Elsevier

Appetite

Volume 57, Issue 2, October 2011, Pages 421-434
Appetite

Research report
Males and females show differential brain activation to taste when hungry and sated in gustatory and reward areas

https://doi.org/10.1016/j.appet.2011.06.009Get rights and content

Abstract

Although males and females differ in eating behavior and prevalence rates for eating disorders and obesity, little is known about gender differences in cortical activation to pleasant and unpleasant pure tastes during the physiological states of hunger and satiety. Twenty-one healthy young adults (12 females and 9 males) underwent two functional magnetic resonance imaging scans. Using four pure tastants of differing qualities (i.e., salty, sour, bitter, sweet), the present study examined gender differences in fMRI activation during two motivational states (hunger and satiety). There was greater change in fMRI activation from hunger to satiety in males than females in response to all tastes within the middle frontal gyrus (BA 10), insula, and cerebellum. Males also had greater change in activation from hunger to satiety, relative to females, in limbic regions including dorsal striatum, amygdala, parahippocampal gyrus, and posterior and anterior cingulate; however, activation was stimulus dependent, despite equivalent ratings in perceived pleasantness and intensity. Interestingly, males and females showed significant change from hunger to satiety in response to citric acid, suggesting that in addition to gender and physiological condition, stimulus quality is an important factor in taste fMRI activation. These gender differences may have implications for the pathophysiology of eating disorders and obesity.

Highlights

► Females demonstrated greater brain activation when hungry and sated, relative to males. ► Females showed less change in brain activation from hunger to satiety than males. ► These differences may provide insight into the mechanisms of disordered eating.

Introduction

Gender differences in eating behavior have been widely documented (Conner et al., 2004, Fagerli and Wandel, 1999, Rolls et al., 1991, Wardle et al., 2004, Zylan, 1996). Clinical manifestations of eating disorders such as bulimia and anorexia nervosa have greater incidence rates among females relative to males (Jacobi et al., 2004, Kjelsas et al., 2004, Woodside et al., 2001) and prevalence of obesity is greater in females (Flegal, Carroll, & Odgen, 2010). Males and females differ in caloric intake (Basiotis, Thomas, Kelsay, & Mertz, 1989), which may in part, be a result of differential eating styles (Green, 1987, Hill and McCutcheon, 1984, Mori and Pliner, 1987). In addition, differential cultural pressures to achieve ideal body shapes may influence the way males and females respond to food to a different degree (Ostovich and Rozin, 2004, Rolls et al., 1991, Rozin et al., 2001).

Food consumption and termination are regulated by a complex system of peripheral and central processes that interact with genetics and environmental factors (Lenard & Berthoud, 2008). The gustatory system is one of the first sensory systems involved in food intake. Interestingly, gustatory psychophysical experiments examining gender differences have been inconsistent (Enns et al., 1979, Robin et al., 2003). Enns et al. (1979) found that while males and females reported identical perceptions of sucrose intensity (using subjective ratings), hedonic evaluations were significantly different. In particular, males perceived higher concentrations of sucrose as more pleasant when compared to females. Conversely, other studies have reported no significant gender differences in the perceived pleasantness of taste stimuli (sweet, sour, salty, bitter; Robin, Rousmans, Dittmar, & Vernet-Maury, 2003) or in the perceived pleasantness and intensity of calcium (Leshem, Katz-Levin, & Schulkin, 2003).

Gender differences in the psychophysical evaluation of taste stimuli are more consistently observed when hunger and satiety are controlled (Laeng, Berridge, & Butter, 1993). Females perceive the sweetness of sucrose as more intense relative to males across physiological condition, and also perceive sucrose as less pleasant than males after a meal (Laeng et al., 1993). Additionally, females rate food images as more pleasant than males after a 12-h fast, and less pleasant than males in a non-fasted condition (Stoeckel, Cox, Cook, & Weller, 2007). Although inconclusive, these findings suggest that physiological state may alter the subjective pleasantness of food-related stimuli to a greater extent in females than males.

Although neuroimaging studies have reported significant gender differences in brain activation during the physiological conditions of hunger and satiety in response to flavor (Del Parigi et al., 2002, Smeets et al., 2006) and food pictures (Cornier et al., 2010, Frank et al., 2010, Uher et al., 2006), to date, no study has examined gender differences during hunger and satiety in response to pure tastes.

The perceived valence of a stimulus (e.g., pleasant or unpleasant) modulates patterns of cortical activation. In regard to chemosensory stimuli, valence specific brain activation has been localized within emotion processing regions such as the orbital frontal cortex (OFC) and amygdala (Francis et al., 1999, Kringelbach et al., 2003, O’Doherty et al., 2001, Small et al., 2001, Zald et al., 2002). Findings from research involving other sensory modalities demonstrate that valence-specific activation is further influenced by gender. Specifically, gender differences have been reported in response to stimuli with various affective characteristics including olfaction (Berglunds et al., 2006, Levy et al., 1997, Royet et al., 2003, Savic et al., 2005, Yousem et al., 1999), visual cues (Killgore and Yurgelun-Todd, 2010, Klein et al., 2003, Schienle et al., 2005, Wrase et al., 2003), happiness and sadness (Azim et al., 2005, Schneider et al., 2000), and unpleasant words associated with body image (Shirao, Okamoto, Mantani, Okamoto, & Yamawaki, 2005). While the direction of gender effects across experiments vary, consistent differences in activation are observed within the inferior frontal gyrus (IFG), anterior cingulate cortex (ACC), and amygdala.

We have previously shown that the physiological conditions of hunger and satiety influence brain activation in young (Haase, Cerf-Ducastel, & Murphy, 2009) and older adults (Jacobson, Green, & Murphy, 2010) in response to pure taste stimuli. However, gender differences in brain activation during hunger and satiety in response to pure taste stimuli have yet to be examined. Additionally, it is unknown what role gender has in cortical activation in response to pleasant and unpleasant taste stimuli. Therefore, one aim of the present event-related fMRI study was to investigate gender differences in cortical fMRI activation in response to pure taste stimuli when subjects were hungry or satiated. In addition, using this experimental design we have previously reported decreases in fMRI activation in regions implicated in emotion and modulation of eating behavior (e.g., amygdala, hypothalamus, inferior insula, orbitofrontal cortex; Haase et al., 2009), so we also examined gender differences in the change in brain activation from hunger to satiety.

Section snippets

Methods

A more detailed description of the materials and methods used in this study can be found in Haase, Cerf-Ducastel, Buracas, and Murphy (2007), in the Journal of Neuroscience Methods.

Demographics

Independent samples t-tests were conducted to examine potential differences in demographic characteristics [dependent variables: age, weight (kg), height (CM), body mass index (BMI), cognitive restraint as measured by the Three Factor Eating Questionnaire (TFEQ), odor and taste thresholds, hunger before and after each scan] between males and females (Table 1). As expected, males were significantly taller and weighed significantly more than females. There were no significant differences between

Discussion

The first aim of the present study was to examine potential gender differences in brain activation to taste stimuli during the physiological conditions of hunger and satiety. As expected, there was considerable overlap in the cortical regions activated in males and females, including gustatory, memory, and reward processing regions. However, significant differences in brain activation were also observed, which varied as a function of gender, physiological condition, and stimulus quality.

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    We acknowledge and thank Drs. Barbara Cerf-Ducastel and Nobuko Kemmotsu for their fMRI expertise. We thank Aaron Jacobson, Delaney Downer and Lindsay Ramos for their assistance in data analysis. Supported by NIH grant AG04085-24 from the National Institute on Aging to CM.

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