Is comfort food really comforting? Mechanisms underlying stress-induced eating

Highlights

• Stress decreases the hedonic pleasure experienced during the consumption of highly palatable food.

• Stress triggers food-seeking behaviors, whether food consumption elicits liking or not.

• Stress increases the control exerted by the habitual and the Pavlovian systems over the goal-directed system.

• Interventions regulating the food environment could be a promising strategy to reduce overeating behaviors.

Abstract

Overeating behaviors are nowadays a worldwide issue, and cumulative evidence shows that stress induces excessive pursuit of highly palatable food. However, the role of stress in this phenomenon remains poorly understood. The classic interpretation is that excessive eating is an attempt to reduce the aversive feeling associated with the stress response through the hedonic properties of highly palatable food. In this review, we propose an alternative hypothesis based on theoretical models developed in the framework of reward processing. We review recent literature on animal and human studies suggesting that stress reduces hedonic pleasure during highly palatable food consumption and increases the control that the habitual and Pavlovian systems exert on food-seeking behaviors over the control exerted by the goal-directed system. From this literature, we propose that (a) stress amplifies automatic attentional orienting toward stimuli associated with palatable food (i.e., Pavlovian stimuli), rendering them more likely to be perceived; and (b) once perceived, these stimuli trigger stress-amplified motivational bursts and the control that the habitual system exerts on food-seeking behaviors. We hypothesize that stress-induced eating is driven by habits and Pavlovian motivational bursts, independent of hedonic pleasure or even of the goal of reducing the stress-related aversive state. Thus, if a stressed person encounters an environmental stimulus associated with highly palatable food, this may trigger excessive pursuit of highly palatable food, whether or not the food elicits liking during its consumption.

Introduction

In the last century, many countries have experienced a considerable increase in overeating behaviors (Prentice, 2006). Overeating can have severe consequences, in particular obesity and associated diseases, such as diabetes mellitus type 2, cardiovascular diseases (Ruhm, 2012) and even cognitive deficits and increased risk of dementia (Kerwin et al., 2011). Stress has an important influence on eating behaviors: During stressful periods, a subgroup of people (i.e., 30%) decreases their food intake, whereas most individuals considerably increase their food intake (Epel et al., 2004, Stone and Brownell, 1994; for a review, see Adam & Epel, 2007). Stress-induced overeating is a phenomenon that is particularly robust among people who try to control their excessive food intake (e.g., restraint eaters). During stressful periods, they often relapse and overeat (Polivy & Herman, 1999).

A stressful event (i.e., a stressor) is defined as (a) an event that is perceived as threatening for the physiological or psychological integrity of the individual, combined with (b) the perception of being unable to successfully cope with such an event (Lazarus & Folkman, 1984). Stressors trigger a complex response in the individual (i.e., stress), which is physiologically characterized by the activation, at the central nervous system level, of dopaminergic and noradrenergic systems (Cabib and Puglisi-Allegra, 2012, Schwabe, Dickinson and Wolf, 2011), together with the activation of the sympathetic nervous system and the hypothalamic–pituitary–adrenal axis (HPA; Koolhaas et al., 2011). The activation of the HPA leads to the secretion of glucocorticoids (i.e., cortisol in humans) and numerous other hormones, neuropeptides and neurotransmitters (see Herman et al., 2003, for a review). For instance, a powerful stressor that can activate this system in humans consists of situations that are perceived as threatening for the social self because of a form of social evaluation such as public speaking or being judged by other people (Dickerson & Kemeny, 2004).

The kind of food that is overeaten under stressful conditions tends to be highly palatable, which means that it triggers hedonic pleasure and is usually highly caloric (e.g., sucrose or lard; Pecoraro et al., 2004, Tomiyama et al., 2011, Zellner et al., 2006). Experiments modeling stress-induced eating in animals have demonstrated that stressed rodents usually consume less food under stress, unless it is highly palatable, in which case consumption considerably increases (see Bazhan & Zelena, 2013, for a review). Experiments conducted on humans have also shown that participants in stressful conditions eat more highly palatable food than do participants in stress-free conditions (Epel et al., 2001, Tomiyama et al., 2011, Zellner et al., 2006).

The stress-induced increase in consumption of highly palatable food has been widely documented in animals and humans (Adam and Epel, 2007, Dallman et al., 2005, Dallman et al., 2003, Greeno and Wing, 1994, Maniam and Morris, 2012), but the underlying psychological mechanisms of this behavioral change have been poorly explored. The most common explanation in mechanistic terms is the following: Highly palatable food is consumed because its rewarding hedonic properties reduce the discomfort generated by the stressful situation (Adam and Epel, 2007, Dallman et al., 2003, Dallman et al., 2005).

Highly palatable food is conceived as one of the most powerful rewards in animals (Berridge, 2009), including humans (Kringelbach, 2004). In this narrative review, we capitalize on a theoretical model developed within a reward processing framework (Berridge and Robinson, 2003, Rangel et al., 2008) suggesting that other psychological mechanisms could be involved in stress-induced eating beyond hedonic pleasure. More particularly, we suggest that the theoretical framework proposed by Rangel et al. (2008) is well suited to study the interaction between reward and overeating behavior. This model postulates that reward-seeking behaviors are controlled by three functionally interacting systems: Pavlovian, habitual and goal directed.

The Pavlovian system assigns intrinsic affective properties of a rewarding outcome (e.g., highly palatable food) to a neutral stimulus with which it has been systematically associated (e.g., a bell ringing). After the associative learning is completed, the Pavlovian stimulus acquires the ability to evoke behavioral reactions originally triggered by the rewarding outcome (e.g., salivating after hearing the bell ringing).

The habitual system controls automatic instrumental actions. An instrumental action (e.g., pressing on a lever) leading to a reward (e.g., highly palatable food) is learned through trial and error. During the course of these repetitions, the action becomes more and more automatized and, eventually, habits are no longer triggered by the representation of a particular reward (e.g., highly palatable food), but rather by environmental stimuli from the context in which the instrumental action has been learned (e.g., seeing the lever, pressing the lever; stimulus–response learning even in the absence of hunger).

In the habitual system, the action is not accomplished with the intention to obtain a reward, whereas in the goal-directed system, the representation of the rewarding outcome is critical. The goal-directed system involves learning the association between a specific action (e.g., jogging) and a rewarding outcome (e.g., feeling fit; action-outcome learning). The representation of the outcome and its causal relation with the instrumental action is vital to the goal-directed system, but it is not necessary for the habitual system, which involves direct learning between an environmental stimulus and an instrumental action (stimulus–response learning). Therefore, goal-directed actions demand a higher load of cognitive resources and are slower compared with habits. However, the effort invested in goal-directed actions is flexibly proportional to the value of the rewarding outcome that they are leading to.

In this narrative review, we present recent representative literature investigating how stress influences these three systems in food-seeking behaviors for highly palatable food. First, we illustrate how the stress-induced eating behavior might not exclusively be driven by the goal or the experience of a stress reduction through a pleasant food consumption experience (i.e., the so-called aversive state reduction hypothesis; Robbins & Fray, 1980). Rather, we propose that (a) stress increases the attention towards and the motivation triggered by the perception of the Pavlovian stimuli, which is then (b) channeled by the habitual system, which predominates over the goal-directed system when an individual is under stress. More precisely, we propose that the Pavlovian system determines the affective intensity of stress-induced eating (i.e., how much effort is mobilized in food-seeking behaviors, how much food is wanted), and the habitual system determines the direction of stress-induced eating (i.e., which kind of food is sought under stressful conditions).