Research reportAsymmetric prefrontal cortex activation in relation to markers of overeating in obese humans
Introduction
Chronic overeating has reached pandemic proportions (CDC, 2006). Such overeating ranges from chronic passive overconsumption (Blundell & MacDiarmid, 1997), to recurrent binge episodes reported in up to 40% of individuals seeking weight loss treatment (Spitzer, Devlin, Walsh, & Hasin, 1992). Theories explaining the propensity to overeat have been primarily based on behavioral studies and have not yielded effective long-term behavioral interventions. The need for improved methods of examining and conceptualizing the appetitive vulnerabilities that lead to overeating in obese individuals may be, in part, fulfilled by examining the neurobiological correlates of appetitive drive.
Although the investigation of the neural activity associated with appetitive drive remains in its infancy (Chowdhury & Lask, 2001), a relationship between ingestive behavior and activation in the prefrontal cortex (PFC) has emerged (Alonso-Alonso and Pascual-Leone, 2007, Le et al., 2006). Several authors suggest a prominent role of the PFC in the cognitive regulation of food intake (Le et al., 2006, Tataranni and DelParigi, 2003) and further evidence indicates that the (a)symmetry of PFC activation (activation in one, relative to the other, hemisphere of the PFC) may be integral in identifying the specific role of the PFC in appetitive behavior (Andreason et al., 1992, Karhunen et al., 2000, Silva et al., 2002). At rest, individuals typically display relatively symmetrical activation in the PFC (Murphy, Nimmo-Smith, & Lawrence, 2003); however, recent research suggests that individuals reporting disordered eating patterns may experience asymmetry in activation of the PFC or “prefrontal asymmetry” (Andreason et al., 1992, Karhunen et al., 2000, Silva et al., 2002). Obese binge eaters, for example, display greater increases in left-, relative to right-, sided prefrontal asymmetry as compared to lean and obese non-binge eaters following exposure to palatable food (Karhunen et al., 2000). Strong linear correlations were also observed in obese binge eaters between increases in hunger and left-, greater than right-, sided (left-sided) prefrontal asymmetry (Karhunen et al., 2000).
The PFC is proposed to be responsible for instantiating the experience and execution of affect-related behavior (Davidson et al., 2000, Miller and Cohen, 2001). According to the affective theory (Davidson, 2000, Davidson, 2003), emotion results from neural signals in the PFC, separated into two systems: the approach-related positive affect, and withdrawal-related negative affect, systems. Accordingly, the positive affect system is activated as a person moves toward an appetitive goal, while the negative affect system facilitates withdrawal from sources of aversive stimulation (Davidson, 2003, Tomarken et al., 1992). Several neuroimaging studies have related positive affect to left-sided prefrontal asymmetry (Davidson, 2000, Sutton and Davidson, 2000, Tomarken et al., 1992) and negative affect to right-sided prefrontal asymmetry (Davidson et al., 2000, Davidson, 2003, Wheeler et al., 1993).
Based on the proposed relationship between negative affect and right-sided prefrontal asymmetry (Davidson, 2000), and the relationship between negative affect and dietary restraint in normal weight individuals (Sheppard-Sawyer, McNalley, & Fischer, 2000), Silva et al. (2002) hypothesized that restrained eating would be related to right-sided prefrontal asymmetry in a normal weight sample. Dietary restraint and prefrontal asymmetry were assessed using the Restraint Scale (Herman & Polivy, 1980) and EEG imaging (respectively), and results confirmed the proposed hypothesis. However, affect was not found to mediate the relationship between prefrontal asymmetry and Restraint Scale scores, suggesting a relationship between dietary restraint in lean individuals and prefrontal asymmetry independent of affect (Silva et al., 2002).
Silva et al. (2002) additionally suggest that right-sided prefrontal asymmetry may be related to other indicators of disordered eating, such as bulimia. However, bulimic individuals have been shown to display more left-sided PFC activation relative to normal individuals (Andreason et al., 1992) despite the strong association between bulimia and depression (Hinz & Williamson, 1987). Noting other findings inconsistent with the affective model, particularly the relationship between anger (a negative, but approach-related emotion) and left-sided prefrontal asymmetry (Harmon-Jones & Allen, 1997), Harmon-Jones, 2003, Harmon-Jones, 2004 proposed that affective valence (positive–negative) and approach–withdrawal tendencies were two related but distinct constructs. He suggests that left- and right-sided prefrontal asymmetry reflect motivational direction (approach vs. withdrawal, respectively) irrespective of associated affect (Harmon-Jones, 2003, Harmon-Jones, 2004).
The present study was designed to test, in an overweight and obese sample, the primary hypotheses that prefrontal asymmetry would be related to dietary restraint as well as binge eating, disinhibition, hunger and appetitive responsivity and that these relationships would be found independent of affect at the time of assessment. The two competing models of prefrontal asymmetry predicted different outcomes in terms of the directionality of the asymmetry. The affective model would have predicted that dietary restraint, binge eating and disinhibition (appetitive behaviors associated with negative affect; Sheppard-Sawyer et al., 2000, Wardle et al., 2001) would be related to right-sided prefrontal asymmetry. The motivation direction model would also have predicted that dietary restraint (reflecting a withdrawal-like tendency in the absence of disinhibiting stimuli; Herman and Polivy, 1980, Silva et al., 2002) would be associated with right-sided prefrontal asymmetry, but that binge eating, disinhibition, hunger and appetitive responsivity (reflecting approach-like tendencies) would be related to left-sided prefrontal asymmetry. Being the preeminent theory of prefrontal asymmetry, secondary hypotheses regarding the directionality of asymmetry were based on the affective model.
Section snippets
Participants
Forty participants were recruited through physician referral to a weight loss intervention study being conducted at Drexel University in Philadelphia, PA. Participants were told they were being recruited for an unrelated study of brain activity and all participants completed this study prior to any weight loss intervention. Nine female and three male participants either failed to arrive at their scheduled appointment, produced unusable EEG data due to equipment failure, or were eliminated from
Relationships between appetitive and affective measures
Pearson correlations between all self-report measures are shown in Table 3. Unsurprisingly, anhedonic depression [MASQ subscale] was inversely related to positive affect [PANAS subscale], and positively related to negative affect (p < 0.001 and p = 0.043, respectively). Binge eating [BES] was positively related to disinhibition [TFEQ subscale] (p = 0.002) and appetitive responsivity [PFS] (p = 0.005). Disinhibition was also positively related to hunger (p = 0.01) and both disinhibition and hunger were
Discussion
In this overweight and obese sample, measures of dietary restraint, binge eating, disinhibition, hunger, and appetitive responsivity were examined in relation to prefrontal asymmetry and affect at the time of assessment. Dietary restraint was not related to other appetitive measures; however, consistent with previous literature (Cappelleri et al., in press, Marcus et al., 1985), individuals reporting more binge eating also reported greater levels of disinhibition and appetitive responsivity.
Conclusion
Left-sided PFC activation in obese individuals was related to measures of disinhibition, hunger, and appetitive responsivity, but not dietary restraint or binge eating in this overweight and obese sample. In addition, disinhibition was correlated with negative affect (anxiety) and appetitive responsivity was inversely correlated with positive affect; however, affect at the time of assessment was not related to prefrontal asymmetry. These results partially support the proposed relationship
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2016, International Journal of PsychophysiologyCitation Excerpt :Further support for the relation between frontal EEG asymmetries and approach- and avoidance-related behaviour comes from a study showing that restrained eaters display right-sided frontal alpha EEG asymmetry (Silva et al., 2002). In addition, greater left-to-right frontal alpha EEG asymmetries have been found to relate to behavioural disinhibition and increased approach-related responsivity to food in individuals with obesity (Ochner et al., 2009). Thus in addition to the links between eating disorders, reward processing and hedonic valuation of food (Davis et al., 2008; Soussignan et al., 2011; Witt and Lowe, 2014), resting state EEG asymmetries may provide for an electrophysiological correlate.
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2016, Physiology and BehaviorCitation Excerpt :The current study aimed to expand on prior findings by examining several hypotheses pertaining to the relationship between resting-state EEG and measures associated with food-specific approach and avoidance. Specifically, the PFS has been previously related to left frontal asymmetry [2], thus it was tested as a predictor of food-specific, relative left-sided frontal activation. Restrained eaters are posited to represent “effective” preventers of weight gain for two reasons: (1) restraint, unlike dieting, does not predict future weight gain [9]; and (2) restrained eating is associated with a significant reduction in the rate of weight gain compared to unrestrained eaters [10].