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A systematic review of resting-state functional connectivity in obesity: Refining current neurobiological frameworks and methodological considerations moving forward

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Abstract

Obesity is the second most common cause of preventable morbidity worldwide. Resting-state functional magnetic resonance imaging (fMRI) has been used extensively to characterise altered communication between brain regions in individuals with obesity, though findings from this research have not yet been systematically evaluated within the context of prominent neurobiological frameworks. This systematic review aggregated resting-state fMRI findings in individuals with obesity and evaluated the contribution of these findings to current neurobiological models. Findings were considered in relation to a triadic model of problematic eating, outlining disrupted communication between reward, inhibitory, and homeostatic systems. We identified a pattern of consistently increased orbitofrontal and decreased insula cortex resting-state functional connectivity in individuals with obesity in comparison to healthy weight controls. BOLD signal amplitude was also increased in people with obesity across studies, predominantly confined to subcortical regions, including the hippocampus, amygdala, and putamen. We posit that altered orbitofrontal cortex connectivity may be indicative of a shift in the valuation of food-based rewards and that dysfunctional insula connectivity likely contributes to altered homeostatic signal processing. Homeostatic violation signals in obesity may be maintained despite satiety, thereby ‘hijacking’ the executive system and promoting further food intake. Moving forward, we provide a roadmap for more reliable resting-state and task-based functional connectivity experiments, which must be reconciled within a common framework if we are to uncover the interplay between psychological and biological factors within current theoretical frameworks.

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Availability of data and material

Raw data can be made available upon request.

Code availability

A MATLAB file containing analyses steps can be made available upon request.

Abbreviations

AAL:

Automatic Anatomical Labelling

ALFF:

Amplitude of Low Frequency Fluctuation

BMI:

Body Mass Index

BOLD:

Blood Oxygenated Level Dependency

DEBQ:

Dutch Eating Behaviour Questionnaire

dlPFC:

Dorsolateral Prefrontal Cortex

DMN:

Default Mode Network

FC:

Functional Connectivity

fMRI:

Functional Magnetic Resonance Imaging

FPN:

Frontoparietal Network

BES:

Binge Eating Scale

HADS:

Hospital Anxiety and Depression Scale

ICA:

Independent Component Analysis

MNI:

Montreal Neurological Institute

OFC:

Orbitofrontal Cortex

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

ROI:

Region of Interest

SN:

Salience Network

SPSRQ:

The Sensitivity to Punishment and Sensitivity to Reward Questionnaire

YFAS:

Yale Food Addiction Scale

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Funding

NP is supported by a Deakin University Postgraduate Research Scholarship (DUPRS). HA is supported by the Special Research Fund of Ghent University (grant No. BOF16/DOC/282; https://www.ugent.be/), and a grant for long stay abroad from the Fund for Scientific Research-Flanders (FWO–V; awarded to HA; http://www.fwo.be). TS is supported by a NHMRC/MRFF Investigator Grant (MRF1193736), a BBRF Young Investigator Grant, and a University of Melbourne McKenzie Fellowship. The authors Rebecca Clohesy and Leonie Duehlmeyer received no specific funding for this work.

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Authors and Affiliations

  1. Cognitive Neuroscience Unit, School of Psychology, Deakin University, Melbourne Burwood Campus, VIC, Australia

    Nicholas Parsons

  2. Melbourne School of Psychological Sciences, University of Melbourne, Parkville, VIC, Australia

    Trevor Steward

  3. School of Psychology, Deakin University, Melbourne Burwood Campus, VIC, Australia

    Rebecca Clohesy

  4. Department of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada

    Hannes Almgren

  5. Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada

    Hannes Almgren

  6. Department of Data Analysis, Faculty of Psychology and Educational Sciences, Ghent University, Ghent, Belgium

    Hannes Almgren

  7. Australian Catholic University, Melbourne Campus, VIC, Australia

    Leonie Duehlmeyer

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  3. Rebecca Clohesy
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  5. Leonie Duehlmeyer
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Correspondence to Leonie Duehlmeyer.

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Supplementary Information

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11154_2021_9665_MOESM1_ESM.tiff

Supplementary file1 Online Resource Fig. 1. PRISMA Flow Diagram Screening process applied to identified studies including identification, screening, eligibility assessments. A total of 1045 studies were identified, of which 24 met inclusion criteria (TIFF 964 KB)

11154_2021_9665_MOESM2_ESM.tiff

Supplementary file2 Online Resource Fig. 2. Aggregated MRI acquisition parameters. This figure shows aggregated MRI scanning parameters: Panel A shows repetition time in milliseconds; Panel B shows scan time in minutes; Panel C shows the number of volumes. In most studies, scans were acquired with 2000 ms repetition times using between 150 and 200 EPI volumes. Over 50% of studies used a scan duration of between 6 and 7 min (TIFF 2580 KB)

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Parsons, N., Steward, T., Clohesy, R. et al. A systematic review of resting-state functional connectivity in obesity: Refining current neurobiological frameworks and methodological considerations moving forward. Rev Endocr Metab Disord 23, 861–879 (2022). https://doi.org/10.1007/s11154-021-09665-x

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