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Physiology & Behavior
journal homepage: www.elsevier.com/locate/physbeh
The impact of elevated body mass on brain responses during appetitive
prediction error in postpartum women
Grace E. Shearrer
a
, Tonja R. Nansel
b
, Leah M. Lipsky
b
, Jennifer R. Sadler
a
, Kyle S. Burger
a,c,
⁎
a
Department of Nutrition, University of North Carolina at Chapel Hill, Chapel Hill, NC, United States of America
b
Social and Behavioral Sciences Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health & Human
Development, Bethesda, MD, United States of America
c
Biomedical Research Imaging Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, United States of America
ARTICLE INFO
Keywords:
Functional MRI
Reward, obesity
Prediction error
ABSTRACT
Repeated exposure to highly palatable foods and elevated weight promote: 1) insensitivity to punishment in
striatal regions and, 2) increased willingness to work for food. We hypothesized that BMI would be positively
associated with negative prediction error BOLD response in the occipital cortex. Additionally, we postulated that
food reinforcement value would be negatively associated with negative prediction error BOLD response in the
orbital frontal cortex and amygdala. Postpartum women (n = 47; BMI = 25.5 ± 5.1) were ‘trained’ to associate
specific cues paired to either a highly palatable milkshake or a sub-palatable milkshake. We then violated these
cue-taste pairings in 40% of the trials by showing a palatable cue followed by the sub-palatable taste (negative
prediction error). Contrary to our hypotheses, during negative prediction error (mismatched cue-taste) versus
matched palatable cue-taste, women showed increased BOLD response in the central operculum (pFWE = 0.002;
k = 1680; MNI: -57, -7,14) and postcentral gyrus (pFWE = 0.006, k = 1219; MNI: 62, -8,18). When com-
paring the matched sub-palatable cue-taste to the negative prediction error trials, BOLD response increased in
the postcentral gyrus (r = -0.60, pFWE = 0.008), putamen (r = -0.55, pFWE = 0.02), and insula (r = -0.50,
pFWE = 0.01). Similarly, viewing the palatable cue vs sub-palatable cue was related to BOLD response in the
putamen (pFWE = 0.025, k = 53; MNI: -20, 6, -8) and the insula (pFWE = 0.04, k = 19, MNI:38, -12, -6).
Neither BMI at 6-month postpartum nor food reinforcement value was related to BOLD response. The insula and
putamen appear to encode for visual food cue processing, and the gustatory and somatosensory cortices appear
to encode negative prediction errors. Differential response in the somatosensory cortex to the matched cue-taste
pairs to negative prediction error may indicate that a palatable cue may dull aversive qualities in the stimulus.
1. Introduction
Increased energy needs and weight gain characterize pregnancy [1].
However, in the last two decades pregnancy weight retention has be-
come a risk factor for future development of obesity in both the mother
and child [2–7]. Despite substantial evidence of the negative con-
sequences of postpartum weight retention, interventions have been
generally unsuccessful [8,9]. Desire to consume palatable foods is a
noted barrier to weight loss in women [10] and overconsumption of
palatable foods has been linked overweight and obese status [11].
Understanding the desire and motivation to over consume palatable
foods may inform the development of more effective intervention
strategies.
Intake of palatable food, a hedonic reward, is a multidimensional
behavior comprised of learning, incentive motivation, and pleasure
[12]. While the expected value of a stimulus [13], salience of both a cue
and a stimulus [13] are important components of learning; Mirenowicz
and Schultz’ prediction error theory posits that the brain learns about
rewarding stimuli through coding unexpected outcomes as pleasurable
or unpleasant if they are better or worse than the expected respectively
[14,15]. As a simple example, consider a tray of cookies that appear to
be chocolate chip. However, upon biting into a cookie one realizes that
it is in fact an oatmeal raisin cookie, a flavor the individual does not
enjoy. As the person dislikes oatmeal raisin cookies, but was expecting a
highly pleasant chocolate chip cookie, she/he experienced negative
prediction error; characterized as an anticipated pleasant outcome that,
when experience, is worse than expected. As a function of this re-
inforcing learning experience, the person now has learned that this tray
of cookies contains different cookies and cookie selection requires
closer attention. As such, prediction errors act to update the brain with
https://doi.org/10.1016/j.physbeh.2019.04.009
Received 30 November 2018; Received in revised form 11 April 2019; Accepted 11 April 2019
⁎
Corresponding author at: 2212 McGravran-Greenberg Hall, CB 7461, Chapel Hill, NC 27599, United States of America
E-mail address: kyle_burger@unc.edu (K.S. Burger).
Physiology & Behavior 206 (2019) 243–251
Available online 13 April 2019
0031-9384/ © 2019 Published by Elsevier Inc.
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