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Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin
Weight gain is often associated with the pleasure of eating food rich in calories. This idea is based on the findings that people with obesity showed increased neural activity in the reward and motivation systems of the brain in response to food cues. Such correlations, however, overlook the possibi...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7884604/ https://www.ncbi.nlm.nih.gov/pubmed/33615220 http://dx.doi.org/10.1093/braincomms/fcab005 |
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author | Schmidt, Liane Medawar, Evelyn Aron-Wisnewsky, Judith Genser, Laurent Poitou, Christine Clément, Karine Plassmann, Hilke |
author_facet | Schmidt, Liane Medawar, Evelyn Aron-Wisnewsky, Judith Genser, Laurent Poitou, Christine Clément, Karine Plassmann, Hilke |
author_sort | Schmidt, Liane |
collection | PubMed |
description | Weight gain is often associated with the pleasure of eating food rich in calories. This idea is based on the findings that people with obesity showed increased neural activity in the reward and motivation systems of the brain in response to food cues. Such correlations, however, overlook the possibility that obesity may be associated with a metabolic state that impacts the functioning of reward and motivation systems, which in turn could be linked to reactivity to food and eating behaviour and weight gain. In a study involving 44 female participants [14 patients with obesity, aged 20–63 years (mean: 42, SEM: 3.2 years), and 30 matched lean controls, aged 22–60 years (mean: 37, SEM: 1.8 years)], we investigated how ventromedial prefrontal cortex seed-to-voxel resting-state connectivity distinguished between lean and obese participants at baseline. We used the results of this first step of our analyses to examine whether changes in ventromedial prefrontal cortex resting-state connectivity over 8 months could formally predict weight gain or loss. It is important to note that participants with obesity underwent bariatric surgery at the beginning of our investigation period. We found that ventromedial prefrontal cortex–ventral striatum resting-state connectivity and ventromedial–dorsolateral prefrontal cortex resting-state connectivity were sensitive to obesity at baseline. However, only the ventromedial prefrontal cortex–ventral striatum resting-state connectivity predicted weight changes over time using cross-validation, out-of-sample prediction analysis. Such an out-of-sample prediction analysis uses the data of all participants of a training set to predict the actually observed data in one independent participant in the hold-out validation sample and is then repeated for all participants. In seeking to explain the reason why ventromedial pre-frontal cortex–ventral striatum resting-state connectivity as the central hub of the brain’s reward and motivational system may predict weight change over time, we linked weight loss surgery-induced changes in ventromedial prefrontal cortex–ventral striatum resting-state connectivity to surgery-induced changes in homeostatic hormone regulation. More specifically, we focussed on changes in fasting state systemic leptin, a homeostatic hormone signalling satiety, and inhibiting reward-related dopamine signalling. We found that the surgery-induced increase in ventromedial prefrontal cortex–ventral striatum resting-state connectivity was correlated with a decrease in fasting-state systemic leptin. These findings establish the first link between individual differences in brain connectivity in reward circuits in a more tonic state at rest, weight change over time and homeostatic hormone regulation. |
format | Online Article Text |
id | pubmed-7884604 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-78846042021-02-19 Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin Schmidt, Liane Medawar, Evelyn Aron-Wisnewsky, Judith Genser, Laurent Poitou, Christine Clément, Karine Plassmann, Hilke Brain Commun Original Article Weight gain is often associated with the pleasure of eating food rich in calories. This idea is based on the findings that people with obesity showed increased neural activity in the reward and motivation systems of the brain in response to food cues. Such correlations, however, overlook the possibility that obesity may be associated with a metabolic state that impacts the functioning of reward and motivation systems, which in turn could be linked to reactivity to food and eating behaviour and weight gain. In a study involving 44 female participants [14 patients with obesity, aged 20–63 years (mean: 42, SEM: 3.2 years), and 30 matched lean controls, aged 22–60 years (mean: 37, SEM: 1.8 years)], we investigated how ventromedial prefrontal cortex seed-to-voxel resting-state connectivity distinguished between lean and obese participants at baseline. We used the results of this first step of our analyses to examine whether changes in ventromedial prefrontal cortex resting-state connectivity over 8 months could formally predict weight gain or loss. It is important to note that participants with obesity underwent bariatric surgery at the beginning of our investigation period. We found that ventromedial prefrontal cortex–ventral striatum resting-state connectivity and ventromedial–dorsolateral prefrontal cortex resting-state connectivity were sensitive to obesity at baseline. However, only the ventromedial prefrontal cortex–ventral striatum resting-state connectivity predicted weight changes over time using cross-validation, out-of-sample prediction analysis. Such an out-of-sample prediction analysis uses the data of all participants of a training set to predict the actually observed data in one independent participant in the hold-out validation sample and is then repeated for all participants. In seeking to explain the reason why ventromedial pre-frontal cortex–ventral striatum resting-state connectivity as the central hub of the brain’s reward and motivational system may predict weight change over time, we linked weight loss surgery-induced changes in ventromedial prefrontal cortex–ventral striatum resting-state connectivity to surgery-induced changes in homeostatic hormone regulation. More specifically, we focussed on changes in fasting state systemic leptin, a homeostatic hormone signalling satiety, and inhibiting reward-related dopamine signalling. We found that the surgery-induced increase in ventromedial prefrontal cortex–ventral striatum resting-state connectivity was correlated with a decrease in fasting-state systemic leptin. These findings establish the first link between individual differences in brain connectivity in reward circuits in a more tonic state at rest, weight change over time and homeostatic hormone regulation. Oxford University Press 2021-02-02 /pmc/articles/PMC7884604/ /pubmed/33615220 http://dx.doi.org/10.1093/braincomms/fcab005 Text en © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Original Article Schmidt, Liane Medawar, Evelyn Aron-Wisnewsky, Judith Genser, Laurent Poitou, Christine Clément, Karine Plassmann, Hilke Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin |
title | Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin |
title_full | Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin |
title_fullStr | Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin |
title_full_unstemmed | Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin |
title_short | Resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin |
title_sort | resting-state connectivity within the brain’s reward system predicts weight loss and correlates with leptin |
topic | Original Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7884604/ https://www.ncbi.nlm.nih.gov/pubmed/33615220 http://dx.doi.org/10.1093/braincomms/fcab005 |
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