Hunger does not motivate reward in women remitted from anorexia nervosa

Abstract

Background: Hunger enhances sensitivity to reward, yet individuals with anorexia nervosa (AN) are not motivated to eat when starved. This study investigated brain response to rewards during hunger and satiated states to examine whether diminished response to reward could underlie food restriction in AN.

Methods: Using a delay discounting monetary decision task known to discriminate brain regions contributing to processing of immediate rewards and cognitive control important for decision making regarding future rewards, we compared 23 women remitted from AN (RAN group; to reduce the confounding effects of starvation) with 17 healthy comparison women (CW group). Monetary rewards were used because the rewarding value of food may be confounded by anxiety in AN.

Results: Interactions of Group (RAN, CW) × Visit (hunger, satiety) revealed that, for the CW group, hunger significantly increased activation in reward salience circuitry (ventral striatum, dorsal caudate, anterior cingulate cortex) during processing of immediate reward, whereas satiety increased activation in cognitive control circuitry (ventrolateral prefrontal cortex, insula) during decision making. In contrast, brain response in reward and cognitive neurocircuitry did not differ during hunger and satiety in the RAN group. A main effect of group revealed elevated response in the middle frontal gyrus for the RAN group compared with the CW group.

Conclusions: Women remitted from AN failed to increase activation of reward valuation circuitry when hungry and showed elevated response in cognitive control circuitry independent of metabolic state. Decreased sensitivity to the motivational drive of hunger may explain the ability of individuals with AN to restrict food when emaciated. Difficulties in valuating emotional salience may contribute to inabilities to appreciate the risks inherent in this disorder.

Keywords: Anorexia nervosa; Decision making; Delay discounting; Eating disorders; Functional MRI; Reward processing.

Conflict of interest statement

FINANCIAL DISCLOSURES

All authors report no biomedical financial interests or potential conflicts of interest.

Copyright © 2015 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Figures

Figure 1

Line graphs reflecting self-report Likert visual analog scale values. Line graph of pre- and post-scan self-report measures of hunger shows a main effect of visit [F(1,111)=123.2, p<0.001, d=3.6] and of interval [F(1,111)=12.7, p=<0.001, d=1.1] resulting from a group (RAN, CW) × visit (Hungry, Satiated) × interval period (pre-scan, post-scan) LME. Participants reported greater hunger during the hungry condition relative to the satiated condition [z=6.0, p<0.001]; participants also tended to be more hungry at the post-scan interval relative to the pre-scan interval [z=1.8, p=0.08]. Error bars represent the standard error. CW: healthy comparison women; RAN: women recovered from anorexia nervosa.

Figure 2

Plots showing group differences in behavioral choice and their modulation by satiety. Hard choices were defined as those in which the probability of choosing the smaller-sooner was approximately 50%, and corresponded to difference in dollar amounts between 10 and 15%; all other choices were defined as easy. A) We examined the probability of choosing the early reward with respect to the percent difference in amount between the early and later choices. Participants showed a main effect of percent difference [F(2,190)=173.0, p<0.001, d=4.2], such that participants were less likely to choose the early option as the percent monetary difference between choices grew larger [3–5% – 10–15%: z=3.1, p=0.006; 3–5% – 25–35%: z=7.8, p<0.001; 10–15% – 25–35%: z=4.7, p<0.001]. There was also a significant interaction of group with visit [F(1,190)=4.2, p=0.04, d=0.7], but the post hoc analyses were not significant [all p>0.6]. B) For reaction time, there was a main effect of visit [F(1,114)=5.1, p=0.03, d=0.7], with participants showing a tendency for faster response times when hungry than when satiated [z=1.7, p=0.09]. There was also a trend for an interaction of group with satiety [F(1,114)=3.0, p=0.09, d=0.6]. Post hoc analyses found that this was due to CW having a faster response time when hungry [z=2.8, p=0.02]. RAN did not show this effect. RAN: women recovered from anorexia nervosa; CW: healthy comparison women.

Figure 3

Plots demonstrating a significant group × visit interaction within representative regions of interest. A) Valuation-related ROIs for the beta (“Today”) regressor. Left: Within the right dorsal anterior caudate, CW had an elevated response when hungry relative to when satiated [z=2.8, p=0.02], and, when satiated, RAN had a greater response relative to CW [z=3.2, p=0.008]. Middle: Within the rostral zone of the left anterior cingulate, CW had an elevated response when hungry relative to when satiated [z=2.4, p=0.07], and, when satiated, RAN had a greater response relative to CW [z=3.3, p=0.01]. Right: Within the right ventral striatum, CW had a greater response when hungry than when satiated [z=2.7, p=0.04], and RAN had a greater response than CW when satiated [z=2.8, p=0.03]. B) Cognitive-related ROIs for the delta (“All Decisions”) regressor. Left: Within the left middle frontal gyrus, CW responded more strongly when hungry than when satiated [z=2.6, p=0.04], and RAN responded more robustly than CW when satiated [z=2.7, p=0.03]. Middle: Within the right ventrolateral prefrontal cortex, CW responded more strongly when satiated than when hungry [z=2.9, p=0.02]. Right: Within the left insula, CW responded more strongly when satiated than when hungry [z=3.6, p=0.002]. Error bars represent the standard error for each group. CW: healthy comparison women; RAN: women remitted from anorexia nervosa. *p<0.05; **p<0.01.

Figure 4

Regions of interest associated with cognition showing a main effect of group for the delta regressor. A) Within the left middle frontal gyrus, RAN responded more robustly than CW [z=2.8, p=0.005]. B) Similarly, RAN responded more robustly than CW within the right middle frontal gyrus [z=2.9, p=0.004]. Error bars represent the standard error for each group. CW: healthy comparison women; RAN: women remitted from anorexia nervosa. **p<0.01

Figure 5

Regions of interest associated with cognition showing a main effect of visit for the delta regressor. A) Within the left middle frontal gyrus, there was a significantly greater response when satiated than when hungry [z=2.9, p=0.004]. B) Within the left ventrolateral prefrontal cortex, there was a greater response when participants were satiated than when hungry [z=2.8, p=0.005]. C) Similarly, participants exhibited a greater response within the left insula when satiated than when hungry [z=3.6, p<0.001]. Error bars represent the standard error for each group. **p<0.01; ***p<0.001.