Neural activation during anticipated peer evaluation and laboratory meal intake in overweight girls with and without loss of control eating

Abstract

The interpersonal model of loss of control (LOC) eating proposes that socially distressing situations lead to anxious states that trigger excessive food consumption. Self-reports support these links, but the neurobiological underpinnings of these relationships remain unclear. We therefore examined brain regions associated with anxiety in relation to LOC eating and energy intake in the laboratory. Twenty-two overweight and obese (BMIz: 1.9±0.4) adolescent (15.8±1.6y) girls with LOC eating (LOC+, n=10) and without LOC eating (LOC-, n=12) underwent functional magnetic resonance imaging (fMRI) during a simulated peer interaction chatroom paradigm. Immediately after the fMRI scan, girls consumed lunch ad libitum from a 10,934-kcal laboratory buffet meal with the instruction to "let yourself go and eat as much as you want." Pre-specified hypotheses regarding activation of five regions of interest were tested. Analysis of fMRI data revealed a significant group by peer feedback interaction in the ventromedial prefrontal cortex (vmPFC), such that LOC+ had less activity following peer rejection (vs. acceptance), while LOC- had increased activity (p<.005). Moreover, functional coupling between vmPFC and striatum for peer rejection (vs. acceptance) interacted with LOC status: coupling was positive for LOC+, but negative in LOC- (p<.005). Activity of fusiform face area (FFA) during negative peer feedback from high-value peers also interacted with LOC status (p<.005). A positive association between FFA activation and intake during the meal was observed among only those with LOC eating. In conclusion, overweight and obese girls with LOC eating may be distinguished by a failure to engage regions of prefrontal cortex implicated in emotion regulation in response to social distress. The relationship between FFA activation and food intake supports the notion that heightened sensitivity to incoming interpersonal cues and perturbations in socio-emotional neural circuits may lead to overeating in order to cope with negative affect elicited by social discomfort in susceptible youth.

Keywords: Adolescents; Anxiety; Food intake; Loss of control eating; Neural activation; Social distress.

Published by Elsevier Inc.

Figures

Figure 1

Depiction of the Chatroom Social Stress Task. A. Participants are asked to categorize peers as 1) high-value: peers with whom they were interested in chatting; and 2) low-value: peers with whom they were not interested in chatting. B. During the fMRI scan, participants learn if their peers are or are not interested in them.

Figure 2

Significant clusters for the interaction between group and feedback type A. Ventromedial prefrontal cortex (1, 43, −5; ke = 41, F = 35.51). B. Decomposition showed that both groups responded similarly to positive feedback (t(20)= −.63, p = ns), but negative feedback elicited diminished engagement in LOC+ and heighted engagement for LOC− (t(20)=3.40, p <.005). C. Ventrolateral prefrontal cortex (−14, 51, 40, ke = 61, F = 15.71). D. Decomposition showed that while LOC− responded similarly to positive and negative feedback (t(10)= −1.74, p = ns), LOC+ had heightened activity to positive, relative to negative feedback (t(9)=5.34, p = <.001).

Figure 3

Psychophysiological interaction analysis with ventromedial prefrontal cortex (vmPFC) showed functional connectivity between vmPFC and striatum (putamen; −24, −4, −5; ke = 35) varied by peer feedback and group. Negative, relative to positive, feedback, resulted in negative mPFC-striatal coupling in LOC− (t(11)= −2.79, p < .05), but positive coupling in LOC+ (t(9)=4.92, p < .005).

Figure 4

Group differences during feedback from high-value peers (Fisher’s r-to-z’s: Right = −2.40; p < .05; Left = −2.22; p < .05). For LOC+, greater fusiform face area (FFA) activity during negative, relative to positive feedback, from high-value peers was positively associated with greater energy intake during the subsequent test meal (r’s: Right = .76, p = .01; Left = .48, p = ns). For LOC−, FFA activity during peer feedback did not relate to subsequent energy intake (r’s: Right = .27, p = ns; Left = −.54, p = ns).