High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imaging

Whole-brain imaging approaches and optogenetic manipulations are powerful tools to map brain-wide neural circuits in vivo. To date, functional magnetic resonance imaging (fMRI) provides the most comprehensive evaluation of such large-scale circuitry. However, functional ultrasound imaging (fUSI) has...

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Main Authors: Bradley Jay Edelman, Giovanna D. Ielacqua, Russell W. Chan, Mazen Asaad, Mankin Choy, Jin Hyung Lee
Format: Article
Language:English
Published: Elsevier 2021-11-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811921007096
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author Bradley Jay Edelman
Giovanna D. Ielacqua
Russell W. Chan
Mazen Asaad
Mankin Choy
Jin Hyung Lee
author_facet Bradley Jay Edelman
Giovanna D. Ielacqua
Russell W. Chan
Mazen Asaad
Mankin Choy
Jin Hyung Lee
author_sort Bradley Jay Edelman
collection DOAJ
description Whole-brain imaging approaches and optogenetic manipulations are powerful tools to map brain-wide neural circuits in vivo. To date, functional magnetic resonance imaging (fMRI) provides the most comprehensive evaluation of such large-scale circuitry. However, functional ultrasound imaging (fUSI) has recently emerged as a complementary imaging modality that can extend such measurements towards the context of diverse behavioral states and tasks. Nevertheless, in order to properly interpret the fUSI signal during these complicated scenarios, it must first be carefully validated against well-established technologies, such as fMRI, in highly controlled experimental settings. Here, to address this need, we compared subsequent fMRI and fUSI recordings in response to direct neuronal activation via optogenetics in the same animals under an identical anesthetic protocol. Specifically, we applied various intensities of light stimulation to the primary motor cortex (M1) of mice and compared the spatiotemporal dynamics of the elicited fMRI and fUSI signals. Overall, our general linear model analysis (t-scores) and time series analysis (z-scores) revealed that fUSI was more sensitive than fMRI for detecting optogenetically-induced neuronal activation. Local field potential recordings in the bilateral M1 and striatum also better co-localized with fUSI activation patterns than those of fMRI. Finally, the fUSI response contained distinct arterial and venous components that provide vascular readouts of neuronal activity with vessel-type specificity.
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spelling doaj.art-c2eafdacdf954b7497ba533daf155b052022-12-21T21:59:44ZengElsevierNeuroImage1095-95722021-11-01242118434High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imagingBradley Jay Edelman0Giovanna D. Ielacqua1Russell W. Chan2Mazen Asaad3Mankin Choy4Jin Hyung Lee5Department of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USADepartment of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USADepartment of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USADepartment of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USA; Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA, 94305, USADepartment of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USADepartment of Neurology and Neurological Sciences, Stanford University, Stanford, CA 94305, USA; Department of Bioengineering, Stanford University, Stanford, CA, 94305, USA; Department of Electrical Engineering, Stanford University, CA, 94305, USA; Department of Neurosurgery, Stanford University, Stanford, CA, 94305, USA; Corresponding author at: 318 Campus Drive, Clark Center, W300A, Stanford, CA 94305, USA.Whole-brain imaging approaches and optogenetic manipulations are powerful tools to map brain-wide neural circuits in vivo. To date, functional magnetic resonance imaging (fMRI) provides the most comprehensive evaluation of such large-scale circuitry. However, functional ultrasound imaging (fUSI) has recently emerged as a complementary imaging modality that can extend such measurements towards the context of diverse behavioral states and tasks. Nevertheless, in order to properly interpret the fUSI signal during these complicated scenarios, it must first be carefully validated against well-established technologies, such as fMRI, in highly controlled experimental settings. Here, to address this need, we compared subsequent fMRI and fUSI recordings in response to direct neuronal activation via optogenetics in the same animals under an identical anesthetic protocol. Specifically, we applied various intensities of light stimulation to the primary motor cortex (M1) of mice and compared the spatiotemporal dynamics of the elicited fMRI and fUSI signals. Overall, our general linear model analysis (t-scores) and time series analysis (z-scores) revealed that fUSI was more sensitive than fMRI for detecting optogenetically-induced neuronal activation. Local field potential recordings in the bilateral M1 and striatum also better co-localized with fUSI activation patterns than those of fMRI. Finally, the fUSI response contained distinct arterial and venous components that provide vascular readouts of neuronal activity with vessel-type specificity.http://www.sciencedirect.com/science/article/pii/S1053811921007096functional ultrasound imagingFunctional magnetic resonance imagingOptogeneticsNeural circuitsMotor cortex
spellingShingle Bradley Jay Edelman
Giovanna D. Ielacqua
Russell W. Chan
Mazen Asaad
Mankin Choy
Jin Hyung Lee
High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imaging
NeuroImage
functional ultrasound imaging
Functional magnetic resonance imaging
Optogenetics
Neural circuits
Motor cortex
title High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imaging
title_full High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imaging
title_fullStr High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imaging
title_full_unstemmed High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imaging
title_short High-sensitivity detection of optogenetically-induced neural activity with functional ultrasound imaging
title_sort high sensitivity detection of optogenetically induced neural activity with functional ultrasound imaging
topic functional ultrasound imaging
Functional magnetic resonance imaging
Optogenetics
Neural circuits
Motor cortex
url http://www.sciencedirect.com/science/article/pii/S1053811921007096
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