Unique spatiotemporal fMRI dynamics in the awake mouse brain

TY - JOUR

T1 - Unique spatiotemporal fMRI dynamics in the awake mouse brain

AU - Gutierrez-Barragan, Daniel

AU - Singh, Neha Atulkumar

AU - Alvino, Filomena Grazia

AU - Coletta, Ludovico

AU - Rocchi, Federico

AU - De Guzman, Elizabeth

AU - Galbusera, Alberto

AU - Uboldi, Mauro

AU - Panzeri, Stefano

AU - Gozzi, Alessandro

N1 - Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

PY - 2022/2/7

Y1 - 2022/2/7

N2 - 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.

AB - 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.

U2 - 10.1016/j.cub.2021.12.015

DO - 10.1016/j.cub.2021.12.015

M3 - SCORING: Journal article

C2 - 34998465

VL - 32

SP - 631-644.e6

JO - CURR BIOL

JF - CURR BIOL

SN - 0960-9822

IS - 3

ER -