Altered functional connectivity within the central reward network in overweight and obese women

Coveleskie, Kristen; Gupta, Abha R.; Kilpatrick, Lisa A.; Mayer, Emeran; Ashe-McNalley, Cody; Stains, Jean; Labus, Jennifer S.; Mayer, Emeran A.

doi:10.1038/nutd.2014.45

Cited by 70 publications

(64 citation statements)

References 55 publications

(86 reference statements)

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“…Studies using a seed‐based correlation analysis have also identified problems with functional integration in core regions of RSNs; however, these studies have not assessed whether there were disruptions in connectivity between large‐scale brain networks . The correlations between these large‐scale networks are thought to be more important than the activity of the RSNs themselves and to play a critical role in efficient, dynamic communication in the brain .…”

Section: Introductionmentioning

confidence: 99%

Altered Interactions Among Resting‐State Networks in Individuals with Obesity

Ding

et al. 2020

Obesity

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Objective The aim of this study was to investigate alterations in functional connectivity (FC) within and interactions between resting‐state networks involved in salience, executive control, and interoception in participants with obesity (OB). Methods Using resting‐state functional magnetic resonance imaging with independent component analysis and FC, alterations within and interactions between resting‐state networks in 35 OB and 35 normal‐weight controls (NW) were investigated. Results Compared with NW, OB showed reduced FC strength in the ventromedial prefrontal cortex and posterior cingulate cortex/precuneus within the default‐mode network, dorsal anterior cingulate cortex within the salience network (SN), bilateral dorsolateral prefrontal cortex‐angular gyrus within the frontoparietal network (FPN), and increased FC strength in the insula (INS) (Pfamilywise error < 0.0125). The dorsal anterior cingulate cortex FC strength was negatively correlated with craving for food cues, left dorsolateral prefrontal cortex FC strength was negatively correlated with Yale Food Addiction Scale scores, and right INS FC strength was positively correlated with craving for high‐calorie food cues. Compared with NW, OB also showed increased FC between the SN and FPN driven by altered FC of bilateral INS and anterior cingulate cortex‐angular gyrus. Conclusions Alterations in FC within and interactions between the SN, default‐mode network, and FPN might contribute to the high incentive value of food (craving), lack of control of overeating (compulsive overeating), and increased awareness of hunger (impaired interoception) in OB.

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Section: Introductionmentioning

confidence: 99%

Altered Interactions Among Resting‐State Networks in Individuals with Obesity

Ding

et al. 2020

Obesity

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“…Furthermore, structural differences in NAcc volume have been positively associated with body mass index (BMI) in adults (5,6). Because the development of the NAcc precedes the development of prefrontal control systems (7), this structure is suggested to play a key role in motivating and establishing unhealthy eating behaviors early in the lifespan.…”

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confidence: 99%

Genetic risk for obesity predicts nucleus accumbens size and responsivity to real-world food cues

Rapuano

Zieselman

Kelley

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Obesity is a major public health concern that involves an interaction between genetic susceptibility and exposure to environmental cues (e.g., food marketing); however, the mechanisms that link these factors and contribute to unhealthy eating are unclear. Using a well-known obesity risk polymorphism (FTO rs9939609) in a sample of 78 children (ages 9-12 y), we observed that children at risk for obesity exhibited stronger responses to food commercials in the nucleus accumbens (NAcc) than children not at risk. Similarly, children at a higher genetic risk for obesity demonstrated larger NAcc volumes. Although a recessive model of this polymorphism best predicted body mass and adiposity, a dominant model was most predictive of NAcc size and responsivity to food cues. These findings suggest that children genetically at risk for obesity are predisposed to represent reward signals more strongly, which, in turn, may contribute to unhealthy eating behaviors later in life.T he relationship between genes and sensitivity to environmental cues is elusive, yet it is paramount to understanding the development of potentially maladaptive human behaviors. The rising prevalence of obesity is a major public health concern that has been attributed to various factors, such as genetic susceptibility (1), and increases in the availability and marketing of calorie-dense foods (2). However, little is known about how genetic predisposition to obesity influences sensitivity to real-world food cues and contributes to the development of unhealthy eating behaviors.Previous neuroimaging studies have demonstrated that responses to food cues in reward-related regions of the brain, such as the nucleus accumbens (NAcc), predict weight gain in adulthood (3) and giving in to food temptations in daily life (4). Furthermore, structural differences in NAcc volume have been positively associated with body mass index (BMI) in adults (5, 6). Because the development of the NAcc precedes the development of prefrontal control systems (7), this structure is suggested to play a key role in motivating and establishing unhealthy eating behaviors early in the lifespan. Importantly, genetic factors are a known contributor to brain development (8) and may influence risky behaviors during childhood and adolescence by biasing the early development of anatomical structures underlying reward-related brain function.In addition, the notion that genes contribute to obesity has recently gained much attention. More specifically, the fat-mass and obesity-associated (FTO) rs9939609 polymorphism has been strongly related to increased BMI and adiposity across the lifespan, and is suggested to influence food intake and food choice, rather than energy expenditure (9-11). Those with two high-risk "A" alleles (AA) are at an enhanced risk for obesity compared with those with two low-risk "T" alleles (TT) or those who are heterozygous (AT) for the FTO rs9939609 polymorphism. Although the FTO gene is highly expressed in the brain (1), the mechanism by which this gene promotes unhealthy...

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“…The OFC plays a crucial role in hedonic and motivational aspects of reward and has been associated with addiction, which may be related to the function of response inhibition and encoding reward value . The OFC is connected to the central dopamine reward network (such as nucleus accumbens, caudate, and putamen) and is integral in controlling reward‐ and punishment‐related behavior . Additionally, the OFC has often been identified as the secondary gustatory cortex and linked with taste reward circuitry .…”

Section: Discussionmentioning

confidence: 62%

“…Furthermore, results from a diffusion tensor imaging (DTI) study suggest that there are extensive white matter tract connections between the ventral striatum and appetite‐related regions . As demonstrated in previous studies, the gray matter volume of the left ventral striatum was significantly greater in obese females than in normal‐weight females, and altered FC was also observed in the left ventral striatum . Accordingly, our findings of increased degree values in the left ventral striatum/caudate provide further evidence from the global FC view that the FC numbers between the left ventral striatum/caudate and appetite‐related function regions are increased.…”

Section: Discussionmentioning

confidence: 99%

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Integration of Neural Reward Processing and Appetite‐Related Signaling in Obese Females: Evidence From Resting‐State fMRI

Zhang

Yang

et al. 2019

Magnetic Resonance Imaging

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Background The reward‐related regions have been considered a crucial component in the regulation of eating behavior. Furthermore, appetite‐related regions associated with reward can influence eating behaviors through altered functional activity related to food in brain areas associated with emotion, memory, sensory processing, motor function, and cognitive control. Purpose To investigate the key nodes in obese females of reward‐related regions and, based on key nodes, to evaluate the directionality of functional connectivity between key nodes and appetite‐related regions. Study Type Prospective. Population Twenty‐eight obese and 28 normal‐weight female controls of similar age. Field Strength/Sequence 3.0 T MRI and echo planar imaging (EPI) sequence, 3D BRAVO sequence. Assessment The fMRI data preprocessing was based on the Data Processing & Analysis of Brain Imaging and Statistical Parametric Mapping 12. Degree centrality calculation was based on the GRETNA toolkit and granger causality analysis were based on the DynamicBC toolbox. Statistical Tests: Independent two‐sample t‐tests were used to assess the differences in demographic and clinical data between two groups. Two‐sample t‐tests were conducted to test the difference in degree centrality and effective connectivity of key nodes between two groups. Results Compared with normal‐weight controls, obese females showed an increased degree centrality in the left ventral striatum/caudate (t = 2.96808, P < 0.05) and decreased degree centrality in right orbitofrontal cortex (OFC) (t = –3.3558, P < 0.05). The obese females showed directional effective connectivity between left ventral striatum/caudate and several regions (left inferior temporal gyrus, fusiform gyrus, postcentral gyrus, and right precentral gyrus) (P < 0.05). Directional effective connectivity was also observed between the right OFC and several regions (left middle temporal gyrus, cuneus, OFC, superior temporal gyrus, middle frontal gyrus, and right inferior parietal lobule) (P < 0.05). Data Conclusion The left ventral striatum/caudate and right OFC are key nodes in reward‐related regions. The key nodes with reward processing mainly enhance visual processing of information and further participate in cognitive, attention, and sensorimotor processing. Level of Evidence: 1. Technical Efficacy: Stage 4. J. Magn. Reson. Imaging 2019;50:541–551.

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Altered functional connectivity within the central reward network in overweight and obese women

Cited by 70 publications

References 55 publications

Altered Interactions Among Resting‐State Networks in Individuals with Obesity

Altered Interactions Among Resting‐State Networks in Individuals with Obesity

Genetic risk for obesity predicts nucleus accumbens size and responsivity to real-world food cues

Integration of Neural Reward Processing and Appetite‐Related Signaling in Obese Females: Evidence From Resting‐State fMRI

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