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

Abstract 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 pathophysiol...

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Autores principales: Camillo Porcaro, Antonio Di Renzo, Emanuele Tinelli, Giorgio Di Lorenzo, Stefano Seri, Cherubino Di Lorenzo, Vincenzo Parisi, Francesca Caramia, Marco Fiorelli, Vittorio Di Piero, Francesco Pierelli, Gianluca Coppola
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:5a3c26301775468d9129c676c05d0a762021-12-02T18:14:00ZHypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks10.1038/s41598-021-98213-32045-2322https://doaj.org/article/5a3c26301775468d9129c676c05d0a762021-09-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-98213-3https://doaj.org/toc/2045-2322Abstract 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.Camillo PorcaroAntonio Di RenzoEmanuele TinelliGiorgio Di LorenzoStefano SeriCherubino Di LorenzoVincenzo ParisiFrancesca CaramiaMarco FiorelliVittorio Di PieroFrancesco PierelliGianluca CoppolaNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-11 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Camillo Porcaro
Antonio Di Renzo
Emanuele Tinelli
Giorgio Di Lorenzo
Stefano Seri
Cherubino Di Lorenzo
Vincenzo Parisi
Francesca Caramia
Marco Fiorelli
Vittorio Di Piero
Francesco Pierelli
Gianluca Coppola
Hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
description Abstract 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.
format article
author Camillo Porcaro
Antonio Di Renzo
Emanuele Tinelli
Giorgio Di Lorenzo
Stefano Seri
Cherubino Di Lorenzo
Vincenzo Parisi
Francesca Caramia
Marco Fiorelli
Vittorio Di Piero
Francesco Pierelli
Gianluca Coppola
author_facet Camillo Porcaro
Antonio Di Renzo
Emanuele Tinelli
Giorgio Di Lorenzo
Stefano Seri
Cherubino Di Lorenzo
Vincenzo Parisi
Francesca Caramia
Marco Fiorelli
Vittorio Di Piero
Francesco Pierelli
Gianluca Coppola
author_sort Camillo Porcaro
title 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_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_sort hypothalamic structural integrity and temporal complexity of cortical information processing at rest in migraine without aura patients between attacks
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/5a3c26301775468d9129c676c05d0a76
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