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Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks

The hypothalamus has been attributed an important role during the premonitory phase of a migraine attack. Less is known about the role played by the hypothalamus in the interictal period and its relationship with the putative neurocognitive networks previously identified in the pathophysiology of mi...

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Autores principales: Porcaro, Camillo, Di Renzo, Antonio, Tinelli, Emanuele, Di Lorenzo, Giorgio, Seri, Stefano, Di Lorenzo, Cherubino, Parisi, Vincenzo, Caramia, Francesca, Fiorelli, Marco, Di Piero, Vittorio, Pierelli, Francesco, Coppola, Gianluca
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8455544/
https://www.ncbi.nlm.nih.gov/pubmed/34548562
http://dx.doi.org/10.1038/s41598-021-98213-3
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author Porcaro, Camillo
Di Renzo, Antonio
Tinelli, Emanuele
Di Lorenzo, Giorgio
Seri, Stefano
Di Lorenzo, Cherubino
Parisi, Vincenzo
Caramia, Francesca
Fiorelli, Marco
Di Piero, Vittorio
Pierelli, Francesco
Coppola, Gianluca
author_facet Porcaro, Camillo
Di Renzo, Antonio
Tinelli, Emanuele
Di Lorenzo, Giorgio
Seri, Stefano
Di Lorenzo, Cherubino
Parisi, Vincenzo
Caramia, Francesca
Fiorelli, Marco
Di Piero, Vittorio
Pierelli, Francesco
Coppola, Gianluca
author_sort Porcaro, Camillo
collection PubMed
description The hypothalamus has been attributed an important role during the premonitory phase of a migraine attack. Less is known about the role played by the hypothalamus in the interictal period and its relationship with the putative neurocognitive networks previously identified in the pathophysiology of migraine. Our aim was to test whether the hypothalamic microstructure would be altered during the interictal period and whether this co-existed with aberrant connectivity at cortical level. We collected multimodal MRI data from 20 untreated patients with migraine without aura between attacks (MO) and 20 healthy controls (HC) and studied fractional anisotropy, mean (MD), radial (RD), and axial diffusivity of the hypothalamus ROI as a whole from diffusion tensor imaging (DTI). Moreover, we performed an exploratory analysis of the same DTI metrics separately for the anterior and posterior hypothalamic ROIs bilaterally. From resting-state functional MRI, we estimated the Higuchi’s fractal dimension (FD), an index of temporal complexity sensible to describe non-periodic patterns characterizing BOLD signature. Finally, we correlated neuroimaging findings with migraine clinical features. In comparison to HC, MO had significantly higher MD, AD, and RD values within the hypothalamus. These findings were confirmed also in the exploratory analysis on the sub-regions of the hypothalamus bilaterally, with the addition of lower FA values on the posterior ROIs. Patients showed higher FD values within the salience network (SN) and the cerebellum, and lower FD values within the primary visual (PV) network compared to HC. We found a positive correlation between cerebellar and SN FD values and severity of migraine. Our findings of hypothalamic abnormalities between migraine attacks may form part of the neuroanatomical substrate that predisposes the onset of the prodromal phase and, therefore, the initiation of an attack. The peculiar fractal dimensionality we found in PV, SN, and cerebellum may be interpreted as an expression of abnormal efficiency demand of brain networks devoted to the integration of sensory, emotional, and cognitive information related to the severity of migraine.
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spelling pubmed-84555442021-09-22 Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks Porcaro, Camillo Di Renzo, Antonio Tinelli, Emanuele Di Lorenzo, Giorgio Seri, Stefano Di Lorenzo, Cherubino Parisi, Vincenzo Caramia, Francesca Fiorelli, Marco Di Piero, Vittorio Pierelli, Francesco Coppola, Gianluca Sci Rep Article The hypothalamus has been attributed an important role during the premonitory phase of a migraine attack. Less is known about the role played by the hypothalamus in the interictal period and its relationship with the putative neurocognitive networks previously identified in the pathophysiology of migraine. Our aim was to test whether the hypothalamic microstructure would be altered during the interictal period and whether this co-existed with aberrant connectivity at cortical level. We collected multimodal MRI data from 20 untreated patients with migraine without aura between attacks (MO) and 20 healthy controls (HC) and studied fractional anisotropy, mean (MD), radial (RD), and axial diffusivity of the hypothalamus ROI as a whole from diffusion tensor imaging (DTI). Moreover, we performed an exploratory analysis of the same DTI metrics separately for the anterior and posterior hypothalamic ROIs bilaterally. From resting-state functional MRI, we estimated the Higuchi’s fractal dimension (FD), an index of temporal complexity sensible to describe non-periodic patterns characterizing BOLD signature. Finally, we correlated neuroimaging findings with migraine clinical features. In comparison to HC, MO had significantly higher MD, AD, and RD values within the hypothalamus. These findings were confirmed also in the exploratory analysis on the sub-regions of the hypothalamus bilaterally, with the addition of lower FA values on the posterior ROIs. Patients showed higher FD values within the salience network (SN) and the cerebellum, and lower FD values within the primary visual (PV) network compared to HC. We found a positive correlation between cerebellar and SN FD values and severity of migraine. Our findings of hypothalamic abnormalities between migraine attacks may form part of the neuroanatomical substrate that predisposes the onset of the prodromal phase and, therefore, the initiation of an attack. The peculiar fractal dimensionality we found in PV, SN, and cerebellum may be interpreted as an expression of abnormal efficiency demand of brain networks devoted to the integration of sensory, emotional, and cognitive information related to the severity of migraine. Nature Publishing Group UK 2021-09-21 /pmc/articles/PMC8455544/ /pubmed/34548562 http://dx.doi.org/10.1038/s41598-021-98213-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Porcaro, Camillo
Di Renzo, Antonio
Tinelli, Emanuele
Di Lorenzo, Giorgio
Seri, Stefano
Di Lorenzo, Cherubino
Parisi, Vincenzo
Caramia, Francesca
Fiorelli, Marco
Di Piero, Vittorio
Pierelli, Francesco
Coppola, Gianluca
Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
title Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
title_full Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
title_fullStr Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
title_full_unstemmed Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
title_short Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
title_sort hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8455544/
https://www.ncbi.nlm.nih.gov/pubmed/34548562
http://dx.doi.org/10.1038/s41598-021-98213-3
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