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 |
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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 |
format | Article |
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[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.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2021.12.015</identifier><identifier>PMID: 34998465</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>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</subject><ispartof>Current biology, 2022-02, Vol.32 (3), p.631-644.e6</ispartof><rights>2021 The Author(s)</rights><rights>Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><rights>2021 The Author(s) 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c499t-db45c63c9169f38987c33d4068363c4095b8ff30da4d508fb5584313c8c76a013</citedby><cites>FETCH-LOGICAL-c499t-db45c63c9169f38987c33d4068363c4095b8ff30da4d508fb5584313c8c76a013</cites><orcidid>0000-0002-5731-4137 ; 0000-0003-2609-4722 ; 0000-0002-7116-4710 ; 0000-0001-7465-7564</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0960982221016912$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34998465$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><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><title>Unique spatiotemporal fMRI dynamics in the awake mouse brain</title><title>Current biology</title><addtitle>Curr Biol</addtitle><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.</description><subject>anesthesia</subject><subject>Animals</subject><subject>brain</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - physiology</subject><subject>Brain Mapping - methods</subject><subject>CAPs</subject><subject>connectivity</subject><subject>connectome</subject><subject>Connectome - methods</subject><subject>consciousness</subject><subject>DMN</subject><subject>head-fixed</subject><subject>isoflurane</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Mammals</subject><subject>medetomidine</subject><subject>Mice</subject><subject>Nerve Net - physiology</subject><subject>Wakefulness</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1LAzEQhoMotlZ_gBfZo5dd870JiiDFj0JFEHsO2WzWpnZ3a7Kt9N-b0lr04mlg5p133nkAOEcwQxDxq1lmlkWGIUYZwhlE7AD0kchlCillh6APJYepFBj3wEkIMwgRFpIfgx6hUgrKWR_cTBr3ubRJWOjOtZ2tF63X86R6fh0l5brRtTMhcU3STW2iv_SHTep2GWxSeO2aU3BU6XmwZ7s6AJOH-7fhUzp-eRwN78apiXe6tCwoM5wYibisiJAiN4SUFHJBYpdCyQpRVQSWmpYMiqpgTFCCiBEm5xoiMgC3W9_FsqhtaWzTxZBq4V2t_Vq12qm_k8ZN1Xu7UkKQHOd5NLjcGfg2fhs6Vbtg7HyuGxvfUZgjwVBOCYtStJUa34bgbbU_g6DaUFczFamrDXWFsIrU487F73z7jR_MUXC9FdhIaeWsV8E42xhbOm9Np8rW_WP_DZpGklY</recordid><startdate>20220207</startdate><enddate>20220207</enddate><creator>Gutierrez-Barragan, Daniel</creator><creator>Singh, Neha Atulkumar</creator><creator>Alvino, Filomena Grazia</creator><creator>Coletta, Ludovico</creator><creator>Rocchi, Federico</creator><creator>De Guzman, Elizabeth</creator><creator>Galbusera, Alberto</creator><creator>Uboldi, Mauro</creator><creator>Panzeri, Stefano</creator><creator>Gozzi, Alessandro</creator><general>Elsevier Inc</general><general>Cell Press</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5731-4137</orcidid><orcidid>https://orcid.org/0000-0003-2609-4722</orcidid><orcidid>https://orcid.org/0000-0002-7116-4710</orcidid><orcidid>https://orcid.org/0000-0001-7465-7564</orcidid></search><sort><creationdate>20220207</creationdate><title>Unique spatiotemporal fMRI dynamics in the awake mouse brain</title><author>Gutierrez-Barragan, Daniel ; 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. 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.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>34998465</pmid><doi>10.1016/j.cub.2021.12.015</doi><orcidid>https://orcid.org/0000-0002-5731-4137</orcidid><orcidid>https://orcid.org/0000-0003-2609-4722</orcidid><orcidid>https://orcid.org/0000-0002-7116-4710</orcidid><orcidid>https://orcid.org/0000-0001-7465-7564</orcidid><oa>free_for_read</oa></addata></record> |
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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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