Negative affect and neural response to palatable food intake in bulimia nervosa

Cara Bohon, Eric Stice, Cara Bohon, Eric Stice

Abstract

Binge eating is often preceded by reports of negative affect, but the mechanism by which affect may lead to binge eating is unclear. This study evaluated the effect of negative affect on neural response to anticipation and receipt of palatable food in women with bulimia nervosa (BN) versus healthy controls. We also evaluated connectivity between the amygdala and reward-related brain regions. Females with and without BN (n=26) underwent functional magnetic resonance imaging (fMRI) during receipt and anticipated receipt of chocolate milkshake and a tasteless solution. We measured negative affect just prior to the scan. Women with BN showed a positive correlation between negative affect and activity in the putamen, caudate, and pallidum during anticipated receipt of milkshake (versus tasteless solution). There were no significant relations between negative affect and receipt of milkshake. Connectivity analyses revealed a greater relation of amygdala activity to activation in the left putamen and insula during anticipated receipt of milkshake in the bulimia group relative to the control group. The opposite pattern was found for the taste of milkshake; the control group showed a greater relation of amygdala activity to activation in the left putamen and insula in response to milkshake receipt than the bulimia group. Results show that as negative affect increases, so does responsivity of reward regions to anticipated intake of palatable food, implying that negative affect may increase the reward value of food for individuals with bulimia nervosa or that negative affect has become a conditioned cue due to a history of binge eating in a negative mood.

Copyright © 2012 Elsevier Ltd. All rights reserved.

Figures

Figure 1
Figure 1
Positive correlations between negative affect and signal change in the left caudate, putamen, and pallidum in the bulimia nervosa group. Images are in radiological view on the MNI- 152 standard brain, with the left hemisphere displayed on the right in axial and coronal slices. Scatterplot reveals percentage signal change in this region as function of negative affect. Bulimia nervosa in blue and healthy controls in red.
Figure 2
Figure 2
Left putamen and insula show stronger positive correlations with amygdala activity in the BN group compared to the healthy controls as a function of seeing the visual cue associated with the milkshake taste versus the cue associated with the tasteless control taste. The same regions showed stronger positive correlations with amygdala activity in healthy controls compared to the BN group as a function of receiving the milkshake taste versus the tasteless control taste. Images are in radiological view on the MNI-152 standard brain, with the left hemisphere displayed on the right in axial and coronal slices.

References

    1. Agras WS, Crow SJ, Halmi KA, Mitchell JE, Wilson GT, Kraemer HC. Outcome Predictors for the Cognitive Behavior Treatment of Bulimia Nervosa: Data From a Multisite Study. American Journal of Psychiatry. 157(8):1302–1308. n.d.
    1. American Psychiatric Association DSM-5 Development. 2010 .
    1. Bohon C, Stice E. Reward abnormalities among women with full and subthreshold bulimia nervosa: A functional magnetic resonance imaging study. International Journal of Eating Disorders. 2011;44(7):585–595. doi:10.1002/eat.20869.
    1. Bohon C, Stice E, Spoor S. Female emotional eaters show abnormalities in consummatory and anticipatory food reward: A functional magnetic resonance imaging study. International Journal of Eating Disorders. 2009;42(3):210–221. doi:10.1002/eat.20615.
    1. Brooks SJ, O'Daly OG, Uher R, Friederich H-C, Giampietro V, Brammer M, Williams SCR, et al. Differential neural responses to food images in women with bulimia versus anorexia nervosa. PloS One. 2011;6(7):e22259. doi:10.1371/journal.pone.0022259.
    1. Bulik CM. Anxiety, depression, and eating disorders. In: Fairburn CG, editor. Eating Disorders and Obesity: A Comprehensive Handbook. Guilford; New York: 2002. pp. 193–198.
    1. Camara E. Functional connectivity of reward processing in the brain. Frontiers in Human Neuroscience. 2008;2 doi:10.3389/neuro.09.019.2008.
    1. Cohen MX, Elger CE, Weber B. Amygdala tractography predicts functional connectivity and learning during feedback-guided decision-making. NeuroImage. 2008;39:1396–1407. doi:10.1016/j.neuroimage.2007.10.004.
    1. Devlin MJ, Steinglass JE. Eating disorders. In: Cutler JL, Marcus ER, editors. Psychiatry. 2nd edn. Oxford University Press; New York: 2010.
    1. Fairburn C, Cooper P. The eating disorders examination. In: Fairburn C, Wilson G, editors. Binge Eating: Nature, Assessment and Treatment. 12th edn. Guilford; New York: 1993. pp. 317–360.
    1. Fairburn CG, Cooper Z, Doll HA, Norman P, O'Connor M. The Natural Course of Bulimia Nervosa and Binge Eating Disorder in Young Women. Arch Gen Psychiatry. 2000;57(7):659–665. doi:10.1001/archpsyc.57.7.659.
    1. Frank GKW, Reynolds JR, Shott ME, O'Reilly RC. Altered Temporal Difference Learning in Bulimia Nervosa. Biological Psychiatry. 2011;70(8):728–735. doi:10.1016/j.biopsych.2011.05.011.
    1. Frank GK, Wagner A, Achenbach S, McConaha C, Skovira K, Aizenstein H, Carter CS, et al. Altered brain activity in women recovered from bulimic□type eating disorders after a glucose challenge: A pilot study. International Journal of Eating Disorders. 2006;39(1):76–79. doi:10.1002/eat.20210.
    1. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. NeuroImage. 1997;6(3):218–229. doi:10.1006/nimg.1997.0291.
    1. Grilo CM, Masheb RM, Wilson GT, Gueorguieva R, White MA. Cognitive–behavioral therapy, behavioral weight loss, and sequential treatment for obese patients with binge-eating disorder: A randomized controlled trial. Journal of Consulting and Clinical Psychology. 2011;79(5):675–685. doi:10.1037/a0025049.
    1. Haedt-Matt AA, Keel PK. Revisiting the affect regulation model of binge eating: A meta-analysis of studies using ecological momentary assessment. Psychological Bulletin. 2011;137(4):660–681. doi:10.1037/a0023660.
    1. Hamann S, Mao H. Positive and negative emotional verbal stimuli elicit activity in the left amygdala. NeuroReport. 2002;13(1):15–19.
    1. Hudson JI, Hiripi E, Pope HG, Jr., Kessler RC. The Prevalence and Correlates of Eating Disorders in the National Comorbidity Survey Replication. Biological Psychiatry. 2007;61(3):348–358. doi:10.1016/j.biopsych.2006.03.040.
    1. Kahnt T, Park SQ, Cohen MX, Beck A, Heinz A, Wrase J. Dorsal Striatal–midbrain Connectivity in Humans Predicts How Reinforcements Are Used to Guide Decisions. Journal of Cognitive Neuroscience. 2009;21:1332–1345. doi:10.1162/jocn.2009.21092.
    1. Koob GF, Le Moal M. Plasticity of reward neurocircuitry and the “dark side” of drug addiction. Nat Neurosci. 2005;8(11):1442–1444. doi:10.1038/nn1105-1442.
    1. Lock J, Le Grange D, Agras WS, Moye A, Bryson SW, Jo B. Randomized Clinical Trial Comparing Family-Based Treatment With Adolescent-Focused Individual Therapy for Adolescents With Anorexia Nervosa. Arch Gen Psychiatry. 2010;67(10):1025–1032. doi:10.1001/archgenpsychiatry.2010.128.
    1. Martin LE, Holsen LM, Chambers RJ, Bruce AS, Brooks WM, Zarcone JR, Butler MG, et al. Neural Mechanisms Associated With Food Motivation in Obese and Healthy Weight Adults. Obesity. 2009;18(2):254–260.
    1. Miyake Y, Okamoto Y, Onoda K, Shirao N, Okamoto Y, Otagaki Y, Yamawaki S. Neural processing of negative word stimuli concerning body image in patients with eating disorders: An fMRI study. NeuroImage. 2010;50(3):1333–1339. doi:10.1016/j.neuroimage.2009.12.095.
    1. Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. doi:10.1016/0028-3932(71)90067-4.
    1. Parrish TB, Gitelman DR, LaBar KS, Mesulam M, □Marsel Impact of signal□to□noise on functional MRI. Magnetic Resonance in Medicine. 2000;44(6):925–932. doi:10.1002/1522-2594(200012)44:6<925::AID-MRM14>;2-M.
    1. Peciña S, Schulkin J, Berridge K. Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress? BMC Biology. 2006;4(1):8. doi:10.1186/1741-7007-4-8.
    1. Robinson JL, Laird AR, Glahn DC, Lovallo WR, Fox PT. Metaanalytic connectivity modeling: Delineating the functional connectivity of the human amygdala. Human Brain Mapping. 2010;31(2):173–184. doi:10.1002/hbm.20854.
    1. Rothemund Y, Preuschhof C, Bohner G, Bauknecht H-C, Klingebiel R, Flor H, Klapp BF. Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. NeuroImage. 2007;37(2):410–421. doi:10.1016/j.neuroimage.2007.05.008.
    1. Roy AK, Shehzad Z, Margulies DS, Kelly AMC, Uddin LQ, Gotimer K, Biswal BB, et al. Functional connectivity of the human amygdala using resting state fMRI. NeuroImage. 2009;45(2):614–626. doi:10.1016/j.neuroimage.2008.11.030.
    1. Schacter SC. Studies of handedness and anomalous dominance. In: Galaburda AM, editor. Dyslexia and Development. Harvard University Press; Cambridge, MA: 1993. pp. 269–296.
    1. Schienle A, Schäfer A, Hermann A, Vaitl D. Binge-Eating Disorder: Reward Sensitivity and Brain Activation to Images of Food. Biological Psychiatry. 2009;65(8):654–661. doi:10.1016/j.biopsych.2008.09.028.
    1. Stice E, Bohon C. Eating Disorders. In: Beauchaine TP, Hinshaw SP, editors. Child and Adolescent Psychopathology. 2nd ed. Wiley; Hoboken, NJ: in press.
    1. Stice E, Fisher M, Martinez E. Eating Disorder Diagnostic Scale: Additional Evidence of Reliability and Validity. Psychological Assessment. 2004;16:60–71. doi:10.1037/1040-3590.16.1.60.
    1. Stice E, Marti CN, Shaw H, Jaconis M. An 8-year longitudinal study of the natural history of threshold, subthreshold, and partial eating disorders from a community sample of adolescents. Journal of Abnormal Psychology. 2009;118:587–597. doi:10.1037/a0016481.
    1. Stice E, Shaw H, Burton E, Wade E. Dissonance and healthy weight eating disorder prevention programs: A randomized efficacy trial. Journal of Consulting and Clinical Psychology. 2006;74(2):263–275. doi:10.1037/0022-006X.74.2.263.
    1. Stice E, Spoor S, Bohon C, Small DM. Relation Between Obesity and Blunted Striatal Response to Food Is Moderated by TaqIA A1 Allele. Science. 2008;322(5900):449–452. doi:10.1126/science.1161550.
    1. Stice E, Telch CF, Rizvi SL. Development and validation of the Eating Disorder Diagnostic Scale: A brief self-report measure of anorexia, bulimia, and binge-eating disorder. Psychological Assessment. 2000;12(2):123–131. doi:10.1037/1040-3590.12.2.123.
    1. Stice E, Yokum S, Bohon C, Marti N, Smolen A. Reward circuitry responsivity to food predicts future increases in body mass: Moderating effects of DRD2 and DRD4. NeuroImage. 2010a;50(4):1618–1625. doi:10.1016/j.neuroimage.2010.01.081.
    1. Stoeckel LE, Weller RE, Cook EW, III, Twieg DB, Knowlton RC, Cox JE. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage. 2008;41(2):636–647. doi:10.1016/j.neuroimage.2008.02.031.
    1. Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, Tye KM, et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature. 2011;475(7356):377–380. doi:10.1038/nature10194.
    1. Tomasi D, Volkow ND. Association between Functional Connectivity Hubs and Brain Networks. Cerebral Cortex. 2011 doi:10.1093/cercor/bhq268.
    1. Uher R, Murphy T, Brammer MJ, Dalgleish T, Phillips ML, Ng VW, Andrew CM, et al. Medial Prefrontal Cortex Activity Associated With Symptom Provocation in Eating Disorders. American Journal of Psychiatry. 2004;161(7):1238–1246.
    1. Veldhuizen MG, Bender G, Constable RT, Small DM. Trying to Detect Taste in a Tasteless Solution: Modulation of Early Gustatory Cortex by Attention to Taste. Chemical Senses. 2007;32(6):569–581. doi:10.1093/chemse/bjm025.
    1. Watson D, Clark LA. Affects separable and inseparable: On the hierarchical arrangement of the negative affects. Journal of Personality and Social Psychology. 1992;62(3):489–505. doi:10.1037/0022-3514.62.3.489.
    1. Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality and Social Psychology. 1988;54:1063–1070. doi:10.1037/0022-3514.54.6.1063.
    1. Yin HH, Knowlton BJ. The role of the basal ganglia in habit formation. Nat Rev Neurosci. 2006;7(6):464–476. doi:10.1038/nrn1919.
    1. Zanarini MC, Frankenburg FR. Attainment and maintenance of reliability of axis I and II disorders over the course of a longitudinal study. Comprehensive Psychiatry. 2001;42:369–374. doi:10.1053/comp.2001.24556.
    1. Zanarini MC, Skodol AE, Bender D, Dolan R, Sanislow C, Schaefer E, Morey LC, et al. The Collaborative Longitudinal Personality Disorders Study: Reliability of Axis I and II Diagnoses. Journal of Personality Disorders. 2000;14:291–299. doi:10.1521/pedi.2000.14.4.291.

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