Dorsal Striatum and Its Limbic Connectivity Mediate Abnormal Anticipatory Reward Processing in Obesity

Nummenmaa, Lauri; Hirvonen, Jussi; Hannukainen, Jarna C.; Immonen, Heidi; Lindroos, Markus M.; Salminen, Paulina; Nuutila, Pirjo

doi:10.1371/journal.pone.0031089

Cited by 194 publications

(187 citation statements)

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“…This may be of particular concern in relation to the development and maintenance of obesity given the association between consumption of high energy-dense foods and subsequent weight gain (46)(47)(48) . These findings also reflect results from recent neuroimaging studies (49)(50)(51)(52)(53) that demonstrated greater activation of reward pathways in the brain on exposure to high energy-dense food images. Coupled with attentional bias studies, these neuroimaging studies provide a further insight into how eating behaviours may be affected by potential dysregulation in areas of the brain involved in processing the rewarding properties of foods.…”

Section: Effects Of Energy Density Of Food-related Cuessupporting

confidence: 86%

Attentional bias to food-related visual cues: is there a role in obesity?

et al. 2014

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The incentive sensitisation model of obesity suggests that modification of the dopaminergic associated reward systems in the brain may result in increased awareness of food-related visual cues present in the current food environment. Having a heightened awareness of these visual food cues may impact on food choices and eating behaviours with those being most aware of or demonstrating greater attention to food-related stimuli potentially being at greater risk of overeating and subsequent weight gain. To date, research related to attentional responses to visual food cues has been both limited and conflicting. Such inconsistent findings may in part be explained by the use of different methodological approaches to measure attentional bias and the impact of other factors such as hunger levels, energy density of visual food cues and individual eating style traits that may influence visual attention to food-related cues outside of weight status alone. This review examines the various methodologies employed to measure attentional bias with a particular focus on the role that attentional processing of food-related visual cues may have in obesity. Based on the findings of this review, it appears that it may be too early to clarify the role visual attention to foodrelated cues may have in obesity. Results however highlight the importance of considering the most appropriate methodology to use when measuring attentional bias and the characteristics of the study populations targeted while interpreting results to date and in designing future studies.Incentive sensitisation: Weight status: Eye tracking: Visual probe: Stroop Prevalence of overweight and obesity has now reached epidemic proportions with more than 1·4 billion adults considered as overweight and of these, over 500 million being obese worldwide (1) . On a fundamental level the cause of obesity is linked to an imbalance of energy intake v. energy expenditure; however, it is now evident that obesity is a multifactorial condition that arises from interactions between genetic and environmental factors (2) . One such factor is the present 'obesogenic' environment that is characterised by a wealth of highly palatable, energy-dense foods (3) . These foods are heavily represented in the visual environment for example, through advertising and it has been suggested that frequent exposure to these forms of food-related cues may impact on eating behaviours and food choices (4)(5)(6) .According to the theory of incentive sensitisation, 'addictive substances' modify reward-related pathways in the brain leading to hypersensitisation of rewardrelated stimuli (7) . This results in increased salience to reward-related stimuli resulting in these stimuli becoming more 'attention grabbing'. It has been proposed that this heightened awareness is the consequence of repeated exposure to a particular stimulus and the association between the stimulus and a rewarding experience, which results in related cues becoming salient. The stimulus related to the rewarding experience may then attract g...

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Section: Effects Of Energy Density Of Food-related Cuessupporting

confidence: 86%

Attentional bias to food-related visual cues: is there a role in obesity?

et al. 2014

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“…Postprandially, AA and TT subjects exhibited a differential relationship between postprandial acyl-ghrelin suppression and BOLD responses to food-related images within brain regions involved in visual attention and in encoding visual cue incentive value (44) and integrative/executive decision making. In addition, divergent acyl-ghrelin suppression and BOLD responses to hedonic food cues were observed within the right caudate nucleus, a region implicated in controlling incentive motivation, anticipatory food reward, and food craving (45). Collectively, these results show that the FTO genotype alters CNS responsivity to circulating ghrelin levels.…”

Section: Figurementioning

confidence: 72%

“…This effect was driven by a positive relationship between the BOLD response within these regions and meal-induced acyl-ghrelin suppression in the TT subjects, while the AA subjects displayed a negative relationship (Figure 4, E and F). In response to high-calorie images, the AA and TT subjects exhibited a significantly divergent response within the right caudate nucleus (z = 3.91 [22,8,18]) ( Figure 4G), a brain region that controls incentive motivation and that has been shown to exhibit an increased BOLD response to hedonic food images in obese compared with normal-weight subjects (45). In AA subjects, the BOLD response within the caudate was positively related with postprandial acyl-ghrelin suppression, whereas in TT subjects, a negative relationship was observed (Figure 4, H and I).…”

Section: Figurementioning

confidence: 99%

A link between FTO, ghrelin, and impaired brain food-cue responsivity

Karra

O’Daly

Choudhury³

et al. 2013

J. Clin. Invest.

334

323

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Polymorphisms in the fat mass and obesity-associated gene (FTO) are associated with human obesity and obesity-prone behaviors, including increased food intake and a preference for energy-dense foods. FTO demethylates N 6 -methyladenosine, a potential regulatory RNA modification, but the mechanisms by which FTO predisposes humans to obesity remain unclear. In adiposity-matched, normal-weight humans, we showed that subjects homozygous for the FTO "obesity-risk" rs9939609 A allele have dysregulated circulating levels of the orexigenic hormone acyl-ghrelin and attenuated postprandial appetite reduction. Using functional MRI (fMRI) in normal-weight AA and TT humans, we found that the FTO genotype modulates the neural responses to food images in homeostatic and brain reward regions. Furthermore, AA and TT subjects exhibited divergent neural responsiveness to circulating acyl-ghrelin within brain regions that regulate appetite, reward processing, and incentive motivation. In cell models, FTO overexpression reduced ghrelin mRNA N 6 -methyladenosine methylation, concomitantly increasing ghrelin mRNA and peptide levels. Furthermore, peripheral blood cells from AA human subjects exhibited increased FTO mRNA, reduced ghrelin mRNA N 6 -methyladenosine methylation, and increased ghrelin mRNA abundance compared with TT subjects. Our findings show that FTO regulates ghrelin, a key mediator of ingestive behavior, and offer insight into how FTO obesity-risk alleles predispose to increased energy intake and obesity in humans.Introduction FTO is an AlkB-like 2-oxoglutarate-dependent nucleic acid demethylase of uncertain cellular function (1). Genome-wide association studies (GWAS) have reliably established that SNPs within the first intron of FTO are robustly associated with increased BMI and adiposity across different ages and populations (2-6). Subjects homozygous for the "obesity-risk" A allele of FTO rs9939609 have a 1.7-fold increased risk for obesity compared with subjects homozygous for the low-risk T allele (2). Evidence to date suggests that the association between SNPs in FTO and BMI is predominantly driven by increased energy intake. Subjects homozygous for the obesity-risk A allele of rs9939609 exhibit overall increased ad libitum food-intake (7-9), particularly fat consumption (7, 9-11), and impaired satiety (12, 13). Furthermore, preschool AA children (AA denotes homozygosity for the A obesity-risk allele in the rs9939609 FTO variant) exhibit obesity-prone eating behaviors, including increased food responsiveness and a tendency to eat in

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“…Increased amygdala responses to food cues in obese compared to healthy-weight individuals is one of the most replicated findings in the neuroimaging of obesity (e.g., [111,113]; see [16] for a review), including in children (e.g., [14]). External food sensitivity, i.e.…”

Section: Amygdala and Cue-induced Feedingmentioning

confidence: 94%

The anterior medial temporal lobes: Their role in food intake and body weight regulation

Coppin

2016

Physiology & Behavior

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• The amygdala and hippocampus play a major role in food intake and weight regulation.• These functions are far less known to cognitive and affective scientists.• This review uniquely expands on the interactions between these two brain structures. a b s t r a c t a r t i c l e i n f o The anterior medial temporal lobes are one of the most studied parts of the brain. Classically, their two main structures -the amygdalae and the hippocampi -have been linked to key cognitive and affective functions, related in particular to learning and memory. Based on abundant evidence, we will argue for an alternative but complementary point of view: they may also play a major role in food intake and body weight regulation. First, an overview is given of early clinical evidence in this line of thought. Subsequently, empirical evidence is presented on how food intake, including in the extreme case of obesity, may relate to amygdalian and hippocampal functioning. The focus is on the amygdala's role in processing the relevance of food stimuli, cue-induced feeding, and stress-induced eating and on the hippocampus' involvement in the use of interoceptive signals of hunger and satiety, as well as memory and inhibitory processes related to food intake. Additionally, an elaboration takes place on possible reciprocal links between food intake, body weight, and amygdala and hippocampus functioning. Finally, issues that seemed particularly critical for future research in the field are discussed.

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Dorsal Striatum and Its Limbic Connectivity Mediate Abnormal Anticipatory Reward Processing in Obesity

Cited by 194 publications

References 57 publications

Attentional bias to food-related visual cues: is there a role in obesity?

Attentional bias to food-related visual cues: is there a role in obesity?

A link between FTO, ghrelin, and impaired brain food-cue responsivity

The anterior medial temporal lobes: Their role in food intake and body weight regulation

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