Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI

Despite remarkable advances in mapping the functional connectivity of the cortex, the functional connectivity of subcortical regions is understudied in living humans. This is the case for brainstem nuclei that control vital processes, such as autonomic, limbic, nociceptive and sensory functions. Thi...

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Main Authors: Simone Cauzzo, Kavita Singh, Matthew Stauder, María Guadalupe García-Gomar, Nicola Vanello, Claudio Passino, Jeffrey Staab, Iole Indovina, Marta Bianciardi
Format: Article
Language:English
Published: Elsevier 2022-04-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922000544
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author Simone Cauzzo
Kavita Singh
Matthew Stauder
María Guadalupe García-Gomar
Nicola Vanello
Claudio Passino
Jeffrey Staab
Iole Indovina
Marta Bianciardi
author_facet Simone Cauzzo
Kavita Singh
Matthew Stauder
María Guadalupe García-Gomar
Nicola Vanello
Claudio Passino
Jeffrey Staab
Iole Indovina
Marta Bianciardi
author_sort Simone Cauzzo
collection DOAJ
description Despite remarkable advances in mapping the functional connectivity of the cortex, the functional connectivity of subcortical regions is understudied in living humans. This is the case for brainstem nuclei that control vital processes, such as autonomic, limbic, nociceptive and sensory functions. This is because of the lack of precise brainstem nuclei localization, of adequate sensitivity and resolution in the deepest brain regions, as well as of optimized processing for the brainstem. To close the gap between the cortex and the brainstem, on 20 healthy subjects, we computed a correlation-based functional connectome of 15 brainstem nuclei involved in autonomic, limbic, nociceptive, and sensory function (superior and inferior colliculi, ventral tegmental area-parabrachial pigmented nucleus complex, microcellular tegmental nucleus-prabigeminal nucleus complex, lateral and medial parabrachial nuclei, vestibular and superior olivary complex, superior and inferior medullary reticular formation, viscerosensory motor nucleus, raphe magnus, pallidus, and obscurus, and parvicellular reticular nucleus – alpha part) with the rest of the brain. Specifically, we exploited 1.1mm isotropic resolution 7 Tesla resting-state fMRI, ad-hoc coregistration and physiological noise correction strategies, and a recently developed probabilistic template of brainstem nuclei. Further, we used 2.5mm isotropic resolution resting-state fMRI data acquired on a 3 Tesla scanner to assess the translatability of our results to conventional datasets. We report highly consistent correlation coefficients across subjects, confirming available literature on autonomic, limbic, nociceptive and sensory pathways, as well as high interconnectivity within the central autonomic network and the vestibular network. Interestingly, our results showed evidence of vestibulo-autonomic interactions in line with previous work. Comparison of 7 Tesla and 3 Tesla findings showed high translatability of results to conventional settings for brainstem-cortical connectivity and good yet weaker translatability for brainstem-brainstem connectivity. The brainstem functional connectome might bring new insight in the understanding of autonomic, limbic, nociceptive and sensory function in health and disease.
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spelling doaj.art-9ac034084290485ba891aadcc5b6010c2022-12-21T16:54:09ZengElsevierNeuroImage1095-95722022-04-01250118925Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRISimone Cauzzo0Kavita Singh1Matthew Stauder2María Guadalupe García-Gomar3Nicola Vanello4Claudio Passino5Jeffrey Staab6Iole Indovina7Marta Bianciardi8Brainstem Imaging Laboratory, Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Life Sciences Institute, Sant'Anna School of Advanced Studies, Pisa, Italy; Research Center E. Piaggio, University of Pisa, Pisa, Italy; Corresponding authors.Brainstem Imaging Laboratory, Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USABrainstem Imaging Laboratory, Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USABrainstem Imaging Laboratory, Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Escuela Nacional de Estudios Superiores, Juriquilla, Universidad Nacional Autónoma de México, Querétaro, MéxicoDipartimento di Ingegneria dell'Informazione, University of Pisa, Pisa, ItalyLife Sciences Institute, Sant'Anna School of Advanced Studies, Pisa, Italy; Fondazione Toscana Gabriele Monasterio, Pisa, ItalyDepartment of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA; Department of Otorhinolaryngology – Head and Neck Surgery, Mayo Clinic, Rochester, MN, USADepartment of Biomedical and Dental Sciences and Morphofunctional Imaging, University of Messina, Italy; Laboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, Rome, ItalyBrainstem Imaging Laboratory, Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; Division of Sleep Medicine, Harvard University, Boston, MA USA; Corresponding authors.Despite remarkable advances in mapping the functional connectivity of the cortex, the functional connectivity of subcortical regions is understudied in living humans. This is the case for brainstem nuclei that control vital processes, such as autonomic, limbic, nociceptive and sensory functions. This is because of the lack of precise brainstem nuclei localization, of adequate sensitivity and resolution in the deepest brain regions, as well as of optimized processing for the brainstem. To close the gap between the cortex and the brainstem, on 20 healthy subjects, we computed a correlation-based functional connectome of 15 brainstem nuclei involved in autonomic, limbic, nociceptive, and sensory function (superior and inferior colliculi, ventral tegmental area-parabrachial pigmented nucleus complex, microcellular tegmental nucleus-prabigeminal nucleus complex, lateral and medial parabrachial nuclei, vestibular and superior olivary complex, superior and inferior medullary reticular formation, viscerosensory motor nucleus, raphe magnus, pallidus, and obscurus, and parvicellular reticular nucleus – alpha part) with the rest of the brain. Specifically, we exploited 1.1mm isotropic resolution 7 Tesla resting-state fMRI, ad-hoc coregistration and physiological noise correction strategies, and a recently developed probabilistic template of brainstem nuclei. Further, we used 2.5mm isotropic resolution resting-state fMRI data acquired on a 3 Tesla scanner to assess the translatability of our results to conventional datasets. We report highly consistent correlation coefficients across subjects, confirming available literature on autonomic, limbic, nociceptive and sensory pathways, as well as high interconnectivity within the central autonomic network and the vestibular network. Interestingly, our results showed evidence of vestibulo-autonomic interactions in line with previous work. Comparison of 7 Tesla and 3 Tesla findings showed high translatability of results to conventional settings for brainstem-cortical connectivity and good yet weaker translatability for brainstem-brainstem connectivity. The brainstem functional connectome might bring new insight in the understanding of autonomic, limbic, nociceptive and sensory function in health and disease.http://www.sciencedirect.com/science/article/pii/S10538119220005447 TeslaHuman functional connectomeBrainstemCentral autonomic networkVestibular network
spellingShingle Simone Cauzzo
Kavita Singh
Matthew Stauder
María Guadalupe García-Gomar
Nicola Vanello
Claudio Passino
Jeffrey Staab
Iole Indovina
Marta Bianciardi
Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI
NeuroImage
7 Tesla
Human functional connectome
Brainstem
Central autonomic network
Vestibular network
title Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI
title_full Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI
title_fullStr Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI
title_full_unstemmed Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI
title_short Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI
title_sort functional connectome of brainstem nuclei involved in autonomic limbic pain and sensory processing in living humans from 7 tesla resting state fmri
topic 7 Tesla
Human functional connectome
Brainstem
Central autonomic network
Vestibular network
url http://www.sciencedirect.com/science/article/pii/S1053811922000544
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