Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasound

Functional ultrasound (fUS) imaging is a method for visualizing deep brain activity based on cerebral blood volume changes coupled with neural activity, while functional MRI (fMRI) relies on the blood-oxygenation-level-dependent signal coupled with neural activity. Low-frequency fluctuations (LFF) o...

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Main Authors: Keigo Hikishima, Tomokazu Tsurugizawa, Kazumi Kasahara, Ryo Takagi, Kiyoshi Yoshinaka, Naotaka Nitta
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811923004482
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author Keigo Hikishima
Tomokazu Tsurugizawa
Kazumi Kasahara
Ryo Takagi
Kiyoshi Yoshinaka
Naotaka Nitta
author_facet Keigo Hikishima
Tomokazu Tsurugizawa
Kazumi Kasahara
Ryo Takagi
Kiyoshi Yoshinaka
Naotaka Nitta
author_sort Keigo Hikishima
collection DOAJ
description Functional ultrasound (fUS) imaging is a method for visualizing deep brain activity based on cerebral blood volume changes coupled with neural activity, while functional MRI (fMRI) relies on the blood-oxygenation-level-dependent signal coupled with neural activity. Low-frequency fluctuations (LFF) of fMRI signals during resting-state can be measured by resting-state fMRI (rsfMRI), which allows functional imaging of the whole brain, and the distributions of resting-state network (RSN) can then be estimated from these fluctuations using independent component analysis (ICA). This procedure provides an important method for studying cognitive and psychophysiological diseases affecting specific brain networks. The distributions of RSNs in the brain-wide area has been reported primarily by rsfMRI. RSNs using rsfMRI are generally computed from the time-course of fMRI signals for more than 5 min. However, a recent dynamic functional connectivity study revealed that RSNs are still not perfectly stable even after 10 min. Importantly, fUS has a higher temporal resolution and stronger correlation with neural activity compared with fMRI. Therefore, we hypothesized that fUS applied during the resting-state for a shorter than 5 min would provide similar RSNs compared to fMRI. High temporal resolution rsfUS data were acquired at 10 Hz in awake mice. The quality of the default mode network (DMN), a well-known RSN, was evaluated using signal-noise separation (SNS) applied to different measurement durations of rsfUS. The results showed that the SNS did not change when the measurement duration was increased to more than 210 s. Next, we measured short-duration rsfUS multi-slice measurements in the brain-wide area. The results showed that rsfUS with the short duration succeeded in detecting RSNs distributed in the brain-wide area consistent with RSNs detected by 11.7-T MRI under awake conditions (medial prefrontal cortex and cingulate cortex in the anterior DMN, retrosplenial cortex and visual cortex in the posterior DMN, somatosensory and motor cortexes in the lateral cortical network, thalamus, dorsal hippocampus, and medial cerebellum), confirming the reliability of the RSNs detected by rsfUS. However, bilateral RSNs located in the secondary somatosensory cortex, ventral hippocampus, auditory cortex, and lateral cerebellum extracted from rsfUS were different from the unilateral RSNs extracted from rsfMRI. These findings indicate the potential of rsfUS as a method for analyzing functional brain networks and should encourage future research to elucidate functional brain networks and their relationships with disease model mice.
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spelling doaj.art-b03467bb0f254218a8c6257f419f39452023-09-02T04:31:12ZengElsevierNeuroImage1095-95722023-10-01279120297Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasoundKeigo Hikishima0Tomokazu Tsurugizawa1Kazumi Kasahara2Ryo Takagi3Kiyoshi Yoshinaka4Naotaka Nitta5Health and Medical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, Japan; Okinawa Institute of Science and Technology Graduate University (OIST), Okinawa, Japan; Corresponding author at: Health and Medical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, Japan.Human Informatics and Interaction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, JapanHuman Informatics and Interaction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, JapanHealth and Medical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, JapanHealth and Medical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, JapanHealth and Medical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Ibaraki, JapanFunctional ultrasound (fUS) imaging is a method for visualizing deep brain activity based on cerebral blood volume changes coupled with neural activity, while functional MRI (fMRI) relies on the blood-oxygenation-level-dependent signal coupled with neural activity. Low-frequency fluctuations (LFF) of fMRI signals during resting-state can be measured by resting-state fMRI (rsfMRI), which allows functional imaging of the whole brain, and the distributions of resting-state network (RSN) can then be estimated from these fluctuations using independent component analysis (ICA). This procedure provides an important method for studying cognitive and psychophysiological diseases affecting specific brain networks. The distributions of RSNs in the brain-wide area has been reported primarily by rsfMRI. RSNs using rsfMRI are generally computed from the time-course of fMRI signals for more than 5 min. However, a recent dynamic functional connectivity study revealed that RSNs are still not perfectly stable even after 10 min. Importantly, fUS has a higher temporal resolution and stronger correlation with neural activity compared with fMRI. Therefore, we hypothesized that fUS applied during the resting-state for a shorter than 5 min would provide similar RSNs compared to fMRI. High temporal resolution rsfUS data were acquired at 10 Hz in awake mice. The quality of the default mode network (DMN), a well-known RSN, was evaluated using signal-noise separation (SNS) applied to different measurement durations of rsfUS. The results showed that the SNS did not change when the measurement duration was increased to more than 210 s. Next, we measured short-duration rsfUS multi-slice measurements in the brain-wide area. The results showed that rsfUS with the short duration succeeded in detecting RSNs distributed in the brain-wide area consistent with RSNs detected by 11.7-T MRI under awake conditions (medial prefrontal cortex and cingulate cortex in the anterior DMN, retrosplenial cortex and visual cortex in the posterior DMN, somatosensory and motor cortexes in the lateral cortical network, thalamus, dorsal hippocampus, and medial cerebellum), confirming the reliability of the RSNs detected by rsfUS. However, bilateral RSNs located in the secondary somatosensory cortex, ventral hippocampus, auditory cortex, and lateral cerebellum extracted from rsfUS were different from the unilateral RSNs extracted from rsfMRI. These findings indicate the potential of rsfUS as a method for analyzing functional brain networks and should encourage future research to elucidate functional brain networks and their relationships with disease model mice.http://www.sciencedirect.com/science/article/pii/S1053811923004482Resting-state network (RSN)Functional ultrasound (fUS)Resting-state functional MRI (rsfMRI)Independent component analysis (ICA)Default mode network (DMN)
spellingShingle Keigo Hikishima
Tomokazu Tsurugizawa
Kazumi Kasahara
Ryo Takagi
Kiyoshi Yoshinaka
Naotaka Nitta
Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasound
NeuroImage
Resting-state network (RSN)
Functional ultrasound (fUS)
Resting-state functional MRI (rsfMRI)
Independent component analysis (ICA)
Default mode network (DMN)
title Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasound
title_full Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasound
title_fullStr Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasound
title_full_unstemmed Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasound
title_short Brain-wide mapping of resting-state networks in mice using high-frame rate functional ultrasound
title_sort brain wide mapping of resting state networks in mice using high frame rate functional ultrasound
topic Resting-state network (RSN)
Functional ultrasound (fUS)
Resting-state functional MRI (rsfMRI)
Independent component analysis (ICA)
Default mode network (DMN)
url http://www.sciencedirect.com/science/article/pii/S1053811923004482
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