Elsevier

Appetite

Volume 60, 1 January 2013, Pages 168-174
Appetite

Research report
Midbrain response to milkshake correlates with ad libitum milkshake intake in the absence of hunger

https://doi.org/10.1016/j.appet.2012.09.032Get rights and content

Abstract

There is now widespread agreement that individual variation in the neural circuits representing the reinforcing properties of foods may be associated with risk for overeating and obesity. What is currently unknown is how and whether brain response to a food is related to immediate subsequent intake of that food. Here we used functional magnetic resonance imaging (fMRI) to test whether response to a palatable milkshake is associated with subsequent ad libitum milkshake consumption. We predicted that enhanced responses in key reward regions (insula, striatum, midbrain, medial orbitofrontal cortex) and decreased responses in regions implicated in self-control (lateral prefrontal and lateral orbitofrontal cortex) would be associated with greater intake. We found a significant positive association between response to milkshake in the periaqueductal gray region of the midbrain and ad libitum milkshake intake. Although strong bilateral insular responses were observed during consumption of the milkshake this response did not correlate with subsequent intake. The associations observed in the midbrain and orbitofrontal cortex were uninfluenced by ratings of hunger, which were near neutral. We conclude that midbrain response to a palatable food is related to eating in the absence of hunger.

Highlights

Periaqueductal gray response to milkshake is correlated with subsequent milkshake intake. ► This relationship is not influenced by ratings of hunger, BMI, or eating style. ► Insular response to milkshake is not correlated with subsequent milkshake intake.

Introduction

The hedonic properties of food can drive the motivation to eat beyond homeostatic energy needs (Kenney, 2011, Zheng et al., 2009). In an early neuroimaging study of feeding we showed that response to chocolate consumption in the insula/operculum, midbrain, striatum, and medial orbitofrontal cortex decreased as motivation to consume the chocolate decreased, whereas response in the lateral orbitofrontal cortex and lateral prefrontal cortex increased (Small, Zatorre, Dagher, Evans, & Jones-Gotman, 2001). We suggested that these two circuits governed meal initiation and meal termination, respectively.

Since this time functional neuroimaging studies have elucidated brain response to food pictures, odors and flavors across differing internal states (Cornier et al., 2007, Frank et al., 2010, Führer et al., 2008, Goldstone et al., 2009, La Bar et al., 2001, Malik et al., 2008, O’Doherty et al., 2000, Siep et al., 2009), body weights (Rothemund et al., 2007, Stice et al., 2008, Stice et al., 2008, Stoeckel et al., 2008), eating phenotypes (e.g. restraint, food addiction) (Beaver et al., 2006, Demos et al., 2011, Lowe et al., 2009) and as a function of prospective weight gain (Stice et al., 2010, Stice et al., 2008, Stice et al., 2008) or loss (Cornier, Melanson, Salzberg, Bechtell, & Tregellas, 2012). Enhanced responses in regions thought to represent the reinforcing properties of foods, such as the insula/operculum, midbrain, medial orbitofrontal cortex, striatum and insula are associated with higher body mass index (BMI) (Rothemund et al., 2007, Stice et al., 2008, Stice et al., 2008, Stice et al., 2010, Stoeckel et al., 2008). In contrast, reduced responses in regions critical for inhibitory behavior and self-control, such as the lateral orbitofrontal cortex and lateral prefrontal cortex (Hare et al., 2011, Hollmann et al., 2012) are often associated with higher BMI (Batterink et al., 2010, Volkow et al., 2009). There is also evidence for reduced gray matter density in lateral prefrontal cortex in obesity (Pannacciulli et al., 2006). Consequently, an important theme to emerge is that heightened reward responses, coupled with decreased inhibitory control, increase risk for overeating and weight gain (Del Parigi et al., 2003, Small, 2009, Volkow and Wise, 2005). What is less understood is how brain response to a food relates to subsequent intake of that food. Batterham and colleagues showed that the neural activity recorded during an fMRI scan could predict subjects’ subsequent caloric intake (Batterham et al., 2007). However the scanning paradigm was unrelated to the test meal as no food or food-related cues were presented during scanning. This is an important issue because the relationship between brain response to a food and its subsequent intake is presumably an important mediator of the relationship between brain response to food and body weight.

The aim of the current fMRI study was to address this gap in the literature by identifying regions in which response to a palatable and energy-dense milkshake is associated with the immediate subsequent intake of that milkshake in non-deprived individuals who self-report being neither hungry nor full. We reasoned that there would be automatic engagement of circuits coding the appetitive aspects of the stimulus as well as circuits representing inhibitory control in the face of consuming a palatable food. An overarching prediction was that greater responses in brain regions representing the reinforcing properties of foods would be positively associated with intake while reduced responses in regions representing response inhibition and self-control would be negatively associated with intake.

Section snippets

Subjects

Twenty-three right-handed nonsmokers, taking no daily medication and having no known history of loss of consciousness, chemosensory impairment, neurological, or psychiatric disorders, gave written informed consent to participate in our study that was approved by Yale University School of Medicine Human Investigation Committee. Two subjects were excluded because of excessive movement during scanning, which was defined as greater than 2 mm movement in any direction. An additional subject was

Behavioral results

Average hunger and fullness ratings were near neutral before and after scanning ((mean ± SEM) hunger before scan: 8.92 ± 6.83; hunger after scan: 12.24 ± 7.21; fullness before scan: −14.95 ± 7.98; fullness after scan: −19.20 ± 7.14) and did not differ as a function of time (hunger, F(1, 19) = 0.345, p = 0.564; fullness, F(1, 19) = 0.231, p = 0.636). Before and after scanning, the milkshake was rated as pleasant (before scan: 26.34 ± 3.04; after scan: 25.19 ± 3.05 – note that a score of 17 corresponds to “like

Discussion

The primary aim of this study was to test whether response to tasting small quantities of milkshake predicts subsequent milkshake intake in subjects who report being neither hungry nor full. In other words, we wished to isolate regions of the brain that might promote eating in the absence of hunger. Our primary prediction was that enhanced responses in the midbrain, insula, striatum and medial OFC and decreased responses in lateral OFC and lateral prefrontal cortex to the taste of milkshake

References (70)

  • P.M. Macey et al.

    A method for removal of global effects from fMRI time series

    NeuroImage

    (2004)
  • J.A. Maldjian et al.

    An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets

    NeuroImage

    (2003)
  • S. Malik et al.

    Ghrelin modulates brain activity in areas that control appetitive behavior

    Cell Metabolism

    (2008)
  • A. Mansour et al.

    Opioid-receptor mRNA expression in the rat CNS. Anatomical and functional implications

    Trends in Neuroscience

    (1995)
  • A. Mansour et al.

    Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS

    Journal of Chemical Neuroanatomy

    (1995)
  • V. Napadow et al.

    Automated brainstem co-registration (ABC) for MRI

    NeuroImage

    (2006)
  • N. Pannacciulli et al.

    Brain abnormalities in human obesity. A voxel-based morphometric study

    NeuroImage

    (2006)
  • Y. Rothemund et al.

    Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals

    NeuroImage

    (2007)
  • Y.B. Shah et al.

    Detection of cannabinoid agonist evoked increase in BOLD contrast in rats using functional magnetic resonance imaging

    Neuropharmacology

    (2004)
  • N. Siep et al.

    Hunger is the best spice. An fMRI study of the effects of attention, hunger and calorie content on food reward processing in the amygdala and orbitofrontal cortex

    Behavioural Brain Research

    (2009)
  • D.M. Small et al.

    Dissociation of neural representation of intensity and affective valuation in human gustation

    Neuron

    (2003)
  • E. Stice et al.

    Reward circuitry responsivity to food predicts increases in body mass. Moderating effects of DRD2 and DRD4

    NeuroImage

    (2010)
  • L.E. Stoeckel et al.

    Widespread reward-system activation in obese women in response to pictures of high calorie foods

    NeuroImage

    (2008)
  • A.J. Stunkard et al.

    The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger

    Journal of Psychosomatic Research

    (1985)
  • C.M. Williams et al.

    Hyperphagia in pre-fed rats following oral [DELTA]9-THC

    Physiology & Behavior

    (1998)
  • M.R. Yeomans et al.

    Selective effects of naltrexone on food pleasantness and intake

    Physiology & Behavior

    (1996)
  • M.R. Yeomans et al.

    Opiod peptides and the control of human ingestive behavior

    Neuroscience Biobehavioral Reviews

    (2002)
  • E.L. Abel

    Effects of marihuana on solution of anagrams, memory and appetite

    Nature

    (1971)
  • R.L. Batterham et al.

    PYY modulation of cortical and hypothalamic brain areas predicts feeding behavior in humans

    Nature

    (2007)
  • J.D. Beaver et al.

    Individual differences in reward drive predict neural responses to images of food

    The Journal of Neuroscience

    (2006)
  • C.A. Davis et al.

    Dopamine for “wanting” and opiods for “liking”. A comparison of obese adults with and without binge eating

    Obesity

    (2009)
  • A. Del Parigi et al.

    Persistence of abnormal neural responses to a meal in postobese individuals

    International Journal of Obesity

    (2004)
  • A. Del Parigi et al.

    Are we addicted to food?

    Obesity

    (2003)
  • K.E. Demos et al.

    Dietary restraint violations influence reward responses in nucleus accumbens and amygdala

    Journal of Cognitive Neuroscience

    (2011)
  • J.A. Flores et al.

    Role for dopamine neurons of the rostral linear nucleus and periaqueductal gray in the rewarding and sensitizing properties of heroin

    Neuropsychopharmacology

    (2006)
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    Acknowledgment: This work was supported by NIH Grant RO1K085579.

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