High-resolution awake mouse fMRI at 14 tesla

High-resolution awake mouse functional magnetic resonance imaging (fMRI) remains challenging despite extensive efforts to address motion-induced artifacts and stress. This study introduces an implantable radio frequency (RF) surface coil design that minimizes image distortion caused by the air/tissu...

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Main Authors: David Hike, Xiaochen Liu, Zeping Xie, Bei Zhang, Sangcheon Choi, Xiaoqing Alice Zhou, Andy Liu, Alyssa Murstein, Yuanyuan Jiang, Anna Devor, Xin Yu
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-01-01
Series:eLife
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Online Access:https://elifesciences.org/articles/95528
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author David Hike
Xiaochen Liu
Zeping Xie
Bei Zhang
Sangcheon Choi
Xiaoqing Alice Zhou
Andy Liu
Alyssa Murstein
Yuanyuan Jiang
Anna Devor
Xin Yu
author_facet David Hike
Xiaochen Liu
Zeping Xie
Bei Zhang
Sangcheon Choi
Xiaoqing Alice Zhou
Andy Liu
Alyssa Murstein
Yuanyuan Jiang
Anna Devor
Xin Yu
author_sort David Hike
collection DOAJ
description High-resolution awake mouse functional magnetic resonance imaging (fMRI) remains challenging despite extensive efforts to address motion-induced artifacts and stress. This study introduces an implantable radio frequency (RF) surface coil design that minimizes image distortion caused by the air/tissue interface of mouse brains while simultaneously serving as a headpost for fixation during scanning. Furthermore, this study provides a thorough acclimation method used to accustom animals to the MRI environment minimizing motion-induced artifacts. Using a 14 T scanner, high-resolution fMRI enabled brain-wide functional mapping of visual and vibrissa stimulation at 100 µm×100 µm×200 µm resolution with a 2 s per frame sampling rate. Besides activated ascending visual and vibrissa pathways, robust blood oxygen level-dependent (BOLD) responses were detected in the anterior cingulate cortex upon visual stimulation and spread through the ventral retrosplenial area (VRA) with vibrissa air-puff stimulation, demonstrating higher-order sensory processing in association cortices of awake mice. In particular, the rapid hemodynamic responses in VRA upon vibrissa stimulation showed a strong correlation with the hippocampus, thalamus, and prefrontal cortical areas. Cross-correlation analysis with designated VRA responses revealed early positive BOLD signals at the contralateral barrel cortex (BC) occurring 2 s prior to the air-puff in awake mice with repetitive stimulation, which was not detected using a randomized stimulation paradigm. This early BC activation indicated a learned anticipation through the vibrissa system and association cortices in awake mice under continuous exposure of repetitive air-puff stimulation. This work establishes a high-resolution awake mouse fMRI platform, enabling brain-wide functional mapping of sensory signal processing in higher association cortical areas.
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spelling doaj-art-283f5ed857684669bdbc5a7d393ba4ef2025-01-09T15:15:04ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011310.7554/eLife.95528High-resolution awake mouse fMRI at 14 teslaDavid Hike0https://orcid.org/0000-0001-5294-1767Xiaochen Liu1https://orcid.org/0000-0001-6342-7704Zeping Xie2Bei Zhang3Sangcheon Choi4https://orcid.org/0000-0001-7327-1344Xiaoqing Alice Zhou5Andy Liu6https://orcid.org/0009-0004-0080-8429Alyssa Murstein7Yuanyuan Jiang8https://orcid.org/0000-0001-7758-7450Anna Devor9https://orcid.org/0000-0002-5143-3960Xin Yu10https://orcid.org/0000-0001-9890-5489Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United States; Graduate Program in Neuroscience, Boston University, Boston, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United States; Graduate Program in Neuroscience, Boston University, Boston, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United States; Department of Biomedical Engineering, Boston University, Boston, United StatesAthinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, United StatesHigh-resolution awake mouse functional magnetic resonance imaging (fMRI) remains challenging despite extensive efforts to address motion-induced artifacts and stress. This study introduces an implantable radio frequency (RF) surface coil design that minimizes image distortion caused by the air/tissue interface of mouse brains while simultaneously serving as a headpost for fixation during scanning. Furthermore, this study provides a thorough acclimation method used to accustom animals to the MRI environment minimizing motion-induced artifacts. Using a 14 T scanner, high-resolution fMRI enabled brain-wide functional mapping of visual and vibrissa stimulation at 100 µm×100 µm×200 µm resolution with a 2 s per frame sampling rate. Besides activated ascending visual and vibrissa pathways, robust blood oxygen level-dependent (BOLD) responses were detected in the anterior cingulate cortex upon visual stimulation and spread through the ventral retrosplenial area (VRA) with vibrissa air-puff stimulation, demonstrating higher-order sensory processing in association cortices of awake mice. In particular, the rapid hemodynamic responses in VRA upon vibrissa stimulation showed a strong correlation with the hippocampus, thalamus, and prefrontal cortical areas. Cross-correlation analysis with designated VRA responses revealed early positive BOLD signals at the contralateral barrel cortex (BC) occurring 2 s prior to the air-puff in awake mice with repetitive stimulation, which was not detected using a randomized stimulation paradigm. This early BC activation indicated a learned anticipation through the vibrissa system and association cortices in awake mice under continuous exposure of repetitive air-puff stimulation. This work establishes a high-resolution awake mouse fMRI platform, enabling brain-wide functional mapping of sensory signal processing in higher association cortical areas.https://elifesciences.org/articles/95528fMRIBOLDpredictionvisual stimulationvibrissa stimulationawake mouse
spellingShingle David Hike
Xiaochen Liu
Zeping Xie
Bei Zhang
Sangcheon Choi
Xiaoqing Alice Zhou
Andy Liu
Alyssa Murstein
Yuanyuan Jiang
Anna Devor
Xin Yu
High-resolution awake mouse fMRI at 14 tesla
eLife
fMRI
BOLD
prediction
visual stimulation
vibrissa stimulation
awake mouse
title High-resolution awake mouse fMRI at 14 tesla
title_full High-resolution awake mouse fMRI at 14 tesla
title_fullStr High-resolution awake mouse fMRI at 14 tesla
title_full_unstemmed High-resolution awake mouse fMRI at 14 tesla
title_short High-resolution awake mouse fMRI at 14 tesla
title_sort high resolution awake mouse fmri at 14 tesla
topic fMRI
BOLD
prediction
visual stimulation
vibrissa stimulation
awake mouse
url https://elifesciences.org/articles/95528
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AT sangcheonchoi highresolutionawakemousefmriat14tesla
AT xiaoqingalicezhou highresolutionawakemousefmriat14tesla
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