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Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions.

Gawryluk JR, Mazerolle EL, D'Arcy RC - Front Neurosci (2014)

Bottom Line: There are two main reasons white matter fMRI remains controversial: (1) the blood oxygen level dependent (BOLD) fMRI signal depends on cerebral blood flow and volume, which are lower in white matter than gray matter and (2) fMRI signal has been associated with post-synaptic potentials (mainly localized in gray matter) as opposed to action potentials (the primary type of neural activity in white matter).White matter fMRI activation has the potential to greatly expand the breadth of brain connectivity research, as well as improve the assessment and diagnosis of white matter and connectivity disorders.We end with a discussion of future basic and clinical research directions in the study of white matter fMRI.

View Article: PubMed Central - PubMed

Affiliation: Division of Medical Sciences, Department of Psychology, University of Victoria Victoria, BC, Canada.

ABSTRACT
Functional magnetic resonance imaging (fMRI) is a non-invasive technique that allows for visualization of activated brain regions. Until recently, fMRI studies have focused on gray matter. There are two main reasons white matter fMRI remains controversial: (1) the blood oxygen level dependent (BOLD) fMRI signal depends on cerebral blood flow and volume, which are lower in white matter than gray matter and (2) fMRI signal has been associated with post-synaptic potentials (mainly localized in gray matter) as opposed to action potentials (the primary type of neural activity in white matter). Despite these observations, there is no direct evidence against measuring fMRI activation in white matter and reports of fMRI activation in white matter continue to increase. The questions underlying white matter fMRI activation are important. White matter fMRI activation has the potential to greatly expand the breadth of brain connectivity research, as well as improve the assessment and diagnosis of white matter and connectivity disorders. The current review provides an overview of the motivation to investigate white matter fMRI activation, as well as the published evidence of this phenomenon. We speculate on possible neurophysiologic bases of white matter fMRI signals, and discuss potential explanations for why reports of white matter fMRI activation are relatively scarce. We end with a discussion of future basic and clinical research directions in the study of white matter fMRI.

No MeSH data available.


Examples of white matter fMRI activation from studies published in 2006-2011. (A) An exploratory study of white matter activation by D'Arcy et al. in 2006 used a Sperry interhemispheric transfer task and detected activation near the splenium of the corpus callosum. This initial study led to (B) a prospective study of fMRI activation in white matter, which used a similar task and also revealed activation in the posterior corpus callosum. A follow up study, (C) aimed to improve sensitivity to the detection of white matter fMRI activation, used a Poffenberger interhemispheric transfer task and detected a cluster of activation in the anterior corpus callosum. Taken together, this series of studies led to (D), an investigation of whether different tasks could be used to functionally map different regions of the corpus callosum in the same group of individuals. The results were consistent with previous work and showed activation in the anterior corpus callosum during the Poffenberger task and posterior corpus callosum activation during the Sperry task.
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Figure 2: Examples of white matter fMRI activation from studies published in 2006-2011. (A) An exploratory study of white matter activation by D'Arcy et al. in 2006 used a Sperry interhemispheric transfer task and detected activation near the splenium of the corpus callosum. This initial study led to (B) a prospective study of fMRI activation in white matter, which used a similar task and also revealed activation in the posterior corpus callosum. A follow up study, (C) aimed to improve sensitivity to the detection of white matter fMRI activation, used a Poffenberger interhemispheric transfer task and detected a cluster of activation in the anterior corpus callosum. Taken together, this series of studies led to (D), an investigation of whether different tasks could be used to functionally map different regions of the corpus callosum in the same group of individuals. The results were consistent with previous work and showed activation in the anterior corpus callosum during the Poffenberger task and posterior corpus callosum activation during the Sperry task.

Mentions: Other interhemispheric transfer tasks have been used to target posterior regions of the corpus callosum. One such task is referred to as the Sperry paradigm, in recognition of the seminal work by Sperry and colleagues in which the function of the corpus callosum was probed by studying on split-brain patients (e.g., Gazzaniga et al., 1965; Myers and Sperry, 1985). In the Sperry task, word stimuli (for which the left hemisphere is relatively specialized) and face stimuli (for which the right hemisphere is relatively specialized) are presented briefly to the right or left visual hemifield. Crossed conditions involve presenting stimuli to the contralateral hemisphere (e.g., presenting word stimuli to the right hemisphere via the left visual field). D'Arcy et al. (2006) employed a Sperry task and an exploratory data analysis approach. Activation in the splenium of the corpus callosum activation could be observed, providing the first fMRI evidence of posterior callosal activation associated with an interhemispheric transfer task. Mazerolle et al. (2008) expanded and refined the approach taken by D'Arcy et al. (2006) by employing whole brain coverage, acquiring data at high field (4 T), and using a general linear model-based analysis technique. Splenium activation was observed in approximately 21% of individuals, as well as at the group level when liberal thresholds were applied (p < 0.005 uncorrected; Figure 2). Gawryluk et al. (2011a) went on to functionally map the corpus callosum within subjects, showing distinct areas of callosal activation for the Poffenberger and Sperry interhemispheric transfer tasks (Figure 2).


Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions.

Gawryluk JR, Mazerolle EL, D'Arcy RC - Front Neurosci (2014)

Examples of white matter fMRI activation from studies published in 2006-2011. (A) An exploratory study of white matter activation by D'Arcy et al. in 2006 used a Sperry interhemispheric transfer task and detected activation near the splenium of the corpus callosum. This initial study led to (B) a prospective study of fMRI activation in white matter, which used a similar task and also revealed activation in the posterior corpus callosum. A follow up study, (C) aimed to improve sensitivity to the detection of white matter fMRI activation, used a Poffenberger interhemispheric transfer task and detected a cluster of activation in the anterior corpus callosum. Taken together, this series of studies led to (D), an investigation of whether different tasks could be used to functionally map different regions of the corpus callosum in the same group of individuals. The results were consistent with previous work and showed activation in the anterior corpus callosum during the Poffenberger task and posterior corpus callosum activation during the Sperry task.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4125856&req=5

Figure 2: Examples of white matter fMRI activation from studies published in 2006-2011. (A) An exploratory study of white matter activation by D'Arcy et al. in 2006 used a Sperry interhemispheric transfer task and detected activation near the splenium of the corpus callosum. This initial study led to (B) a prospective study of fMRI activation in white matter, which used a similar task and also revealed activation in the posterior corpus callosum. A follow up study, (C) aimed to improve sensitivity to the detection of white matter fMRI activation, used a Poffenberger interhemispheric transfer task and detected a cluster of activation in the anterior corpus callosum. Taken together, this series of studies led to (D), an investigation of whether different tasks could be used to functionally map different regions of the corpus callosum in the same group of individuals. The results were consistent with previous work and showed activation in the anterior corpus callosum during the Poffenberger task and posterior corpus callosum activation during the Sperry task.
Mentions: Other interhemispheric transfer tasks have been used to target posterior regions of the corpus callosum. One such task is referred to as the Sperry paradigm, in recognition of the seminal work by Sperry and colleagues in which the function of the corpus callosum was probed by studying on split-brain patients (e.g., Gazzaniga et al., 1965; Myers and Sperry, 1985). In the Sperry task, word stimuli (for which the left hemisphere is relatively specialized) and face stimuli (for which the right hemisphere is relatively specialized) are presented briefly to the right or left visual hemifield. Crossed conditions involve presenting stimuli to the contralateral hemisphere (e.g., presenting word stimuli to the right hemisphere via the left visual field). D'Arcy et al. (2006) employed a Sperry task and an exploratory data analysis approach. Activation in the splenium of the corpus callosum activation could be observed, providing the first fMRI evidence of posterior callosal activation associated with an interhemispheric transfer task. Mazerolle et al. (2008) expanded and refined the approach taken by D'Arcy et al. (2006) by employing whole brain coverage, acquiring data at high field (4 T), and using a general linear model-based analysis technique. Splenium activation was observed in approximately 21% of individuals, as well as at the group level when liberal thresholds were applied (p < 0.005 uncorrected; Figure 2). Gawryluk et al. (2011a) went on to functionally map the corpus callosum within subjects, showing distinct areas of callosal activation for the Poffenberger and Sperry interhemispheric transfer tasks (Figure 2).

Bottom Line: There are two main reasons white matter fMRI remains controversial: (1) the blood oxygen level dependent (BOLD) fMRI signal depends on cerebral blood flow and volume, which are lower in white matter than gray matter and (2) fMRI signal has been associated with post-synaptic potentials (mainly localized in gray matter) as opposed to action potentials (the primary type of neural activity in white matter).White matter fMRI activation has the potential to greatly expand the breadth of brain connectivity research, as well as improve the assessment and diagnosis of white matter and connectivity disorders.We end with a discussion of future basic and clinical research directions in the study of white matter fMRI.

View Article: PubMed Central - PubMed

Affiliation: Division of Medical Sciences, Department of Psychology, University of Victoria Victoria, BC, Canada.

ABSTRACT
Functional magnetic resonance imaging (fMRI) is a non-invasive technique that allows for visualization of activated brain regions. Until recently, fMRI studies have focused on gray matter. There are two main reasons white matter fMRI remains controversial: (1) the blood oxygen level dependent (BOLD) fMRI signal depends on cerebral blood flow and volume, which are lower in white matter than gray matter and (2) fMRI signal has been associated with post-synaptic potentials (mainly localized in gray matter) as opposed to action potentials (the primary type of neural activity in white matter). Despite these observations, there is no direct evidence against measuring fMRI activation in white matter and reports of fMRI activation in white matter continue to increase. The questions underlying white matter fMRI activation are important. White matter fMRI activation has the potential to greatly expand the breadth of brain connectivity research, as well as improve the assessment and diagnosis of white matter and connectivity disorders. The current review provides an overview of the motivation to investigate white matter fMRI activation, as well as the published evidence of this phenomenon. We speculate on possible neurophysiologic bases of white matter fMRI signals, and discuss potential explanations for why reports of white matter fMRI activation are relatively scarce. We end with a discussion of future basic and clinical research directions in the study of white matter fMRI.

No MeSH data available.