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Biological Psychology 131 (2018) 31–42

Contents lists available at ScienceDirect

Biological Psychology
journal homepage: www.elsevier.com/locate/biopsycho

The role of reward circuitry and food addiction in the obesity


epidemic: An update
Sarah-Jane Leigh, Margaret J. Morris ∗
Department of Pharmacology, School of Medical Sciences, UNSW Australia, UNSW Sydney, NSW 2052, Australia

a r t i c l e i n f o a b s t r a c t

Article history: The increasing worldwide prevalence of obesity is partially related to the ready availability of highly
Received 3 June 2016 palatable foods which increases the incidence of hedonic, non-homeostatic feeding. The “food addic-
Received in revised form 10 October 2016 tion” hypothesis postulates that exposure to these foods alters the brain’s reward circuitry, driving an
Accepted 15 December 2016
addiction-like behavioural phenotype of compulsive overeating. This review highlights recent evidence
Available online 21 December 2016
that examines changes in the mesolimbic dopaminergic circuit, the primary component of the reward
system, associated with exposure to highly palatable foods and obesity. The majority of obesity stud-
Keywords:
ies in animals have not measured addictive-like behaviours, but reports of such behaviours have been
Food addiction
Obesity
restricted to experiments using models of binge eating. Where examined, the prevalence of addiction-
Binge eating like behaviour in overweight and obese subjects indicates that 10–25% of the population meets the Yale
Reward Food Addiction Score criteria. There is considerable overlap in the behaviours ascribed to food addiction
Highly palatable food and binge eating disorder, and food addiction scores correlate highly with measures of binge eating. We
Yale food addiction scale feel that more research is required in humans to determine whether food addiction is both behaviourally
and neurobiologically distinct from binge eating disorder. While the reward circuitry is clearly affected
by both highly palatable foods and diet-induced obesity in a similar manner to short and long exposure to
drugs of abuse, the challenge for the future is to show that these neurobiological changes are associated
with addiction-like behaviour.
© 2016 Elsevier B.V. All rights reserved.

1. Introduction excess adiposity fail to address one of the most common underlying
causes of increased weight gain and obesity: dysregulated feeding
The prevalence of obesity has increased dramatically in recent behaviour.
decades and is now considered the most serious health issue fac- Hyperphagia, or chronic overeating, is a primary behavioural
ing the developed world by the World Health Organisation (WHO, component of both genetic and common forms of overweight
2000). Obesity can be defined in terms of body mass index (BMI): and obesity (Barsh, Farooqi, & O’Rahilly, 2000; Webber, 2003) and
individuals with a BMI ≥25 and ≥30 are considered overweight and therefore many forms of obesity can be considered to occur par-
obese respectively. While there are alternative definitions of over- tially as a consequence of overeating. This form of dysregulated
weight and obesity (Ogden, Yanovski, Carroll, & Flegal, 2007; WHO, feeding behaviour is believed to result from the relatively recent
2014), the majority of human studies utilise the BMI definition increased availability of and exposure to highly palatable, energy
which will subsequently be adopted for this review. dense foods (Avena & Gold, 2011b; Berthoud, 2012), as well as other
Despite considerable research into both the causes of over- environmental factors such as reduced activity and increased stress
weight and obesity as well as potential interventions to reduce exposure (Dallman et al., 2003).
excessive adiposity, current treatments for obesity have had lim- These feeding patterns are often considered to result from alter-
ited success, and most people who do experience successful weight ations in the reward circuitry that governs hedonic feeding, driven
loss fail to maintain it (Lemmens, Oenema, Klepp, Henriksen, & by the rewarding aspects of palatable foods (Alonso-Alonso et al.,
Brug, 2008; Proietto, 2011; Soleymani, Daniel, & Garvey, 2016). 2015; Ziauddeen, Alonso-Alonso, Hill, Kelley, & Khan, 2015). Hedo-
This is believed to occur because all interventions aimed at reducing nic feeding is defined in this review as food consumption for
pleasure in the absence of an energy deficit, that usually manifests
as overeating in the presence of highly palatable foods. Hedonic
∗ Corresponding author.
feeding is considered here as the behavioural outcome of increased
E-mail address: m.morris@unsw.edu.au (M.J. Morris).
reward system activation. Substantial investigation has occurred

https://doi.org/10.1016/j.biopsycho.2016.12.013
0301-0511/© 2016 Elsevier B.V. All rights reserved.
32 S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42

to determine how the reward circuitry is impacted by continued


consumption of highly palatable foods and increased adiposity.
A popular hypothesis in the literature is that highly palatable
foods can impact the reward circuitry in a manner similar to addic-
tive drugs, resulting in the development of “food addiction” (FA)
which is defined in this review as compulsive overeating in the
presence of highly palatable foods. This idea has existed in the
scientific literature since the 1950s but has recently drawn more
attention (Meule, 2015), spurring intensive investigation into the
addictive-like components of feeding behaviour. While the neu-
robiological regulation of compulsive overeating is complex and
involves several additional systems than those classically involved
in the regulation of addiction-related behaviours, there are striking
overlaps in neurobiological mechanisms, brain activation patterns
and behavioural outcomes that suggest common underlying effects
on the reward circuitry.
Despite these similarities, the concept of FA remains con-
troversial due primarily to the heterogeneity of the causes of
overweight and obesity, as well as the fact that feeding, unlike
self-administration of addictive substances, is a natural reward nec- Fig. 1. The brain regions responsible for the control of feeding behaviour are also
essary for survival and thus is dependent on the reward system for involved in regulating stress and reward.
appropriate expression (Tappy, 2016). Several brain regions involved in both homeostatic (dark grey) and hedonic (light
grey) express receptors for peripheral markers of metabolic function, such as insulin
This review aims to evaluate recent findings regarding the role of
and leptin, and change their signalling patterns in response to changes in these
reward circuitry in compulsive overeating, as well as the evidence peripheral signals. The medial hypothalamus is the main centre for the processing
supporting FA. We have focussed predominantly on the litera- of internal metabolic cues and the lateral hypothalamic area (LHA) is responsible for
ture concerning the mesolimbic dopaminergic (DA) system: this is integrating this information into reward circuitries. The mesolimbic reward path-
the primary component of the reward circuitry and has received way – consisting of the ventral tegmental area (VTA), the nucleus accumbens (NAc)
and the fibres connecting these regions – drives food seeking behaviour in response
the most attention in regards to FA. The common underlying to signals of peripheral energy deficit, as well as in the presence of highly palatable
behavioural and neurochemical changes associated with substance foods. This pathway informs the orbitofrontal cortex (OFC) which is a secondary
dependence occur in this neural pathway (Nestler, 2005; Volkow, gustatory cortex, as well as being involved in decision making and reward valua-
Wang, Fowler, & Tomasi, 2012). tion. The VTA is also connected to the amygdala, which is involved in recognising
biologically relevant external stimuli, such as food and stressors, and drives both
approach and avoidance behaviour. The amygdala and paraventricular nucleus of
the hypothalamus are critical regions involved in responding to stressors.
2. The role of reward in normal feeding Dashed arrows represent circulating markers of metabolic function, while unbro-
ken arrows represent white matter tracts. All depicted regions other than the medial
The brain’s reward circuitry evolved to increase an organism’s hypothalamus are direct sites of action for most drugs of abuse.

likelihood of performing behaviours that improve its chances of


survival. Reward is defined as a neural “response” to both inter- DA-ergic and opioidergic systems work interdependently to
nal and external stimuli that incentivises behaviours to reduce a promote food intake: the former creates anticipation and food seek-
physiological or psychological deficit (Berridge, 1996). Eating is ing behaviour while the latter are involved in hedonic pleasure
intrinsically rewarding, and the taste and consumption of palat- (Berridge, 2009). The homeostatic feeding circuitry and neuro-
able foods activate the reward system. While the neural circuitry transmitters, as well as peripheral metabolic signals that inform
responsible for regulating homeostatic and hedonic feeding are the hypothalamus (the primary brain region that regulates home-
often considered as separate entities, this is not the case: the ostatic feeding) regarding the body’s metabolic and nutritional
homeostatic feeding and reward circuitries are heavily integrated status, all interact with the reward pathways, notably the mesolim-
and interdependently regulate feeding behaviour (Muenzberg- bic DA-ergic pathways (Berthoud, 2011; Muenzberg-Gruening
Gruening, Qualls-Creekmore, Yu, Morrison, & Berthoud, 2016) as et al., 2016).
shown in Fig. 1. The lateral hypothalamic area (LHA) is a key site for the
Unlike other homeostatic systems, the feeding system is biased integration of both reward and homeostatic circuitries. The
towards a positive energy balance and the hedonic qualities of LHA regulates reward-seeking behaviours and self-stimulation
food can produce feeding behaviour after energy requirements (Figlewicz, Bennett-Jay, Kittleson, Sipols, & Zavosh, 2011) and
have been met (Kenny, 2011b). This is because homeostatic sig- subpopulations of LHA neurons are involved in arousal and home-
nals tend to be relatively weak, modifying food intake over long ostatic feeding in addition to acting as modulators of motivational
periods of time, and are easily overridden by non-homeostatic sig- circuitry (Burt, Alberto, Parsons, & Hirasawa, 2011). It also mod-
nalling that act from meal to meal (Alonso-Alonso et al., 2015; Begg ulates the ventral tegmental area (VTA) and nucleus accumbens
& Woods, 2013). Many have argued that this tendency towards a (NAc) directly (Gutierrez, Lobo, Zhang, & de Lecea, 2011). Various
positive energy balance in current contexts arises as the feeding neuronal subtypes, orexin- and melanin concentrating hormone-
system evolved in a resource-sparse environment (Albuquerque, containing neurons in particular, project from the LHA to the
Stice, Rodriguez-Lopez, Manco, & Nobrega, 2015; Genne-Bacon, reward circuitry and have been shown to alter DA release (Aston-
2014), where overeating in plentiful times would be outweighed Jones, Smith, Moorman, & Richardson, 2009; Baldo et al., 2004;
by longer periods of limited food access. However, the role that Domingos et al., 2013; Hirasawa, Parsons, & Alberto, 2007; Ho &
hedonics play in increasing feeding behaviour in the presence of Berridge, 2013; Sears et al., 2010).
palatable foods is no longer beneficial in the context of surplus food In addition to the projections from feeding centres to the
availability and is likely contributing to the increased incidence of mesolimbic DA-ergic system, key endocrine signals – including
obesity (Berthoud, 2012; Stice, Figlewicz, Gosnell, Levine, & Pratt, ghrelin, insulin and leptin – reflecting both the short- and long-term
2013). metabolic status of the body, have direct effects on DA release in the
S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42 33

NAc via their receptors on VTA DA-ergic neurons (Liu & Borgland, chemical structure and binding targets, all drugs of abuse share
2015). specific effects on the brain’s reward circuitry after short- and
Ghrelin is an orexigenic hormone produced predominantly in long-term exposures which often result in a common behavioural
the stomach that has been shown to be involved in the regula- repertoire described as addiction (Hyman, 2005; Volkow et al.,
tion of hedonic, as well as homeostatic, feeding. Central ghrelin 2012).
administration has been shown to increase consumption of palat- Addiction behaviour is characterised by compulsive substance
able foods (Egecioglu et al., 2010; Perello et al., 2010) and operant seeking, uncontrolled substance intake and the production of a
responding to sucrose (Skibicka, Hansson, Alvarez-Crespo, Friberg, negative emotional state when the substance is withheld. These
& Dickson, 2011). Pharmacological antagonism or knockout of the behaviours persist despite harm to the individual, and an addicted
ghrelin receptor results in decreased responding to sucrose in both individual will experience chronic relapses into these behaviours
choice (Egecioglu et al., 2010; Landgren et al., 2011; Perello et al., (APA, 2013). Most drugs of addiction are thought to cause common
2010) and operant conditioning (Overduin, Figlewicz, Bennett-Jay, changes in particular brain regions which underlie this behavioural
Kittleson, & Cummings, 2012; Skibicka et al., 2011) paradigms pattern.
without impacting ad libitum chow intake (Skibicka et al., 2011), The mesolimbic DA-ergic pathway, which connects the VTA to
suggesting that ghrelin may be involved in modulating the reward- the NAc, is a primary component of the brain’s reward circuitry
ing aspects of consumption. Ghrelin administration to the VTA and is the major circuit involved in the shared behavioural effects
increased DA-ergic cell activity, synapse formation and DA turnover of addictive substances (Pierce & Kumaresan, 2006). Addictive sub-
in this area in both mice and rats (Abizaid et al., 2006). Thus, ghrelin stances converge on either or both these brain regions, with the net
acts on the mesolimbic reward circuitry to increase food seeking in short-term effect of increasing DA-ergic transmission in the NAc
the presence of highly palatable foods. (Nestler, 2005; Volkow, Koob, & McLellan, 2016). It is this neuro-
Insulin is involved in blood glucose regulation peripherally, and chemical change that makes most addictive substances so acutely
appears to act differently on homeostatic and reward components rewarding (Gardner, 2011), encouraging repeated drug exposure.
of the feeding circuitry. Insulin infusion into the arcuate nucleus of While drugs of abuse are acutely rewarding, only 10% of individ-
the hypothalamus decreases sucrose self-administration, whereas uals exposed to addictive substances will develop the most severe
insulin infusion into the NAc increases sucrose self-administration phenotypic characteristics of addiction (Volkow et al., 2016). This
and the time rats actively engage in the self-administration task has been hypothesised to be due to the shift in reinforcement type:
(Figlewicz, Bennett, Aliakbari, Zavosh, & Sipols, 2008). This indi- drugs are initially taken because they are positively reinforcing but
cates that insulin both reduces and increases feeding behaviour, by continue being taken to relieve the negative states that develop
the homeostatic and hedonic components of the feeding circuitry during withdrawal and abstinence. These late-onset longer-term
respectively. Sucrose consumption increases insulin receptor phos- neurobiological changes are of particular interest, as these are asso-
phorylation in the NAc within 7 min (Stouffer et al., 2015; Woods ciated with the behavioural syndrome that develops as individuals
et al., 2016), and this has been hypothesised to code the nutri- become dependent on addictive substances.
tive value of a substance (Woods et al., 2016). Therefore, despite Chronic exposure to most abused substances results in reduced
reducing homeostatic signalling for food seeking behaviour, insulin baseline NAc DA levels, secondary to a homeostatic response to
likely informs the reward system of the relative nutritive value of repeated activation of the system (Nestler, 2005; Volkow et al.,
different foods, promoting hedonic feeding. 2012). This increases the system’s threshold, and reduces the sub-
Leptin is an adipokine, a small chemical messenger produced by jective experience of reward. Concurrently, chronic exposure to
adipose tissue, that informs the brain about changes in peripheral abused substances sensitises the reward circuitry to other addictive
fat mass. This signalling impacts on both metabolic feeding path- substances, as well as substance-associated cues and environmen-
ways and reward associated regions of the brain. Leptin receptors tal stressors (Schulte, Grilo, & Gearhardt, 2016).
are expressed on a subpopulation of neurons in the LHA which are These characteristic changes in the mesolimbic DA-ergic sys-
distinct from melanin-concentrating hormone (MCH) and orexin tem associated with addictive substances have been shown to
expressing neurons; these leptin receptor expressing neurons were contribute to at least some aspects of the behavioural repertoire
shown to be inhibitory and project to the VTA (Leinninger et al., that characterises addiction, and likely contribute to addiction-like
2009). Leptin administration to the VTA increased VTA tyrosine behaviours in other conditions. Understanding these alterations
hydroxylase (TH) mRNA expression, as well as producing a 40% may allow us to develop broad therapies for addictive behaviour,
increase in DA release in the NAc (Leinninger et al., 2009), showing irrespective of the substance that triggered the behavioural change.
that both the enzyme necessary for DA production and DA itself are
impacted by leptin levels. Reducing leptin receptor expression of
DA-ergic cells in the LHA and midbrain increased intake of high fat 4. Highly palatable foods and the mesolimbic reward
diet and increased motivation to work for food (Davis, Choi et al., system
2011). Therefore, leptin acts on mesolimbic reward pathways to
increase DA-ergic transmission in the NAc, increasing food seeking It is well-established that the circuitry driving hedonic feeding
behaviours. is also affected by addictive substances (Kenny, 2011a; Lutter &
These interactions demonstrate that not only is there crosstalk Nestler, 2009; Tang, Fellows, Small, & Dagher, 2012). One of the
between homeostatic and hedonic feeding systems, but the hedo- major factors promoting overweight and obesity is the abundance
nic feeding system is directly impacted by changes in peripheral of highly palatable foods that are often nutrient poor. It is well-
metabolic and nutritional markers. This allows for the hedonic sys- established that a highly palatable diet increases both food and
tem to respond directly and efficiently to palatable foods. energy consumption (Martire, Holmes, Westbrook, & Morris, 2013;
Martire, Westbrook, & Morris, 2015; Newman, Pascal, Sadeghian,
& Baldo, 2013; South, Holmes, Martire, Westbrook, & Morris, 2014)
3. The common underlying behavioural and molecular but there has been limited research into whether specific macronu-
changes in addiction trients drive overeating. The term FA is often used to imply that
there must be some ingredient or inherent property in particular
Addictive drugs are diverse substances, resulting in unique foods that drives the behavioural disorder (Avena & Gold, 2011a;
behavioural and physiological outcomes. Despite differences in Hebebrand et al., 2014; Meule & Gearhardt, 2014b).
34 S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42

High fat consumption is known to lead to obesity and increased intake has been shown to indirectly modulate mesolimbic DA cir-
fat content in foods has been shown to increase meal size (la Fleur, cuits by altering cholecystokinin, insulin and ghrelin levels (Ochoa,
Luijendijk, van der Zwaal, Brans, & Adan, 2014). Energy intake can Lalles, Malbert, & Val-Laillet, 2015) and glucose levels modulate
be increased by including a lard supplement in an animal’s home GABA terminal transmitter release via ATP-sensitive potassium
cage (Apolzan & Harris, 2012). While increasing fat does lead to channels (Levin, 2001). There is some evidence that glucose may act
increased energy intake, a recent study suggests that once the fat differently to other sugars, since glucose results in greater striatum
levels exceed 35% rats reduce their energy intake (Hoch, Kreitz, activation than fructose (Page et al., 2013).
Gaffling, Pischetsrieder, & Hess, 2015). Increased consumption of In humans high fat liquid meals increases activation in the bilat-
fat is most likely mediated by opioid signalling (Kelley et al., 2002; eral caudate whereas high sugar liquid meals increases activation
Naleid, Grace, Chimukangara, Billington, & Levine, 2007; Nogueiras in the putamen (Stice, Burger, & Yokum, 2013) indicating that dif-
et al., 2012), although this may be modulated by preference (Naleid ferent parts of the reward circuitry may be involved in experiencing
et al., 2007). Joyner, Gearhardt, and White (2015) found that in reward for different macronutrients. In animal models high fat diets
human participants fat cravings were a significant partial media- have been shown to reduce DA receptor D2 and D3 density in the
tor between addictive-like eating behaviours and BMI, although fat NAc (Adams et al., 2015; van de Giessen et al., 2012) and cause
craving did not predict the number of bingeing episodes. The effects deficits in DA reuptake and DA response to cocaine exposure (Cone,
of high fat consumption on motivation for sucrose consumption Chartoff, Potter, Ebner, & Roitman, 2013). Exposure to a sweet-
are contradictory (Blaisdell et al., 2014; Carlin, Hill-Smith, Lucki, & ened fat diet results in increased synaptic density in the VTA (Liu
Reyes, 2013; Figlewicz et al., 2013; Tracy, Wee, Hazeltine, & Carter, et al., 2016) and causes rats to transiently respond more intensely to
2015), and may be impacted by the energy requirements of the muscimol, a GABA-A receptor agonist, infused into the NAc shell,
animal as well as the type of fat added to the diet. increasing feeding for the first two weeks of exposure (Newman
The effects of processed carbohydrates on feeding behaviour are et al., 2013). Conversely, both baclofen, a GABA-B receptor agonist,
much more complex, as it appears that high sugar drinks are con- and naltrexone, a mu-opioid receptor antagonist, reduce consump-
sumed differently to high sugar foods. Liquid carbohydrates appear tion of a palatable diet (Avena & Gold, 2013). These data suggest that
to be less satiating, leading to increased energy intake (Apolzan & sugar, fat or both in combination can modulate the activity of the
Harris, 2012; Pan & Hu, 2011) and consuming a sucrose solution reward system, although it is clear that changes are not restricted
has been shown to increase meal frequency (la Fleur et al., 2014). to DA-ergic and opioidergic signalling pathways.
In humans sweet and carbohydrate cravings are a significant partial While a single exposure to addictive drugs or palatable foods
mediator between addictive-like eating behaviours and the num- both drive the release of DA in the NAc, there are different pop-
ber of binge episodes (Joyner et al., 2015). Rats have been shown ulations of neurons activated by natural and drug reinforcement.
to prefer sucrose to cocaine in a choice paradigm (Ahmed, Guillem, Electrophysiological experiments have shown that 92% and 93% of
& Vandaele, 2013; Lenoir, Serre, Cantin, & Ahmed, 2007) and when phasically active cells in the NAc respond differentially to water
given intermittent access, rats will binge on sweet foods (Avena, and food versus cocaine reinforcement respectively (Cameron,
Rada, & Hoebel, 2009). Wightman, & Carelli, 2014; Carelli, Ijames, & Crumling, 2000; Carelli
There is some evidence suggesting that the combination & Wondolowski, 2003), indicating that different substrates activate
of macronutrients is an important determinant of compulsive different circuits within the mesolimbic DA-ergic system.
overeating. One clinical study found that the level of processing the There is some evidence suggesting that macronutrient type is
food had undergone was the most influential factor that predicted less relevant than its availability and that restricting access to
whether the food was associated with problematic addictive-like highly palatable foods is actually responsible for addictive-like
behaviours (Schulte, Avena, & Gearhardt, 2015). Modern highly behaviours (Avena et al., 2009; Benton, 2010; Corwin & Grigson,
processed foods tend to be high in both fat and refined carbo- 2009). These ideas will be discussed in more detail in sections to
hydrates with a higher glycaemic load. When a cafeteria diet (a follow. Indeed, food choices made by humans would indicate that
normal chow diet supplemented with high-fat, high-sugar human overeaters typically consume a highly variable diet of subjectively
foods like biscuits, cake and meat pies) is used, fat and carbohydrate palatable food. Food is nutritionally complex, and there is limited
intake remains elevated even when differences in protein intake evidence that humans consume specific foods for specific sub-
reduce over time (Martire et al., 2013). Other evidence suggests that stances under normal physiological conditions. Foods, even when
the ratio of fat to carbohydrate content is important: energy intake highly palatable, do not appear to produce bingeing behaviours
was maximised in a group of rats when their food was composed or create physical dependence when provided ad libitum (Avena,
of 35% fat and 45% carbohydrates (Hoch et al., 2015). Cafeteria style 2010; Avena & Hoebel, 2012; Corwin, 2006; Corwin & Babbs,
diets combine both high-fat and high-sugar and tend to increase 2012; de Jong, Meijboom, Vanderschuren, & Adan, 2013; De Jong,
overall feeding bout frequency (Martire et al., 2013), resulting from Vanderschuren, & Adan, 2016; Martire et al., 2013, 2015). Instead,
increased snack consumption (Hoch, Pischetsrieder, & Hess, 2014; exposure to palatable foods is a necessary initial step in the pro-
Martire et al., 2013). Cafeteria diets also increase food approach cess that ends in addictive-like feeding behaviours, irrespective
behaviour (Liu et al., 2016). This is unsurprising since increased of the food’s nutritional or chemical composition (Benton, 2010;
food choice leads to greater energy intake and weight gain (Rolls, Hebebrand et al., 2014).
Rowe, & Rolls, 1982; van de Giessen, la Fleur, de Bruin, van den
Brink, & Booij, 2012).
While it is unclear whether high fat, high sugar or a combination 5. Obesity and the mesolimbic reward system
of both is the most effective macronutrient to drive overconsump-
tion, there has been considerable work aimed at understanding The chief similarity between the brain changes resulting from
how these macronutrients impact the brain. Administration of glu- chronic drug abuse and obesity is reduced baseline DA transmis-
cose into the livers of rats increases activity in regions associated sion in the NAc. The striatum (which includes the NAc) is a major
with both homeostatic and hedonic feeding, including the hypotha- anatomical area involved in reward processing and has frequently
lamus, NAc and orbitofrontal cortex (Delaere, Akaoka, De Vadder, been observed to function differently in obesity-vulnerable and
Duchampt, & Mithieux, 2013). Higher venous plasma glucose in obese individuals in response to both food and associated cues.
otherwise healthy overweight and obese men elicited increased Animal studies show reduced motivation toward chow or
activity in the right NAc and striatum (Lennerz et al., 2013). Sugar sucrose after prolonged exposure to a highly palatable diet
S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42 35

(Blaisdell et al., 2014; Carlin et al., 2013; Naneix, Darlot, Coutureau, date and putamen in women who are already obese (Stoeckel et al.,
& Cador, 2016; South et al., 2014; Tracy et al., 2015; Vucetic, 2008). Despite this evidence, a recent meta-analysis has revealed
Kimmel, & Reyes, 2011) and these changes have been associated there are no differences in BMI between individuals with and with-
with lower levels of DA-ergic activity markers in the NAc and stria- out the Taq1A polymorphism, which has been linked to reward
tum (Ahmed et al., 2014; Carlin et al., 2013; Geiger et al., 2009; deficiency and substance abuse (Benton & Young, 2016). While evi-
Naneix et al., 2016; Rada, Bocarsly, Barson, Hoebel, & Leibowitz, dence of reward circuitry function changes in humans are in line
2010; Sharma & Fulton, 2013). These findings indicate that pro- with findings in animals, further research needs to be conducted to
longed exposure to a highly palatable diet induces tolerance and determine how these areas are affected and whether these changes
reduced baseline DA levels in the NAc, similar to prolonged expo- are related to DA-ergic signalling in particular.
sure to addictive substances. One paper has argued that these Animal models also indicate that there are obesity-related
motivational changes are part of the development of a diet-induced changes to opioid signalling in the mesolimbic reward pathways.
depressive phenotype (Sharma & Fulton, 2013), but this has not Evidence for changes in the opioidergic signalling pathways indi-
been replicated. In line with this evidence, Geiger et al. (2009) cate that repeated exposures to highly palatable foods reduce
reported that an acute cafeteria diet challenge could stimulate DA mu-opioid receptor mRNA expression in the NAc (Alsiö et al.,
release in the NAc in diet-induced obese rats, while exposure to 2010; Vucetic et al., 2011) and VTA (Martire et al., 2014; Vucetic
chow did not. This suggests that the mesolimbic reward circuitry et al., 2011). Suppression of mu-opioid receptor expression in the
becomes less responsive to general reward but remains sensitive NAc prevents the development of diet induced obesity (Lenard,
to exposure to highly palatable foods. Zheng, & Berthoud, 2010). Changes in cannabinoid receptor 1 mRNA
It is unclear whether obesity results in a change in DA expression (Martire et al., 2014) and delta-opioid receptor mRNA
metabolism and receptor expression in animal models, or if these expression (Vucetic et al., 2011) have also been reported in the
differences predate obesity and can confer susceptibility or resis- rat VTA. Overall, the evidence, while limited, points to mu-opioid
tance to weight gain. While there is some evidence a highly receptors being the most likely candidates involved in reward
palatable diet reduces DA D1 receptor mRNA expression in the NAc changes associated with diet-induced obesity.
(Alsiö et al., 2010; Vucetic, Carlin, Totoki, & Reyes, 2012), levels Using naltrexone-induced nausea and cortisol release as a func-
of DA D2 receptor may be associated with obesity vulnerability. tional measure of opioidergic activity in overweight and obese
Obesity-resistant animals have been shown to have reduced base- women, Daubenmier et al. (2014) showed that naltrexone-induced
line D2 receptor expression in the NAc while obesity-prone rats increases in cortisol positively predicted emotional and restrained
have increased D2 receptor expression throughout the caudate eating scores, and was negatively associated with interoceptive
putamen (Huang, Yu, Zavitsanou, Han, & Storlien, 2005). One study awareness. Therefore, similar to the results found in animal studies,
found that 17 weeks exposure to a high fat diet increases TH and DA endogenous opioid signalling may be associated with behavioural
transporter (DAT) mRNA expression in the VTA, and that changes changes towards food in overweight and obese humans.
in mRNA expression in the VTA are associated with changes in While many of the brain changes reported in obese humans and
methylation of TH and DAT gene promoter regions (Vucetic et al., animals are largely a replication of those observed after chronic
2012). exposure to substances of abuse, the differences in the behavioural
There is some evidence that a high fat diet changes insulin sig- phenotype in the overweight and obese population would indicate
nalling in reward regions, resulting in disrupted DA homeostasis that these changes are not sufficient to induce FA-like behaviours.
(Speed et al., 2011). Diet-induced obesity has also been shown to This is unsurprising since the reward circuitry that modulates
reduce the effects of ghrelin on progressive ratio responding, as feeding evolved to increase behaviours that are beneficial to an
well as reducing ghrelin receptor mRNA in the hypothalamus and organism’s survival, and drugs of addiction are addictive because
NAc (Finger, Dinan, & Cryan, 2012). More research is needed to they directly impact on this circuitry to create feelings of pleasure
specifically probe the effects of long-term exposures to palatable and reward.
foods on these peripheral metabolic and nutritive markers and their
interactions with the hedonic feeding system.
Human imaging studies have provided evidence that there is 6. Addiction-like behaviours in animal models of obesity:
a decrease in D2/D3 receptor availability in the striatum associ- binge eating
ated with obesity (de Weijer et al., 2011; Haltia et al., 2007; Wang
et al., 2001), although a few studies have shown no effect of obe- While it is clear that reward circuitry is altered due to increased
sity (Eisenstein et al., 2013) or increased DA receptor availability intake of highly palatable, high caloric food, addiction-like
(Dunn et al., 2012). Studies utilising functional magnetic reso- behaviour only develop in animals under a specific experimental
nance imaging (fMRI) have shown that obese adults experience design: intermittent access to highly palatable foods, or bingeing
increased activation in the striatal and insular regions in response models (Corwin, Avena, & Boggiano, 2011; de Jong et al., 2013;
to highly palatable food cues (Jastreboff et al., 2013), and subse- Rada, Avena, & Hoebel, 2005; Ziauddeen, Farooqi, & Fletcher, 2012;
quent weight gain in adult women has been associated with a Ziauddeen and Fletcher, 2013). Most animal models of binge eating
reduction in right striatal BOLD signal in response to milkshake involve restricting access to a highly palatable food intermittently,
intake, relative to their baseline activity (Stice, Yokum, Blum, & which results in rapid overconsumption when the food is presented
Bohon, 2010). Conversely, striatal activity during food commercials (Rospond, Szpigiel, Sadakierska-Chudy, & Filip, 2015; Wojnicki,
predicted increases in BMI over one year in adolescents (Yokum, Stine, & Corwin, 2007).
Gearhardt, Harris, Brownell, & Stice, 2014). Interestingly, when Restricting access to a highly palatable food, containing either
adolescents were already obese, food commercials increased BOLD high fat or high sugar, is sufficient to induce binge eating (Corwin,
signalling in other areas of the reward system, including the PFC 2004; Corwin, 2006; Davis et al., 2007; Dimitriou, Rice, & Corwin,
and ACC, but not the striatum (Gearhardt, Yokum et al., 2014). In 2000) which is associated with a concomitant decrease in chow
adult women, BMI has been shown to predict activation in the dor- consumption (Berner, Avena, & Hoebel, 2008; Cottone, Sabino,
sal striatum and orbitofrontal cortex, which is involved in assigning Steardo, & Zorrilla, 2007). The development of bingeing behaviour
tastes reward values, when viewing high calorie foods (Rothemund is heavily dependent on the schedule of access: highly palatable
et al., 2007) and these types of images elicit BOLD signalling in the food needs to be presented frequently, but for short periods (Rada
medial and lateral OFC, NAc and ventral striatum, and in the cau- et al., 2005; Wojnicki et al., 2007). Intermittent access to highly
36 S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42

palatable food prevents animals from becoming less motivated by both receptors is downregulated after continued restricted expo-
food over long term experiments, and this is associated with a sure to a highly palatable diet (Alsiö et al., 2010; Carlin et al.,
continued increase in NAc extracellular DA levels which would nor- 2016), consistent with models of addiction. D2 receptor expres-
mally attenuate with ad libitum access over the same time frame sion has been shown to be inversely proportional to body weight,
(Dimitriou et al., 2000; Hajnal & Norgren, 2002; Hoebel, Avena, and therefore tends to be lower in unrestricted animals, rela-
Bocarsly, & Rada, 2009; Rada et al., 2005; Sahr et al., 2008; Wojnicki, tive to restricted rats, and knocking down D2 receptor increases
Roberts, & Corwin, 2006). Animals that are more prone to binge reward thresholds (Johnson & Kenny, 2010). Increased D3 receptor
eat were shown to tolerate higher levels of foot shock for palat- and reduced proenkephalin mRNA expression has been noted in
able foods and cyclic restriction-refeeding increases foot shock the NAc (Spangler et al., 2004). Mu-opioid receptor binding was
tolerance for palatable food in binge eating resistant rats (Oswald, increased in the NAc and correlated with glucose intake in the
Murdaugh, King, & Boggiano, 2011), showing that similar to models first hour of access on the last day of testing (Colantuoni et al.,
of substance abuse, the animals continue their bingeing behaviour 2001). Increased DAT mRNA expression has been observed in VTA
in the face of adverse consequences. (Carlin et al., 2016; Colantuoni et al., 2001). Both restricted and
The evidence that animal models of binge eating result in psy- unrestricted access to a cafeteria diet reduce CB1 and mu-opioid
chological withdrawal when palatable food is removed indefinitely receptor mRNA expression in the VTA (Martire et al., 2014). There-
is less clear. While some have shown that intermittent food expo- fore, there are no apparent unique changes in bingeing animals: as
sure does not affect the response to food deprivation (Newman a rule the differences observed are in the same direction but not as
et al., 2013; Parylak, Cottone, Sabino, Rice, & Zorrilla, 2012), oth- pronounced as those in ad libitum models. This indicates that the
ers have shown increased anxiety as assessed by the elevated plus behavioural phenotype may arise from environmental constraints
maze with a concomitant attenuation of food-induced NAc DA imposed by the model, rather than from internal changes to reward
release and increase in NAc acetylcholine (ACh) release after 36 h circuitry.
of food deprivation (Avena, Bocarsly, Rada, Kim, & Hoebel, 2008). It Studies from Hoebel’s laboratory (Avena, Rada, Moise, & Hoebel,
should be noted that another study has found that restricted ani- 2006; Rada et al., 2005) have suggested that the reason sugar binge
mals spend less time in the open arm of the elevated plus maze eating rats develop FA-like behaviour is due to changes in ACh
when not deprived (Cottone et al., 2007), so restricted access to release in the NAc. ACh seems to be released in response to sati-
palatable food may increase anxiety generally and not only in ety (Avena et al., 2006; Avena & Rada, 2012) and bingeing on sugar
instances of food deprivation. Measures of anxiety can be reduced postpones ACh release. This is the mechanism by which substance
in bingeing animals by treatment with a corticotropin-releasing addiction is thought to develop (Avena & Rada, 2012; Hoebel et al.,
factor 1 (CRF1) receptor antagonist (Cottone et al., 2009), sug- 2009). This in an interesting avenue of research, since ad libitum
gesting that bingeing impacts the central stress circuitry. Bingeing exposure to sucrose does not change ACh release, however few
animals also exhibit larger startle responses during sucrose depri- other studies have been conducted to investigate the role of ACh in
vation (Yakovenko, Speidel, Chapman, & Dess, 2011). Depriving compulsive overeating.
animals of the palatable food they have been exposed to inter- Drugs that reduce substance dependence have been shown
mittently increases their motivation for palatable foods (Avena, to successfully reduce binge eating. Opioid antagonists appear to
Long, & Hoebel, 2005; Corwin et al., 1998; Grimm, Manaois, reduce feeding in bingeing animals without affecting chow con-
Osincup, Wells, & Buse, 2007), although this effect may be limited sumption, and this is associated with reduced NAc levels of DA in
to obesity-prone rats (Pickering, Alsio, Hulting, & Schioth, 2009), response to food (Sahr et al., 2008). Naloxone has been shown to
and accelerates habitual control of instrumental learning (Furlong, reduce responding to palatable food when bingeing animals are
Jayaweera, Balleine, & Corbit, 2014). Intermittent access to sucrose food deprived (Grimm et al., 2007) and treatment with a cannabi-
also reduces blocking: animals are more likely to approach a food noid 1 receptor antagonist reduces bingeing in both animals
cue that is usually blocked by prior learning (Sharpe, Clemens, exposed to palatable food and chow (Bharne, Borkar, Subhedar, &
Morris, & Westbrook, 2016). These data indicate that removing Kokare, 2015; Parylak et al., 2012), indicating that binge eating may
access after intermittent access to palatable foods may cause a be regulated by opioid signalling. Results for measures of anxiety in
similar behavioural state to psychological withdrawal observed in bingeing animals are mixed (Colantuoni et al., 2002; Cottone et al.,
animal models of addiction, although bingeing animals show signs 2007) and treatment with CRF1 receptor antagonists has mixed
of increased anxiety during intermittent food exposure as well. effects on bingeing episodes: it either reduces the quantity of food
While there have been some reports of physiological withdrawal consumed (Parylak et al., 2012) or has no effect (Cottone et al.,
symptoms resulting from naloxone treatment or glucose depri- 2009). GS 455534, a highly selective reversible aldehyde dehydro-
vation (Colantuoni et al., 2002), others have not found evidence genase 2 inhibitor which reduces both alcohol and cocaine intake
of withdrawal when intermittent access to highly palatable foods in rats, has been shown to reduce sugar and fat intake in binge-
is removed (Bocarsly, Berner, Hoebel, & Avena, 2011; Yakovenko ing animals. This reduced bingeing effect was associated with a
et al., 2011) or when the animals are given naloxone (Bocarsly 50% reduction in NAc DA release (Bocarsly et al., 2014). Activating
et al., 2011). Others have argued that these withdrawal effects GABA-B receptors reduces increased lever pressing for fat in ani-
may be specific to intermittent access to sucrose (Ahmed et al., mals exposed to restricted access to shortening (Wojnicki et al.,
2013; Avena, 2006; Avena et al., 2009), but further investigations 2006). It should be noted that most of these drug effects have yet
are required to confirm this hypothesis. Withdrawal symptoms to be replicated, and further research is required.
are particularly important in models of addiction, because it is While extended unrestricted access to a palatable diet induces
hypothesised that avoidance of withdrawal symptoms helps per- addiction-like motivation deficits and over-eating, restricted access
petuate addiction-like behaviours. If models of FA do not elicit to this diet is necessary to create binge-like patterns of consump-
withdrawal-like responses another mechanism that could perpet- tion, but these are usually not accompanied by the molecular
uate addiction-like behaviours will need to be proposed. changes reported in drug self-administration and addiction.
Bingeing on sugar increases DOPAC levels and DA turnover in the Although some studies do report behavioural and molecular evi-
NAc (Hajnal & Norgren, 2002; Rada et al., 2005). D1 receptor bind- dence of FA, the bulk of the data suggests that binge eating has
ing is increased in the NAc and other parts of the reward circuitry, relatively less impact on reward circuitry than unrestricted access
while D2 receptor binding is generally decreased (Colantuoni et al., to palatable foods. It remains unclear whether FA can be studied
2001; Spangler et al., 2004), although the mRNA expression for in animals, since animals in models of binge eating do not consis-
S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42 37

Table 1
The human and animal evidence for a model of food addiction based on the DSM-IV Criteria for Substance Use Disorder.

DSM-IV Criteria for Substance Use Food Addiction in Animal Models of Food Addiction in Humans
Disorder (APA, 2000) Binge Eating

Substance taken in larger amount and Seen consistently during binge Commonly reported by children (Merlo
for longer period than intended sessions (Corwin et al., 2011; de Jong et al., 2009; Pretlow, 2011) and adults
et al., 2013; Rada et al., 2005; (Gearhardt et al., 2009a; Gearhardt,
Ziauddeen et al., 2012; Ziauddeen and White et al., 2011; Gearhardt, Yokum
Fletcher, 2013). et al., 2011; Merlo et al., 2009)
Persistent desire or repeated – Commonly reported by children (Merlo
unsuccessful attempts to quit et al., 2009; Pretlow, 2011) and adults
(Gearhardt et al., 2009a,; Gearhardt,
White et al., 2011; Gearhardt, Yokum
et al., 2011; Merlo et al., 2009). Most
commonly reported symptom (Flint
et al., 2014). This is reported by almost
100% of overweight participants
(Eichen et al., 2013; Gearhardt et al.,
2013; Gearhardt et al., 2012).
Much time/activity to obtain, use and Increased motivation for palatable food Reported by adults (Gearhardt et al.,
recover (Dimitriou et al., 2000; Hajnal and 2009a,; Gearhardt, White et al., 2011;
Norgren, 2002; Hoebel et al., 2009; Gearhardt, Yokum et al., 2011; Merlo
Rada et al., 2005; Sahr et al., 2008; et al., 2009)
Wojnicki et al., 2006).
Important social, occupational or – –
recreational activities given up or
reduced
Use continues despite knowledge of One study showing binge eating prone Commonly reported by children
adverse consequences rats have increased foot shock (Pretlow, 2011) and by adults
tolerance for palatable food (Oswald (Gearhardt et al., 2009a,; Gearhardt,
et al., 2011). White et al., 2011; Gearhardt, Yokum
et al., 2011; Merlo et al., 2009)
Tolerance – Reported by 77% of participants in an
overweight-to-obese paediatric
sample (Pretlow, 2011) and commonly
observed in obese adults (Eichen et al.,
2013; Gearhardt et al., 2013; Gearhardt
et al., 2012).
Characteristic withdrawal symptoms; Observed in one study with sucrose –
substance taken to relieve withdrawal (Colantuoni et al., 2002). Not observed
in fat bingeing (Bocarsly et al., 2011).

tently exhibit addiction-like behaviours, other than uncontrolled sample was shown to occur in 6.7% of women and 3% of men
consumption, as shown in Table 1. in the general population (Pedram et al., 2013). In women, FA
appears to be more prevalent between 45 and 61 years of age and
is most common in women between 45 and 49 with a BMI > 35
7. Measuring food addiction in humans (Flint et al., 2014). This may be associated with perimenopausal
changes in female sex hormones, which have been shown to alter
There is a growing body of evidence that a subset of indi- food intake, although further research is required to investigate
viduals with disordered eating display addiction-like behaviours this. It is estimated that approximately 15–25% of obese patients
in response to foods. The Yale Food Addiction Scale (YFAS) was meet the YFAS criteria for FA (Brunault et al., 2016; Eichen, Lent,
designed in 2009 (Gearhardt, Corbin, & Brownell, 2009) to investi- Goldbacher, & Foster, 2013; Gearhardt, Boswell et al., 2014; Lent,
gate the prevalence and comorbidity of addictive-like behaviours Eichen, Goldbacher, Wadden, & Foster, 2014). However, it should
specific to food in humans. It is a self-report measure that is based be noted that both these studies have been fairly small and may not
on the DSM-IV criteria for substance dependence (shown in Table 1 be representative (Yau et al., 2014).
below). While there has been some debate regarding the external The number of YFAS symptoms positively correlates with BMI
validity of the scale (Davis, Curtis et al., 2011; Gearhardt, 2013; (Flint et al., 2014; Gearhardt, Boswell et al., 2014; Meule, 2011;
Gearhardt and Yokum, 2012; Pursey, Collins, Stanwell, & Burrows, Pedram et al., 2013; Schulte, Joyner, Potenza, Grilo, & Gearhardt,
2015; Yau, Gottlieb, Krasna, & Potenza, 2014), it has been shown 2015), although 8.8–11.4% of individuals who meet the FA crite-
to be internally valid and reliably identifies a subset of individuals ria are not overweight or obese (Meule, 2011). Higher lifetime BMI
who compulsively overeat and struggle with weight management. and lower age of first diet were also positively associated with YFAS
The most common symptom reported on the YFAS is repeated scores (Gearhardt, Boswell et al., 2014; Gearhardt, White, Masheb,
unsuccessful attempts to restrict food intake, and almost 100% of & Grilo, 2013). There is mixed evidence regarding whether indi-
obese individuals will report this criterion (Brunault et al., 2016; viduals with FA experience poorer outcomes during weight loss
Meule, 2011; Meule & Gearhardt, 2014a). This criterion is also interventions (Clark & Saules, 2013; Lent et al., 2014). While indi-
most widely reported when FA is investigated in children (Merlo, viduals who meet the criteria for FA often report that they are
Klingman, Malasanos, & Silverstein, 2009). Another commonly impulsive (Davis, Curtis et al., 2011) their impulsivity is no different
reported criterion is continued consumption despite adverse con- to controls when tested behaviourally, although they do respond
sequences (Meule, 2011; Meule & Gearhardt, 2014a). more quickly to food cues (Meule, Lutz, Vögele, & Kübler, 2012).
The overall prevalence estimate for FA in the adult population is There are limited human studies linking YFAS scores with differ-
between 5.4 and 25.7% (Canada and USA respectively) (Gearhardt, ences in brain function and structure. An fMRI study has indicated
Boswell et al., 2014; Pedram et al., 2013), and in the Canadian
38 S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42

that YFAS scores correlate with increased BOLD signalling in parts that FA may be a more severe form of BED, this has been challenged
of the brain involved in emotional processing, reward evaluation since impaired control over eating behaviour does not necessarily
and decision making in response to anticipated intake of highly have to be limited to a specific type of eating episode (Begin et al.,
palatable food. Specifically, high YFAS scorers exhibit increased 2012; Curtis & Davis, 2014; Hebebrand et al., 2014).
BOLD signalling in the caudate, which contains the NAc (Gearhardt,
Yokum et al., 2011). A recent study has revealed links between FA
9. Food addiction and stress
symptomology and genes that are associated with elevated DA sig-
nalling (Davis et al., 2013) although another study using naltrexone
Despite a large body of literature showing strong reciprocal rela-
induced cortisol and nausea indicates that FA may be associated
tionships between addiction behaviours and the stress response in
with changes in the opioid signalling pathways (Daubenmier et al.,
substance abuse, little research has been conducted into the role of
2014).
stress in FA. There is considerable crosstalk between feeding and
Overall, while the YFAS scale does reliably identify a group of
stress systems, with several regions playing a role in both feed-
individuals who suffer from compulsive overeating, whether this
ing and stress such as the NAc and LHA (Maniam & Morris, 2012;
group is behaviourally distinct from other people with disordered
Morris, Beilharz, Maniam, Reichelt, & Westbrook, 2014a; Sominsky
eating has been called into question. It should be noted that YFAS
& Spencer, 2014). Moreover, one of the major consequences of
scores correlate highly with other measures of disordered eating,
stressor exposure is altered feeding. It has been hypothesised that
particularly binge eating disorder (BED) (Gearhardt et al., 2013;
people overeat highly palatable “comfort” foods to reduce the activ-
Meule & Gearhardt, 2014a; Schulte et al., 2016).
ity in the chronic stress-response circuitry (Dallman et al., 2003;
Parylak, Koob, & Zorrilla, 2011; Pecoraro, Reyes, Gomez, Bhargava,
& Dallman, 2004), and using this model FA may be understood as a
8. The relationship between food addiction and binge
disorder involving a dysregulated stress response where compul-
eating in humans
sive overeating functions as a coping mechanism.
In individuals with FA, there have been limited studies into the
Of all disordered eating behaviours, binge eating is one of the
role of stress. The intensity of routine stress was found to be higher
most strongly associated with YFAS scores, which is of great inter-
in students with FA (Okasaka, Morita, Nakatani, & Fujisawa, 2008)
est considering the conclusions we can draw from animal models.
and type 2 diabetics with FA have higher levels of depression, anxi-
Every animal model of FA requires intermittent access to palat-
ety and stress than type 2 diabetics without FA (Raymond & Lovell,
able food, leading to bingeing episodes, to induce addiction-like
2016). When combined, BMI and FA score accounted for 58% of the
behaviours. BED has a number of behavioural similarities to sub-
variance in stress score (Raymond & Lovell, 2016).
stance dependence, and is often treated using the same procedures
Post-traumatic stress disorder (PTSD) has been shown to be
(Cassin & von Ranson, 2007; Davis, 2009; Meule, 2011).
associated with FA and eating disorder symptomology in a group of
In people, FA scores correlate very highly with instances of binge
mostly male veterans (Mitchell & Wolf, 2016). In a study of female
eating (Brunault et al., 2016; Clark & Saules, 2013; Davis, Curtis
nurses, the FA prevalence was 6% in women with no lifetime PTSD
et al., 2011; Gearhardt et al., 2013; Meule & Gearhardt, 2014a;
symptoms, increasing to 18% in women reporting 6–7 PTSD symp-
Potenza, 2015) and YFAS scores account for a significant proportion
toms. After adjusting for age, PTSD symptoms were associated with
of the variance in binge eating scores after emotional eating and dis-
the prevalence of FA in a dose-dependent manner (Mason et al.,
ordered eating behaviour have been controlled for (Clark & Saules,
2014).
2013; Gearhardt et al., 2013). This is unsurprising since FA as mea-
While all these studies underscore potential associations
sured by the YFAS and BED have considerable behavioural overlap,
between stress, stress disorders and FA, these studies do not com-
including loss of control over food intake and continued consump-
ment on causality. While studies of drug addiction have shown
tion in the face of negative consequences (Gearhardt, White, &
that exposure to stressors can drive addiction behaviours, caus-
Potenza, 2011; Schulte et al., 2016). Approximately half the BED
ing relapse and reducing withdrawal symptoms, this has not been
population meet the criteria for FA (Begin et al., 2012; Gearhardt
replicated in FA. Further research is required to clarify the role of
et al., 2013; Gearhardt et al., 2012; Gearhardt, White et al., 2011)
stress in the epidemiology and expression of FA.
although a recent study has suggested that FA may be more closely
related to bulimia nervosa (Gearhardt, Boswell et al., 2014).
There is some evidence that binge eaters have underlying dif- 10. Conclusions
ferences in their reward circuitry: they have a unique D2 receptor
expression which was postulated to make them hypersensitive to While the reward circuitry that is impacted by drugs of addic-
reward (Davis et al., 2008, 2012). Blocking DA reuptake during tion is prominent in determining food intake, and is influenced
exposure to food cues results in brain increases in DA in individuals by highly palatable foods and diet-induced obesity, it remains
with BED only (Wang et al., 2011). Despite these signs of increased unclear whether these changes can be considered as a type of
sensitivity, another study has found that BED patients show less addiction. Only a subset of obese animals and people display any
striatal BOLD signalling relative to obese individuals without BED of the behavioural characteristics associated with addiction, and
in response to monetary rewards (Balodis et al., 2013). Differences this behavioural phenotype appears to be closely associated with
in opioid signalling may also characterise binge eaters: naltrexone- binge eating rather than a distinct disorder. Further research should
induced nausea has been shown to be associated with binge eating be conducted to determine whether YFAS scores correlate with a
(Daubenmier et al., 2014). distinct behavioural phenotype, and whether these behaviours are
Since the YFAS was developed the DSM-5 has been released. associated with differences in human brain structure and function.
One study has revised the YFAS to be more in line with the current While it is clear that the mesolimbic reward system is modulated by
diagnostic criteria for substance use disorder, which was shown to both short-term exposure to palatable food and diet-induced obe-
increase the likelihood that patients with BED will meet the criteria sity similarly to acute and prolonged drug exposure respectively,
for FA (Curtis & Davis, 2014). the nexus between these reward circuitry changes and addiction-
Despite the large correlations between binge eating and FA, not like behaviour towards food warrants further research. A series
all patients with BED have FA and not all individuals who meet the of well-designed animal studies comparing mesolimbic changes
YFAS criteria for FA have BED. While some studies have suggested following exposure to drugs of abuse and highly palatable foods,
S.-J. Leigh, M.J. Morris / Biological Psychology 131 (2018) 31–42 39

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