In vivo evidence of functional disconnection between brainstem monoaminergic nuclei and brain networks in multiple sclerosis.


Journal

Multiple sclerosis and related disorders
ISSN: 2211-0356
Titre abrégé: Mult Scler Relat Disord
Pays: Netherlands
ID NLM: 101580247

Informations de publication

Date de publication:
Nov 2021
Historique:
received: 30 04 2021
revised: 09 08 2021
accepted: 22 08 2021
pubmed: 31 8 2021
medline: 17 12 2021
entrez: 30 8 2021
Statut: ppublish

Résumé

brainstem monoaminergic (dopaminergic, noradrenergic, and serotoninergic) nuclei (BrMn) contain a variety of ascending neurons that diffusely project to the whole brain, crucially regulating normal brain function. BrMn are directly affected in multiple sclerosis (MS) by inflammation and neurodegeneration. Moreover, inflammation reduces the synthesis of monoamines. Aberrant monoaminergic neurotransmission contributes to the pathogenesis of MS and explains some clinical features of MS. We used resting-state functional MRI (RS-fMRI) to characterize abnormal patterns of BrMn functional connectivity (FC) in MS. BrMn FC was studied with multi-echo RS-fMRI in n = 68 relapsing-remitting MS patients and n = 39 healthy controls (HC), by performing a seed-based analysis, after producing standard space seed masks of the BrMn. FC was assessed between ventral tegmental area (VTA), locus coeruleus (LC), median raphe (MR), dorsal raphe (DR), and the rest of the brain and compared between MS patients and HC. Between-group comparisons were carried out only within the main effect observed in HC, setting p<0.05 family-wise-error corrected ( in HC, VTA displayed FC with the core regions of the default-mode network. As compared to HC, MS patients showed altered FC between VTA and posterior cingulate cortex (p<0.05 our study demonstrated in MS patients a functional disconnection between BrMn and cortical/subcortical efferent targets of central brain networks, possibly due to a loss or a dysregulation of BrMn neurons. This adds new information about how monoaminergic systems contribute to MS pathogenesis and suggests new potential therapeutic targets.

Sections du résumé

BACKGROUND BACKGROUND
brainstem monoaminergic (dopaminergic, noradrenergic, and serotoninergic) nuclei (BrMn) contain a variety of ascending neurons that diffusely project to the whole brain, crucially regulating normal brain function. BrMn are directly affected in multiple sclerosis (MS) by inflammation and neurodegeneration. Moreover, inflammation reduces the synthesis of monoamines. Aberrant monoaminergic neurotransmission contributes to the pathogenesis of MS and explains some clinical features of MS. We used resting-state functional MRI (RS-fMRI) to characterize abnormal patterns of BrMn functional connectivity (FC) in MS.
METHODS METHODS
BrMn FC was studied with multi-echo RS-fMRI in n = 68 relapsing-remitting MS patients and n = 39 healthy controls (HC), by performing a seed-based analysis, after producing standard space seed masks of the BrMn. FC was assessed between ventral tegmental area (VTA), locus coeruleus (LC), median raphe (MR), dorsal raphe (DR), and the rest of the brain and compared between MS patients and HC. Between-group comparisons were carried out only within the main effect observed in HC, setting p<0.05 family-wise-error corrected (
RESULTS RESULTS
in HC, VTA displayed FC with the core regions of the default-mode network. As compared to HC, MS patients showed altered FC between VTA and posterior cingulate cortex (p<0.05
CONCLUSIONS CONCLUSIONS
our study demonstrated in MS patients a functional disconnection between BrMn and cortical/subcortical efferent targets of central brain networks, possibly due to a loss or a dysregulation of BrMn neurons. This adds new information about how monoaminergic systems contribute to MS pathogenesis and suggests new potential therapeutic targets.

Identifiants

pubmed: 34461571
pii: S2211-0348(21)00491-0
doi: 10.1016/j.msard.2021.103224
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

103224

Informations de copyright

Copyright © 2021 Elsevier B.V. All rights reserved.

Auteurs

Tiziana Carandini (T)

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, United Kingdom; Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy; University of Milan, Dino Ferrari Center, Milan, Italy. Electronic address: tiziana.carandini@policlinico.mi.it.

Matteo Mancini (M)

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, United Kingdom; NeuroPoly Lab, Polytechnique Montreal, Montreal, Canada; CUBRIC, Cardiff University, Cardiff, United Kingdom.

Iulia Bogdan (I)

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, United Kingdom.

Charlotte L Rae (CL)

School of Psychology, University of Sussex, United Kingdom.

Andrew W Barritt (AW)

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, United Kingdom.

Marinella Clerico (M)

Clinical and Biological Sciences Department, University of Torino, Orbassano (TO) 10043, Italy.

Arjun Sethi (A)

Psychiatry, Psychology & Neuroscience, King's College London, United Kingdom.

Neil Harrison (N)

Department of Psychology and Department of Medicine, Cardiff, United Kingdom.

Waqar Rashid (W)

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, United Kingdom.

Elio Scarpini (E)

Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy; University of Milan, Dino Ferrari Center, Milan, Italy.

Daniela Galimberti (D)

Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy; University of Milan, Dino Ferrari Center, Milan, Italy.

Marco Bozzali (M)

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, United Kingdom; 'Rita Levi Montalcini' Department of Neuroscience, University of Torino, Turin, Italy.

Mara Cercignani (M)

Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, United Kingdom; Neuroimaging Laboratory, Santa Lucia Foundation IRCCS, Rome, Italy.

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