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Multimodal imaging of mild traumatic brain injury and persistent postconcussion syndrome.

Dean PJ, Sato JR, Vieira G, McNamara A, Sterr A - Brain Behav (2014)

Bottom Line: It was hypothesized that only those mTBI participants with persistent PCS would show functional changes, and that these changes would be related to reduced structural integrity and altered metabolite concentrations.There were no behavioral differences between the groups, but participants with greater PCS symptoms exhibited greater activation in attention-related areas (anterior cingulate), along with reduced activation in temporal, default mode network, and working memory areas (left prefrontal) as cognitive load was increased from the easiest to the most difficult task.Functional changes in these areas correlated with reduced structural integrity in corpus callosum and anterior white matter, and reduced creatine concentration in right dorsolateral prefrontal cortex.

View Article: PubMed Central - PubMed

Affiliation: School of Psychology, University Of Surrey Guildford, UK.

ABSTRACT

Background: Persistent postconcussion syndrome (PCS) occurs in around 5-10% of individuals after mild traumatic brain injury (mTBI), but research into the underlying biology of these ongoing symptoms is limited and inconsistent. One reason for this could be the heterogeneity inherent to mTBI, with individualized injury mechanisms and psychological factors. A multimodal imaging study may be able to characterize the injury better.

Aim: To look at the relationship between functional (fMRI), structural (diffusion tensor imaging), and metabolic (magnetic resonance spectroscopy) data in the same participants in the long term (>1 year) after injury. It was hypothesized that only those mTBI participants with persistent PCS would show functional changes, and that these changes would be related to reduced structural integrity and altered metabolite concentrations.

Methods: Functional changes associated with persistent PCS after mTBI (>1 year postinjury) were investigated in participants with and without PCS (both n = 8) and non-head injured participants (n = 9) during performance of working memory and attention/processing speed tasks. Correlation analyses were performed to look at the relationship between the functional data and structural and metabolic alterations in the same participants.

Results: There were no behavioral differences between the groups, but participants with greater PCS symptoms exhibited greater activation in attention-related areas (anterior cingulate), along with reduced activation in temporal, default mode network, and working memory areas (left prefrontal) as cognitive load was increased from the easiest to the most difficult task. Functional changes in these areas correlated with reduced structural integrity in corpus callosum and anterior white matter, and reduced creatine concentration in right dorsolateral prefrontal cortex.

Conclusion: These data suggest that the top-down attentional regulation and deactivation of task-irrelevant areas may be compensating for the reduction in working memory capacity and variation in white matter transmission caused by the structural and metabolic changes after injury. This may in turn be contributing to secondary PCS symptoms such as fatigue and headache. Further research is required using multimodal data to investigate the mechanisms of injury after mTBI, but also to aid individualized diagnosis and prognosis.

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Paced Visual Serial Addition Task fMRI contrast maps. Column 1: Main effect of 2.5s PVSAT block compared to Rest block for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 2: Parametric (linearly modeled) increase in BOLD response from least taxing (2.5s PVSAT) to most taxing (1s PVSAT) for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 3: Group comparison for the 1 > 2.5s PVSAT contrast showing significant BOLD response differences between mTBI + PCS and Control, MTBI-PCS and Control, as well as between mTBI + PCS and mTBI-PCS. In addition, areas where 1 > 2.5s PVSAT contrast significantly correlates with Postconcussion syndrome symptoms as indexed by the Rivermead Postconcussion Symptoms Questionnaire. Red/Yellow Z scale represents areas with significantly increased BOLD response (Z > 1.9); Blue/Green Z scale represents areas with significantly reduced BOLD response (Z > 1.9). Axial, coronal, and sagittal plane coordinates indicated under each image. Neurological Orientation (R=R).
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fig05: Paced Visual Serial Addition Task fMRI contrast maps. Column 1: Main effect of 2.5s PVSAT block compared to Rest block for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 2: Parametric (linearly modeled) increase in BOLD response from least taxing (2.5s PVSAT) to most taxing (1s PVSAT) for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 3: Group comparison for the 1 > 2.5s PVSAT contrast showing significant BOLD response differences between mTBI + PCS and Control, MTBI-PCS and Control, as well as between mTBI + PCS and mTBI-PCS. In addition, areas where 1 > 2.5s PVSAT contrast significantly correlates with Postconcussion syndrome symptoms as indexed by the Rivermead Postconcussion Symptoms Questionnaire. Red/Yellow Z scale represents areas with significantly increased BOLD response (Z > 1.9); Blue/Green Z scale represents areas with significantly reduced BOLD response (Z > 1.9). Axial, coronal, and sagittal plane coordinates indicated under each image. Neurological Orientation (R=R).

Mentions: Typical BOLD response patterns were observed for all groups for both 0-Back compared to rest (Fig.4, column 1) and 2.5s PVSAT condition compared to rest (Fig.5, column 1). There was increased BOLD response across groups in motor planning and attention-related areas (e.g., premotor cortex, posterior parietal cortex, supplementary motor area [SMA]), as well as other task-relevant areas (contralateral motor cortex, bilateral cerebellum, bilateral visual cortex). BOLD response also increased during the 2.5s PVSAT task in working memory-related areas (bilateral inferior frontal gyrus (IFG), right DLPFC). Reduced BOLD was observed in areas associated with the default mode network (DMN: posterior cingulate cortex (PCC), precuneus, medial frontal cortex, bilateral parietal regions). As both tasks parametrically increased in difficulty they elicited typical BOLD response increases across groups in the same motor planning, attention, and working memory areas (with additional activity in ventrolateral prefrontal cortex (VLPFC) in the n-Back task), and reduced BOLD response in the areas associated with the DMN (Fig.4, column 2; Fig.5, column 2).


Multimodal imaging of mild traumatic brain injury and persistent postconcussion syndrome.

Dean PJ, Sato JR, Vieira G, McNamara A, Sterr A - Brain Behav (2014)

Paced Visual Serial Addition Task fMRI contrast maps. Column 1: Main effect of 2.5s PVSAT block compared to Rest block for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 2: Parametric (linearly modeled) increase in BOLD response from least taxing (2.5s PVSAT) to most taxing (1s PVSAT) for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 3: Group comparison for the 1 > 2.5s PVSAT contrast showing significant BOLD response differences between mTBI + PCS and Control, MTBI-PCS and Control, as well as between mTBI + PCS and mTBI-PCS. In addition, areas where 1 > 2.5s PVSAT contrast significantly correlates with Postconcussion syndrome symptoms as indexed by the Rivermead Postconcussion Symptoms Questionnaire. Red/Yellow Z scale represents areas with significantly increased BOLD response (Z > 1.9); Blue/Green Z scale represents areas with significantly reduced BOLD response (Z > 1.9). Axial, coronal, and sagittal plane coordinates indicated under each image. Neurological Orientation (R=R).
© Copyright Policy - open-access
Related In: Results  -  Collection

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fig05: Paced Visual Serial Addition Task fMRI contrast maps. Column 1: Main effect of 2.5s PVSAT block compared to Rest block for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 2: Parametric (linearly modeled) increase in BOLD response from least taxing (2.5s PVSAT) to most taxing (1s PVSAT) for Control (top row), mTBI-PCS (middle row) and mTBI + PCS (bottom row). Column 3: Group comparison for the 1 > 2.5s PVSAT contrast showing significant BOLD response differences between mTBI + PCS and Control, MTBI-PCS and Control, as well as between mTBI + PCS and mTBI-PCS. In addition, areas where 1 > 2.5s PVSAT contrast significantly correlates with Postconcussion syndrome symptoms as indexed by the Rivermead Postconcussion Symptoms Questionnaire. Red/Yellow Z scale represents areas with significantly increased BOLD response (Z > 1.9); Blue/Green Z scale represents areas with significantly reduced BOLD response (Z > 1.9). Axial, coronal, and sagittal plane coordinates indicated under each image. Neurological Orientation (R=R).
Mentions: Typical BOLD response patterns were observed for all groups for both 0-Back compared to rest (Fig.4, column 1) and 2.5s PVSAT condition compared to rest (Fig.5, column 1). There was increased BOLD response across groups in motor planning and attention-related areas (e.g., premotor cortex, posterior parietal cortex, supplementary motor area [SMA]), as well as other task-relevant areas (contralateral motor cortex, bilateral cerebellum, bilateral visual cortex). BOLD response also increased during the 2.5s PVSAT task in working memory-related areas (bilateral inferior frontal gyrus (IFG), right DLPFC). Reduced BOLD was observed in areas associated with the default mode network (DMN: posterior cingulate cortex (PCC), precuneus, medial frontal cortex, bilateral parietal regions). As both tasks parametrically increased in difficulty they elicited typical BOLD response increases across groups in the same motor planning, attention, and working memory areas (with additional activity in ventrolateral prefrontal cortex (VLPFC) in the n-Back task), and reduced BOLD response in the areas associated with the DMN (Fig.4, column 2; Fig.5, column 2).

Bottom Line: It was hypothesized that only those mTBI participants with persistent PCS would show functional changes, and that these changes would be related to reduced structural integrity and altered metabolite concentrations.There were no behavioral differences between the groups, but participants with greater PCS symptoms exhibited greater activation in attention-related areas (anterior cingulate), along with reduced activation in temporal, default mode network, and working memory areas (left prefrontal) as cognitive load was increased from the easiest to the most difficult task.Functional changes in these areas correlated with reduced structural integrity in corpus callosum and anterior white matter, and reduced creatine concentration in right dorsolateral prefrontal cortex.

View Article: PubMed Central - PubMed

Affiliation: School of Psychology, University Of Surrey Guildford, UK.

ABSTRACT

Background: Persistent postconcussion syndrome (PCS) occurs in around 5-10% of individuals after mild traumatic brain injury (mTBI), but research into the underlying biology of these ongoing symptoms is limited and inconsistent. One reason for this could be the heterogeneity inherent to mTBI, with individualized injury mechanisms and psychological factors. A multimodal imaging study may be able to characterize the injury better.

Aim: To look at the relationship between functional (fMRI), structural (diffusion tensor imaging), and metabolic (magnetic resonance spectroscopy) data in the same participants in the long term (>1 year) after injury. It was hypothesized that only those mTBI participants with persistent PCS would show functional changes, and that these changes would be related to reduced structural integrity and altered metabolite concentrations.

Methods: Functional changes associated with persistent PCS after mTBI (>1 year postinjury) were investigated in participants with and without PCS (both n = 8) and non-head injured participants (n = 9) during performance of working memory and attention/processing speed tasks. Correlation analyses were performed to look at the relationship between the functional data and structural and metabolic alterations in the same participants.

Results: There were no behavioral differences between the groups, but participants with greater PCS symptoms exhibited greater activation in attention-related areas (anterior cingulate), along with reduced activation in temporal, default mode network, and working memory areas (left prefrontal) as cognitive load was increased from the easiest to the most difficult task. Functional changes in these areas correlated with reduced structural integrity in corpus callosum and anterior white matter, and reduced creatine concentration in right dorsolateral prefrontal cortex.

Conclusion: These data suggest that the top-down attentional regulation and deactivation of task-irrelevant areas may be compensating for the reduction in working memory capacity and variation in white matter transmission caused by the structural and metabolic changes after injury. This may in turn be contributing to secondary PCS symptoms such as fatigue and headache. Further research is required using multimodal data to investigate the mechanisms of injury after mTBI, but also to aid individualized diagnosis and prognosis.

Show MeSH
Related in: MedlinePlus