Unique spatiotemporal fMRI dynamics in the awake mouse brain

Human imaging studies have shown that spontaneous brain activity exhibits stereotypic spatiotemporal reorganization in awake, conscious conditions with respect to minimally conscious states. However, whether and how this phenomenon can be generalized to lower mammalian species remains unclear. Lever...

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Veröffentlicht in:Current biology 2022-02, Vol.32 (3), p.631-644.e6
Hauptverfasser: Gutierrez-Barragan, Daniel, Singh, Neha Atulkumar, Alvino, Filomena Grazia, Coletta, Ludovico, Rocchi, Federico, De Guzman, Elizabeth, Galbusera, Alberto, Uboldi, Mauro, Panzeri, Stefano, Gozzi, Alessandro
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container_end_page 644.e6
container_issue 3
container_start_page 631
container_title Current biology
container_volume 32
creator Gutierrez-Barragan, Daniel
Singh, Neha Atulkumar
Alvino, Filomena Grazia
Coletta, Ludovico
Rocchi, Federico
De Guzman, Elizabeth
Galbusera, Alberto
Uboldi, Mauro
Panzeri, Stefano
Gozzi, Alessandro
description Human imaging studies have shown that spontaneous brain activity exhibits stereotypic spatiotemporal reorganization in awake, conscious conditions with respect to minimally conscious states. However, whether and how this phenomenon can be generalized to lower mammalian species remains unclear. Leveraging a robust protocol for resting-state fMRI (rsfMRI) mapping in non-anesthetized, head-fixed mice, we investigated functional network topography and dynamic structure of spontaneous brain activity in wakeful animals. We found that rsfMRI networks in the awake state, while anatomically comparable to those observed under anesthesia, are topologically configured to maximize interregional communication, departing from the underlying community structure of the mouse axonal connectome. We further report that rsfMRI activity in wakeful animals exhibits unique spatiotemporal dynamics characterized by a state-dependent, dominant occurrence of coactivation patterns encompassing a prominent participation of arousal-related forebrain nuclei and functional anti-coordination between visual-auditory and polymodal cortical areas. We finally show that rsfMRI dynamics in awake mice exhibits a stereotypical temporal structure, in which state-dominant coactivation patterns are configured as network attractors. These findings suggest that spontaneous brain activity in awake mice is critically shaped by state-specific involvement of basal forebrain arousal systems and document that its dynamic structure recapitulates distinctive, evolutionarily relevant principles that are predictive of conscious states in higher mammalian species. [Display omitted] •fMRI networks in awake mice depart from underlying anatomical structure•fMRI dynamics in wakeful mice is critically shaped by arousal-related nuclei•Occurrence and topography of rsfMRI coactivation patterns define conscious states•fMRI coactivation dynamics defines a signature of consciousness in the mouse brain Gutierrez-Barragan et al. show that spontaneous fMRI activity in the awake mouse brain exhibits unique spatiotemporal dynamics, recapitulating phylogenetically relevant signatures of consciousness in primates and humans.
doi_str_mv 10.1016/j.cub.2021.12.015
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Singh, Neha Atulkumar ; Alvino, Filomena Grazia ; Coletta, Ludovico ; Rocchi, Federico ; De Guzman, Elizabeth ; Galbusera, Alberto ; Uboldi, Mauro ; Panzeri, Stefano ; Gozzi, Alessandro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c499t-db45c63c9169f38987c33d4068363c4095b8ff30da4d508fb5584313c8c76a013</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>anesthesia</topic><topic>Animals</topic><topic>brain</topic><topic>Brain - diagnostic imaging</topic><topic>Brain - physiology</topic><topic>Brain Mapping - methods</topic><topic>CAPs</topic><topic>connectivity</topic><topic>connectome</topic><topic>Connectome - methods</topic><topic>consciousness</topic><topic>DMN</topic><topic>head-fixed</topic><topic>isoflurane</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Mammals</topic><topic>medetomidine</topic><topic>Mice</topic><topic>Nerve Net - physiology</topic><topic>Wakefulness</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gutierrez-Barragan, Daniel</creatorcontrib><creatorcontrib>Singh, Neha Atulkumar</creatorcontrib><creatorcontrib>Alvino, Filomena Grazia</creatorcontrib><creatorcontrib>Coletta, Ludovico</creatorcontrib><creatorcontrib>Rocchi, Federico</creatorcontrib><creatorcontrib>De Guzman, Elizabeth</creatorcontrib><creatorcontrib>Galbusera, Alberto</creatorcontrib><creatorcontrib>Uboldi, Mauro</creatorcontrib><creatorcontrib>Panzeri, Stefano</creatorcontrib><creatorcontrib>Gozzi, Alessandro</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gutierrez-Barragan, Daniel</au><au>Singh, Neha Atulkumar</au><au>Alvino, Filomena Grazia</au><au>Coletta, Ludovico</au><au>Rocchi, Federico</au><au>De Guzman, Elizabeth</au><au>Galbusera, Alberto</au><au>Uboldi, Mauro</au><au>Panzeri, Stefano</au><au>Gozzi, Alessandro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Unique spatiotemporal fMRI dynamics in the awake mouse brain</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2022-02-07</date><risdate>2022</risdate><volume>32</volume><issue>3</issue><spage>631</spage><epage>644.e6</epage><pages>631-644.e6</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>Human imaging studies have shown that spontaneous brain activity exhibits stereotypic spatiotemporal reorganization in awake, conscious conditions with respect to minimally conscious states. 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We finally show that rsfMRI dynamics in awake mice exhibits a stereotypical temporal structure, in which state-dominant coactivation patterns are configured as network attractors. These findings suggest that spontaneous brain activity in awake mice is critically shaped by state-specific involvement of basal forebrain arousal systems and document that its dynamic structure recapitulates distinctive, evolutionarily relevant principles that are predictive of conscious states in higher mammalian species. 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subjects anesthesia
Animals
brain
Brain - diagnostic imaging
Brain - physiology
Brain Mapping - methods
CAPs
connectivity
connectome
Connectome - methods
consciousness
DMN
head-fixed
isoflurane
Magnetic Resonance Imaging - methods
Mammals
medetomidine
Mice
Nerve Net - physiology
Wakefulness
title Unique spatiotemporal fMRI dynamics in the awake mouse brain
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