- 1Department of Psychology, La Sapienza University of Rome, Rome, Italy
- 2IRCCS Santa Lucia Foundation, Rome, Italy
A Commentary on
Gain in Body Fat Is Associated with Increased Striatal Response to Palatable Food Cues, whereas Body Fat Stability Is Associated with Decreased Striatal Response
by Stice, E., and Yokum, S. (2016). J. Neurosci. 36, 6949–6956. doi: 10.1523/JNEUROSCI.4365-15.2016
Perspectives on Neural Vulnerability to Weight Gain during Adolescence
Obesity has become a global public health challenge in the last few years (Swinburn et al., 2011). Body fat stability is particularly important for preventing future weight gain, and its influence is felt as early as adolescence. Behavioral studies have suggested that palatability and access to a variety of foods may affect appetite, food intake, and weight gain (Johnson and Wardle, 2014). Indeed, it has been demonstrated that food-cue reactivity and cue-induced cravings predict eating habits and weight gain, both systematically and prospectively (Boswell and Kober, 2016).
From a neural perspective, some regions of the brain involved in reward (the ventral striatum and orbitofrontal cortex) and attention (anterior cingulate cortex and precuneus) undergo pronounced changes in response to high-calorie food cues (Small et al., 2001; Berridge et al., 2010; Ziauddeen et al., 2015; Stice and Yokum, 2016a). Although the relationship between the neural circuits activated during food intake or food-cue reactivity and weight gain has been studied in depth, there are few longitudinal studies on the development of food hyper-responsivity during adolescence and neural vulnerability factors (Holsen et al., 2005; Killgore and Yurgelun-Todd, 2005; Yokum et al., 2014).
An article by Stice and Yokum (2016b) published in the Journal of Neuroscience focuses on the link between weight gain (body fat percentage) and the responsivity of neural regions involved in food reward. A repeated-measures fMRI protocol was applied in this longitudinal study of adolescents to assess changes in the blood-oxygen-level dependent (BOLD) signal response within the regions of the brain involved in reward and attention to palatable food cues when the participants gained weight, lost weight, or maintained a stable weight over a two- to three-year follow-up period. As a control procedure, the researchers studied neural responses to the receipt and potential receipt of monetary rewards among the same group of adolescents. The authors found increased activation of the putamen, mid-insula, and Rolandic operculum in response to palatable food images among participants who gained body fat compared to those who remained stable or lost weight after a 2 or 3-year follow-up period.
This finding is in line with other studies that found the activation of these regions to be increased in response to palatable food cues among people with high body mass indices (Stoeckel et al., 2008; Martin et al., 2010; Stice et al., 2010). These studies also align with incentive sensitization theory, according to which elevated responsivity to food cues within the regions of the brain associated with hedonic rewards leads to overconsumption of that food (Berridge et al., 2010). Compared to adolescents who gained weight, whose striatal responsivity increases and leads to future overeating, adolescents who lost weight or maintained body fat show reduced activation of the striatal, insular, and Rolandic opercula in response to palatable foods. Interestingly, the activity in the same neural regions in response to monetary rewards was not increased, suggesting that the hyper-responsivity was specific to food.
The results showed no relationship between neural activation and changes in the pleasure, desire, and reinforcement participants reported in response to a milkshake. However, in adolescents who gained body fat the desire for the milkshake significantly increased from the baseline to the follow up. Taken together, these results may suggest that multiple mechanisms are involved, such as basic motivational and emotional responses as well as cognitive and inhibitory control.
Although increased activity in the striatal regions is mediated by monetary reward among adults (Stice et al., 2011), the absence of modulation in control tasks among adolescents may reflect different structural maturation and neurocognitive strategies between these two age groups. Furthermore, reduction in the amount of time participants worked to earn snack foods or money following the application of a progressive reinforcement paradigm suggests that multiple mechanisms related to social desirability (Leehr et al., 2016), or cognitive strategies may be engaged during the task. As suggested by a novel experimental study (Kemps et al., 2016), restrained eaters who expect to eat high-calorie foods may be able to activate their dieting goal, thereby limiting their food intake or, in this case, food gain. Habitual eating behaviors should therefore be taken into account in future studies, particularly those involving adolescents.
Stice and Yokum's findings shed new light on a rapidly growing area of neuroscience that highlights the neural mechanisms involved in the multifactor etiological process of obesity. These outcomes may have implications for weight loss interventions and the prevention or promotion of healthy diets, habits, and lifestyles since neural hyper-responsivity to food might be a key factor in vulnerability to future weight gain. Encouraging studies suggest that sustained modification of attentional bias may lead to reduced consumption of high-calorie foods, such as chocolate (Kemps et al., 2015), and promote healthy eating (Kakoschke et al., 2014). This may, in turn, reduce the risk of future overeating and weight gain. Identifying the reasons for hyper-responsivity to food cues in people who are gaining weight, are obese, or are candidates for bariatric surgery may be valuable when developing personalized programs in which attention to food cues is addressed.
However, one must use caution when drawing direct links between altered brain responses and obesity since other mediators, such as impulsivity or self-control strategies (Ziauddeen et al., 2015), may be involved, particularly in adolescents. Several developmental neuroimaging studies suggest that, compared to adults and children, adolescents exhibit different responsivity in different neural regions involved in reward processing, such as the ventral striatum and orbitofrontal cortex (Galvan et al., 2006; Gladwin et al., 2011). To generalize these results, as previously noted by Stice and Yokum (2016b), future studies should examine the responsivity of reward-related regions of the brain to a broader range of palatable food, such as salty food and junk food. More work that investigates adolescents is necessary since they are more responsive to reward-related visual food stimuli, such as food advertising (Jastreboff et al., 2014).
Author Contributions
All authors listed, have made substantial, direct and intellectual contribution to the work, and approved it for publication.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Berridge, K. C., Ho, C. Y., Richard, J. M., and Difeliceantonio, A. G. (2010). The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res. 1350, 43–64. doi: 10.1016/j.brainres.2010.04.003
Boswell, R. G., and Kober, H. (2016). Food cue reactivity and craving predict eating and weight gain: a meta-analytic review. Obes. Rev. 17, 159–177. doi: 10.1111/obr.12354
Galvan, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., et al. (2006). Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J. Neurosci. 26, 6885–6892. doi: 10.1523/JNEUROSCI.1062-06.2006
Gladwin, T. E., Figner, B., Crone, E. A., and Wiers, R. W. (2011). Addiction, adolescence, and the integration of control and motivation. Dev. Cogn. Neurosci. 1, 364–376. doi: 10.1016/j.dcn.2011.06.008
Holsen, L. M., Zarcone, J. R., Thompson, T. I., Brooks, W. M., Anderson, M. F., Ahluwalia, J. S., et al. (2005). Neural mechanisms underlying food motivation in children and adolescents. Neuroimage 27, 669–676. doi: 10.1016/j.neuroimage.2005.04.043
Jastreboff, A. M., Lacadie, C., Seo, D., Kubat, J., Van Name, M. A., Giannini, C., et al. (2014). Leptin is associated with exaggerated brain reward and emotion responses to food images in adolescent obesity. Diabetes Care 37, 3061–3068. doi: 10.2337/dc14-0525
Johnson, F., and Wardle, J. (2014). Variety, palatability, and obesity. Adv. Nutr. 5, 851–859. doi: 10.3945/an.114.007120
Kakoschke, N., Kemps, E., and Tiggemann, M. (2014). Attentional bias modification encourages healthy eating. Eat. Behav. 15, 120–124. doi: 10.1016/j.eatbeh.2013.11.001
Kemps, E., Herman, C. P., Hollitt, S., Polivy, J., Prichard, I., and Tiggemann, M. (2016). The role of expectations in the effect of food cue exposure on intake. Appetite 103, 259–264. doi: 10.1016/j.appet.2016.04.026
Kemps, E., Tiggemann, M., and Elford, J. (2015). Sustained effects of attentional re-training on chocolate consumption. J. Behav. Ther. Exp. Psychiatry 49, 94–100. doi: 10.1016/j.jbtep.2014.12.001
Killgore, W. D., and Yurgelun-Todd, D. A. (2005). Developmental changes in the functional brain responses of adolescents to images of high and low-calorie foods. Dev. Psychobiol. 47, 377–397. doi: 10.1002/dev.20099
Leehr, E. J., Schag, K., Brinkmann, A., Ehlis, A. C., Fallgatter, A. J., Zipfel, S., et al. (2016). Alleged approach-avoidance conflict for food stimuli in binge eating disorder. PLoS ONE 11:e0152271. doi: 10.1371/journal.pone.0152271
Martin, L. E., Holsen, L. M., Chambers, R. J., Bruce, A. S., Brooks, W. M., Zarcone, J. R., et al. (2010). Neural mechanisms associated with food motivation in obese and healthy weight adults. Obesity 18, 254–260. doi: 10.1038/oby.2009.220
Small, D. M., Zatorre, R. J., Dagher, A., Evans, A. C., and Jones-Gotman, M. (2001). Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 124, 1720–1733. doi: 10.1093/brain/124.9.1720
Stice, E., and Yokum, S. (2016a). Neural vulnerability factors that increase risk for future weight gain. Psychol. Bull. 142, 447–471. doi: 10.1037/bul0000044
Stice, E., and Yokum, S. (2016b). Gain in body fat is associated with increased striatal response to palatable food cues, whereas body fat stability is associated with decreased striatal response. J. Neurosci. 36, 6949–6956. doi: 10.1523/JNEUROSCI.4365-15.2016
Stice, E., Yokum, S., Bohon, C., Marti, N., and Smolen, A. (2010). Reward circuitry responsivity to food predicts future increases in body mass: moderating effects of DRD2 and DRD4. Neuroimage 50, 1618–1625. doi: 10.1016/j.neuroimage.2010.01.081
Stice, E., Yokum, S., Burger, K. S., Epstein, L. H., and Small, D. M. (2011). Youth at risk for obesity show greater activation of striatal and somatosensory regions to food. J. Neurosci. 31, 4360–4366. doi: 10.1523/JNEUROSCI.6604-10.2011
Stoeckel, L. E., Weller, R. E., Cook, E. W. III., Twieg, D. B., Knowlton, R. C., and Cox, J. E. (2008). Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 41, 636–647. doi: 10.1016/j.neuroimage.2008.02.031
Swinburn, B. A., Sacks, G., Hall, K. D., McPherson, K., Finegood, D. T., Moodie, M. L., et al. (2011). The global obesity pandemic: shaped by global drivers and local environments. Lancet 378, 804–814. doi: 10.1016/S0140-6736(11)60813-1
Yokum, S., Gearhardt, A. N., Harris, J. L., Brownell, K. D., and Stice, E. (2014). Individual differences in striatum activity to food commercials predict weight gain in adolescents. Obesity 22, 2544–2551. doi: 10.1002/oby.20882
Keywords: reward, food-cues, adolescence, striatal response, weight gain
Citation: Cerolini S, Pazzaglia M and Lombardo C (2017) Commentary: Gain in Body Fat Is Associated with Increased Striatal Response to Palatable Food Cues, whereas Body Fat Stability Is Associated with Decreased Striatal Response. Front. Hum. Neurosci. 11:65. doi: 10.3389/fnhum.2017.00065
Received: 25 November 2016; Accepted: 31 January 2017;
Published: 14 February 2017.
Edited by:
Mikhail Lebedev, Duke University, USAReviewed by:
Chase R. Figley, University of Manitoba, CanadaRalph DiLeone, Yale University School of Medicine, USA
Copyright © 2017 Cerolini, Pazzaglia and Lombardo. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Silvia Cerolini, c2lsdmlhLmNlcm9saW5pQHVuaXJvbWExLml0