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Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis

BACKGROUND/OBJECTIVES: The salience network (SN) comprises brain regions that evaluate cues in the external environment in light of internal signals. We examined the SN response to meal intake and potential genetic and acquired influences on SN function. SUBJECTS/METHODS: Monozygotic (MZ; 40 pairs)...

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Autores principales: Sewaybricker, Leticia E., Melhorn, Susan J., Askren, Mary K., Webb, Mary F., Tyagi, Vidhi, De Leon, Mary Rosalynn B., Grabowski, Thomas J., Seeley, William W., Schur, Ellen A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6785381/
https://www.ncbi.nlm.nih.gov/pubmed/30967608
http://dx.doi.org/10.1038/s41366-019-0361-9
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author Sewaybricker, Leticia E.
Melhorn, Susan J.
Askren, Mary K.
Webb, Mary F.
Tyagi, Vidhi
De Leon, Mary Rosalynn B.
Grabowski, Thomas J.
Seeley, William W.
Schur, Ellen A.
author_facet Sewaybricker, Leticia E.
Melhorn, Susan J.
Askren, Mary K.
Webb, Mary F.
Tyagi, Vidhi
De Leon, Mary Rosalynn B.
Grabowski, Thomas J.
Seeley, William W.
Schur, Ellen A.
author_sort Sewaybricker, Leticia E.
collection PubMed
description BACKGROUND/OBJECTIVES: The salience network (SN) comprises brain regions that evaluate cues in the external environment in light of internal signals. We examined the SN response to meal intake and potential genetic and acquired influences on SN function. SUBJECTS/METHODS: Monozygotic (MZ; 40 pairs) and dizygotic (15 pairs) twins had body composition and plasma metabolic profile evaluated (glucose, insulin, leptin, ghrelin and GLP-1). Twins underwent resting-state functional magnetic resonance imaging (fMRI) scans before and after a standardized meal. The strength of SN connectivity was analyzed pre- and post-meal and the percentage change elicited by a meal was calculated. A multi-echo T2 MRI scan measured T2 relaxation time, a radiologic index of gliosis, in the mediobasal hypothalamus (MBH) and control regions. Statistical approaches included intraclass correlations (ICC) to investigate genetic influences and within-pair analyses to exclude genetic confounders. RESULTS: SN connectivity was reduced by meal ingestion (β=−0.20; P<0.001). Inherited influences on both pre- and post-meal connectivity were present (ICC MZ twins 26%, P<0.05 and 47%, P<0.001, respectively), but not percentage change in response to the meal. SN connectivity in response to a meal did not differ between participants with obesity and of normal weight (χ2(1)=0.93; P=0.33). However, when participants were classified as having high or low signs of MBH gliosis, the high MBH gliosis group failed to reduce the connectivity in response to a meal (z=−1.32; P=0.19). Excluding genetic confounders, the percentage change in SN connectivity by a meal correlated to body fat percentage (r=0.24; P<0.01). CONCLUSIONS: SN connectivity was reduced by a meal, indicating potential participation of the SN in control of feeding. The strength of SN connectivity is inherited, but the degree to which SN connectivity is reduced by eating appears to be influenced by adiposity and the presence of hypothalamic gliosis.
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spelling pubmed-67853812019-12-22 Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis Sewaybricker, Leticia E. Melhorn, Susan J. Askren, Mary K. Webb, Mary F. Tyagi, Vidhi De Leon, Mary Rosalynn B. Grabowski, Thomas J. Seeley, William W. Schur, Ellen A. Int J Obes (Lond) Article BACKGROUND/OBJECTIVES: The salience network (SN) comprises brain regions that evaluate cues in the external environment in light of internal signals. We examined the SN response to meal intake and potential genetic and acquired influences on SN function. SUBJECTS/METHODS: Monozygotic (MZ; 40 pairs) and dizygotic (15 pairs) twins had body composition and plasma metabolic profile evaluated (glucose, insulin, leptin, ghrelin and GLP-1). Twins underwent resting-state functional magnetic resonance imaging (fMRI) scans before and after a standardized meal. The strength of SN connectivity was analyzed pre- and post-meal and the percentage change elicited by a meal was calculated. A multi-echo T2 MRI scan measured T2 relaxation time, a radiologic index of gliosis, in the mediobasal hypothalamus (MBH) and control regions. Statistical approaches included intraclass correlations (ICC) to investigate genetic influences and within-pair analyses to exclude genetic confounders. RESULTS: SN connectivity was reduced by meal ingestion (β=−0.20; P<0.001). Inherited influences on both pre- and post-meal connectivity were present (ICC MZ twins 26%, P<0.05 and 47%, P<0.001, respectively), but not percentage change in response to the meal. SN connectivity in response to a meal did not differ between participants with obesity and of normal weight (χ2(1)=0.93; P=0.33). However, when participants were classified as having high or low signs of MBH gliosis, the high MBH gliosis group failed to reduce the connectivity in response to a meal (z=−1.32; P=0.19). Excluding genetic confounders, the percentage change in SN connectivity by a meal correlated to body fat percentage (r=0.24; P<0.01). CONCLUSIONS: SN connectivity was reduced by a meal, indicating potential participation of the SN in control of feeding. The strength of SN connectivity is inherited, but the degree to which SN connectivity is reduced by eating appears to be influenced by adiposity and the presence of hypothalamic gliosis. 2019-04-09 2020-01 /pmc/articles/PMC6785381/ /pubmed/30967608 http://dx.doi.org/10.1038/s41366-019-0361-9 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Sewaybricker, Leticia E.
Melhorn, Susan J.
Askren, Mary K.
Webb, Mary F.
Tyagi, Vidhi
De Leon, Mary Rosalynn B.
Grabowski, Thomas J.
Seeley, William W.
Schur, Ellen A.
Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis
title Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis
title_full Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis
title_fullStr Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis
title_full_unstemmed Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis
title_short Salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis
title_sort salience network connectivity is reduced by a meal and influenced by genetic background and hypothalamic gliosis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6785381/
https://www.ncbi.nlm.nih.gov/pubmed/30967608
http://dx.doi.org/10.1038/s41366-019-0361-9
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