Research reportMidbrain response to milkshake correlates with ad libitum milkshake intake 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
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Acknowledgment: This work was supported by NIH Grant RO1K085579.