Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue Heating

Functional blood-oxygenation-level-dependent (BOLD) MRI provides a brain-wide readout that depends on the hemodynamic response to neuronal activity. Diffusion fMRI has been proposed as an alternative to BOLD fMRI and has been postulated to directly rely on neuronal activity. These complementary func...

Full description

Bibliographic Details
Main Authors: Franziska Albers, Lydia Wachsmuth, Daniel Schache, Henriette Lambers, Cornelius Faber
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-10-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.01104/full
_version_ 1819260561173512192
author Franziska Albers
Lydia Wachsmuth
Daniel Schache
Henriette Lambers
Cornelius Faber
author_facet Franziska Albers
Lydia Wachsmuth
Daniel Schache
Henriette Lambers
Cornelius Faber
author_sort Franziska Albers
collection DOAJ
description Functional blood-oxygenation-level-dependent (BOLD) MRI provides a brain-wide readout that depends on the hemodynamic response to neuronal activity. Diffusion fMRI has been proposed as an alternative to BOLD fMRI and has been postulated to directly rely on neuronal activity. These complementary functional readouts are versatile tools to be combined with optogenetic stimulation to investigate networks of the brain. The cell-specificity and temporal precision of optogenetic manipulations promise to enable further investigation of the origin of fMRI signals. The signal characteristics of the diffusion fMRI readout vice versa may better resolve network effects of optogenetic stimulation. However, the light application needed for optogenetic stimulation is accompanied by heat deposition within the tissue. As both diffusion and BOLD are sensitive to temperature changes, light application can lead to apparent activations confounding the interpretation of fMRI data. The degree of tissue heating, the appearance of apparent activation in different fMRI sequences and the origin of these phenomena are not well understood. Here, we disentangled apparent activations in BOLD and diffusion measurements in rats from physiological activation upon sensory or optogenetic stimulation. Both, BOLD and diffusion fMRI revealed similar signal shapes upon sensory stimulation that differed clearly from those upon heating. Apparent activations induced by high-intensity light application were dominated by T2∗-effects and resulted in mainly negative signal changes. We estimated that even low-intensity light application used for optogenetic stimulation reduces the BOLD response close to the fiber by up to 0.4%. The diffusion fMRI signal contained T2, T2∗ and diffusion components. The apparent diffusion coefficient, which reflects the isolated diffusion component, showed negative changes upon both optogenetic and electric forepaw stimulation. In contrast, positive changes were detected upon high-intensity light application and thus ruled out heating as a major contributor to the diffusion fMRI signal.
first_indexed 2024-12-23T19:27:52Z
format Article
id doaj.art-2e53beb7fccb49569ba7141bf12ddc76
institution Directory Open Access Journal
issn 1662-453X
language English
last_indexed 2024-12-23T19:27:52Z
publishDate 2019-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neuroscience
spelling doaj.art-2e53beb7fccb49569ba7141bf12ddc762022-12-21T17:34:00ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-10-011310.3389/fnins.2019.01104485568Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue HeatingFranziska AlbersLydia WachsmuthDaniel SchacheHenriette LambersCornelius FaberFunctional blood-oxygenation-level-dependent (BOLD) MRI provides a brain-wide readout that depends on the hemodynamic response to neuronal activity. Diffusion fMRI has been proposed as an alternative to BOLD fMRI and has been postulated to directly rely on neuronal activity. These complementary functional readouts are versatile tools to be combined with optogenetic stimulation to investigate networks of the brain. The cell-specificity and temporal precision of optogenetic manipulations promise to enable further investigation of the origin of fMRI signals. The signal characteristics of the diffusion fMRI readout vice versa may better resolve network effects of optogenetic stimulation. However, the light application needed for optogenetic stimulation is accompanied by heat deposition within the tissue. As both diffusion and BOLD are sensitive to temperature changes, light application can lead to apparent activations confounding the interpretation of fMRI data. The degree of tissue heating, the appearance of apparent activation in different fMRI sequences and the origin of these phenomena are not well understood. Here, we disentangled apparent activations in BOLD and diffusion measurements in rats from physiological activation upon sensory or optogenetic stimulation. Both, BOLD and diffusion fMRI revealed similar signal shapes upon sensory stimulation that differed clearly from those upon heating. Apparent activations induced by high-intensity light application were dominated by T2∗-effects and resulted in mainly negative signal changes. We estimated that even low-intensity light application used for optogenetic stimulation reduces the BOLD response close to the fiber by up to 0.4%. The diffusion fMRI signal contained T2, T2∗ and diffusion components. The apparent diffusion coefficient, which reflects the isolated diffusion component, showed negative changes upon both optogenetic and electric forepaw stimulation. In contrast, positive changes were detected upon high-intensity light application and thus ruled out heating as a major contributor to the diffusion fMRI signal.https://www.frontiersin.org/article/10.3389/fnins.2019.01104/fullfunctional diffusionoptogeneticsBOLDheating artifactssmall animal MRI
spellingShingle Franziska Albers
Lydia Wachsmuth
Daniel Schache
Henriette Lambers
Cornelius Faber
Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue Heating
Frontiers in Neuroscience
functional diffusion
optogenetics
BOLD
heating artifacts
small animal MRI
title Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue Heating
title_full Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue Heating
title_fullStr Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue Heating
title_full_unstemmed Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue Heating
title_short Functional MRI Readouts From BOLD and Diffusion Measurements Differentially Respond to Optogenetic Activation and Tissue Heating
title_sort functional mri readouts from bold and diffusion measurements differentially respond to optogenetic activation and tissue heating
topic functional diffusion
optogenetics
BOLD
heating artifacts
small animal MRI
url https://www.frontiersin.org/article/10.3389/fnins.2019.01104/full
work_keys_str_mv AT franziskaalbers functionalmrireadoutsfromboldanddiffusionmeasurementsdifferentiallyrespondtooptogeneticactivationandtissueheating
AT lydiawachsmuth functionalmrireadoutsfromboldanddiffusionmeasurementsdifferentiallyrespondtooptogeneticactivationandtissueheating
AT danielschache functionalmrireadoutsfromboldanddiffusionmeasurementsdifferentiallyrespondtooptogeneticactivationandtissueheating
AT henriettelambers functionalmrireadoutsfromboldanddiffusionmeasurementsdifferentiallyrespondtooptogeneticactivationandtissueheating
AT corneliusfaber functionalmrireadoutsfromboldanddiffusionmeasurementsdifferentiallyrespondtooptogeneticactivationandtissueheating