making involves modulation of the vmPFC valuation system. Science, 324(5927), 646–648. doi: 10.1126/science.1168450.CrossRefPubMedGoogle Scholar
  14. Hare, T., Malmaud, J., & Rangel, A. (2011). Focusing attention on the health aspects of foods changes value signals in vmPFC and improves dietary choice. Journal of Neuroscience, 31(30), 11077–11087. doi: 10.1523/JNEUROSCI.6383-10.2011.CrossRefPubMedGoogle Scholar
  15. Jezzini, A., Mazzucato, L., La Camera, G., & Fontanini, A. (2013). Processing of hedonic and chemosensory features of taste in medial prefrontal and insular networks. The Journal of Neuroscience, 33(48), 18966–18978. doi: 10.1523/JNEUROSCI.2974-13.2013.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kaye, W., Fudge, J., & Paulus, M. (2009). New insights into symptoms and neurocircuit function of anorexia nervosa. Nature reviews. Neuroscience, 10(8), 573–584. doi: 10.1038/nrn2682.PubMedGoogle Scholar
  17. Kelley, A. (2004). Ventral striatal control of appetitive motivation: Role in ingestive behavior and reward-related learning. Neuroscience and Biobehavioral Reviews, 27(8), 765–776. doi: 10.1016/j.neubiorev.2003.11.015.CrossRefPubMedGoogle Scholar
  18. Kerns, J., Cohen, J., MacDonald III, A., Cho, R., Stenger, V., & Carter, C. (2004). Anterior cingulate conflict monitoring and adjustments in control. Science, 303(5660), 1023–1026. doi: 10.1126/science.1089910.CrossRefPubMedGoogle Scholar
  19. Killgore, W., & Yurgelun-Todd, D. (2005). Body mass predicts orbitofrontal activity during visual presentations of high-calorie foods. Neuroreport, 16(8), 859–863.CrossRefPubMedGoogle Scholar
  20. Killgore, W., & Yurgelun-Todd, D. (2010). Sex differences in cerebral responses to images of high versus low-calorie food. Neuroreport, 21(5), 354–358. doi: 10.1097/WNR.0b013e32833774f7.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Killgore, W., Young, A., Femia, L., Bogorodzki, P., Rogowska, J., & Yurgelun-Todd, D. (2003). Cortical and limbic activation during viewing of high- versus low-calorie foods. NeuroImage, 19(4), 1381–1394. doi: 10.1016/S1053-8119(03)00191-5.CrossRefPubMedGoogle Scholar
  22. Killgore, W., Kipman, M., Schwab, Z., Tkachenko, O., Preer, L., Gogel, H., et al. (2013a). Physical exercise and brain responses to images of high-calorie food. Neuroreport, 24(17), 962–967. doi: 10.1097/WNR.0000000000000029.CrossRefPubMedGoogle Scholar
  23. Killgore, W., Schwab, Z., Weber, M., Kipman, M., DelDonno, S., Weiner, M., & Rauch, S. (2013b). Daytime sleepiness affects prefrontal regulation of food intake. NeuroImage, 71, 216–223. doi: 10.1016/j.neuroimage.2013.01.018.CrossRefPubMedGoogle Scholar
  24. Killgore, W., Weber, M., Schwab, Z., Kipman, M., DelDonno, S., Webb, C., & Rauch, S. (2013c). Cortico-limbic responsiveness to high-calorie food images predicts weight status among women. International Journal of Obesity, 37(11), 1435–1442. doi: 10.1038/ijo.2013.26.CrossRefPubMedGoogle Scholar
  25. van der Laan, L., de Ridder, D., Viergever, M., & Smeets, P. (2011). The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues. NeuroImage, 55(1), 296–303. doi: 10.1016/j.neuroimage.2010.11.055.CrossRefPubMedGoogle Scholar
  26. McLaren, D., Ries, M., Xu, G., & Johnson, S. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches. NeuroImage, 61(4), 1277–1286. doi: 10.1016/j.neuroimage.2012.03.068.CrossRefPubMedPubMedCentralGoogle Scholar
  27. van Meer, F., Charbonnier, L., & Smeets, P. (2016). Food decision-making: Effects of weight status and age. Current Diabetes Reports, 16(9), 84. doi: 10.1007/s11892-016-0773-z.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Naqvi, N., Rudrauf, D., Damasio, H., & Bechara, A. (2007). Damage to the insula disrupts addiction to cigarette smoking. Science, 315(5811), 531–534. doi: 10.1126/science.1135926.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Naqvi, N., Gaznick, N., Tranel, D., & Bechara, A. (2014). The insula: A critical neural substrate for craving and drug seeking under conflict and risk. Annals of the New York Academy of Sciences, 1316, 53–70. doi: 10.1111/nyas.12415.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ridderinkhof, K., Ullsperger, M., Crone, E., & Nieuwenhuis, S. (2004). The role of the medial frontal cortex in cognitive control. Science, 306(5695), 443–447. doi: 10.1126/science.1100301.CrossRefPubMedGoogle Scholar
  31. Silvetti, M., Alexander, W., Verguts, T., & Brown, J. (2014). From conflict management to reward-based decision making: Actors and critics in primate medial frontal cortex. Neuroscience and Biobehavioral Reviews, 46(Pt 1), 44–57. doi: 10.1016/j.neubiorev.2013.11.003.CrossRefPubMedGoogle Scholar
  32. Stice, E., Figlewicz, D., Gosnell, B., Levine, A., & Pratt, W. (2013). The contribution of brain reward circuits to the obesity epidemic. Neuroscience and Biobehavioral Reviews, 37(9 Pt a), 2047–2058. doi: 10.1016/j.neubiorev.2012.12.001.CrossRefPubMedGoogle Scholar
  33. Volkow, N., Wang, G.-J., Fowler, J., & Telang, F. (2008). Overlapping neuronal circuits in addiction and obesity: Evidence of systems pathology. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 363(1507), 3191–3200. doi: 10.1098/rstb.2008.0107.CrossRefGoogle Scholar
  34. Weissman, D., Gopalakrishnan, A., Hazlett, C., & Woldorff, M. (2004). Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. Cerebral Cortex, 15(2), 229–237. doi: 10.1093/cercor/bhh125.CrossRefPubMedGoogle Scholar
  35. Werthmann, J., Roefs, A., Nederkoorn, C., Mogg, K., Bradley, B., & Jansen, A. (2013). Attention bias for food is independent of restraint in healthy weight individuals—An eye tracking study. Eating Behaviors, 14(3), 397–400. doi: 10.1016/j.eatbeh.2013.06.005.CrossRefPubMedGoogle Scholar
  36. Zavala, B., Tan, H., Little, S., Ashkan, K., Hariz, M., Foltynie, T., et al. (2014). Midline frontal cortex low-frequency activity drives subthalamic nucleus oscillations during conflict. The Journal of Neuroscience, 34(21), 7322–7333. doi: 10.1523/JNEUROSCI.1169-14.2014.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ziauddeen, H., & Fletcher, P. (2013). Is food addiction a valid and useful concept? Obesity Reviews, 14(1), 19–28. doi: 10.1111/j.1467-789X.2012.01046.x.CrossRefPubMedGoogle Scholar
  38. Ziauddeen, H., Farooqi, I., & Fletcher, P. (2012). Obesity and the brain: How convincing is the addiction model? Nature reviews. Neuroscience, 13(4), 279–286. doi: 10.1038/nrn3212.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Ryan Smith
    • 1
  • Anna Alkozei
    • 1
  • William D. S. Killgore
    • 1
    • 2
  1. 1.Department of PsychiatryUniversity of ArizonaTucsonUSA
  2. 2.Department of PsychiatryMcLean Hospital, Harvard Medical SchoolBelmontUSA

Personalised recommendations