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Official websites use. Share sensitive information only on official, secure websites. Address correspondence to: Stephen R. McCauley, Ph. E-mail: mccauley bcm. Few studies exist investigating the brain-behavior relations of event-based prospective memory EB-PM impairments following traumatic brain injury TBI. To address this, children with moderate-to-severe TBI performed an EB-PM test with two motivational enhancement conditions and underwent concurrent diffusion tensor imaging DTI at 3 months post-injury. Significant group differences were found for fractional anisotropy FA and apparent diffusion coefficient for orbitofrontal white matter WM , cingulum bundles, and uncinate fasciculi. Keywords: cingulum bundles, diffusion tensor imaging, event-based prospective memory, incentive, motivation, pediatrics orbitofrontal white matter, traumatic brain injury, uncinate fasciculus. P rospective memory PM involves a combination of memorial and executive processes that allow one to form intentions that are executed at a later time. Event-based PM EB-PM tasks are triggered by an external cue Einstein and McDaniel, , such as telling a friend of an upcoming party when they are seen next or giving school permission slips to a parent to sign. Everyday life for children and adults alike is replete with instrumental activities, such as PM tasks, to the extent that PM is an essential ability to effectively manage the challenges of daily living Harris, ; Meacham and Dumitru, ; Winograd, Neurologic insults such as traumatic brain injury TBI have been shown to result in impairments of PM performance in adults Cockburn, ; Fortin et al. Although brain-behavior relations of episodic i. One recent neuroimaging study addressing this gap McCauley et al. While this study of cortical gray matter thickness was one of the first to investigate brain-behavior relations between TBI and EB-PM in children, it did not investigate brain regions that may be specifically related to motivation-based EB-PM behavior. Lesion studies have supported the supposition that damage to medial prefrontal areas, temporal cortex Burgess et al. More recent PET work by Okuda and colleagues has implicated bilateral frontal poles, left lingual gyrus, right gyrus rectus, and the anterior cingulate gyrus in subserving EB-PM. Other imaging modalities have yet to be deployed to further our understanding of neural mechanisms underlying PM and the neuropathological processes that impair PM. Diffusion tensor imaging DTI is a relatively new imaging technique that incorporates specific pulsed magnetic field gradients into a standard MRI sequence increasing sensitivity to the diffusion of water molecules Lazar et al. In normal brain tissue, there are physical boundaries restricting water diffusion in white matter WM , resulting in greater water movement parallel to axons with less movement perpendicular to axons. This diffusion restriction is referred to as fractional anisotropy FA; the ratio of anisotropy to isotropy ; FA ranges from 0 to 1, where values nearer to 0 are representative of isotropy or increased diffusion e. Conversely, values closer to 1 represent water diffusion more parallel to WM fiber tracts in normal brain tissue. Isotropic water diffusion is also commonly measured by the apparent diffusion coefficient ADC , which is the mean diffusivity across eigenvalues. Generally speaking, measures of diffusivity such as ADC are inversely related to FA; however, while both ADC and FA reflect changes in WM microstructure, the association between these two indices is complex and incompletely understood. The relation of FA and ADC to WM integrity may be influenced by dynamic processes during childhood and adolescent development, making it a particularly useful imaging tool in detecting neuropathological changes that occur in this population Yung et al. Three regions of interest ROIs were selected for this study based on the following criteria: 1 white matter tracts or regions that are amenable to quantitative tractography using DTI, and 2 white matter underlying structures with known involvement in either memory functioning or reward processing. Based on these criteria, the cingulum bundle, orbitofrontal white matter, and uncinate fasciculi were selected. The hippocampus was not selected as it is primarily a gray matter structure that is difficult to assess reliably using DTI tractography. The cingulum bundle is a critical fiber pathway coursing the cingulate gyrus, possessing myriad connections linking the prefrontal cortex and parietal areas i. The anterior cingulate cortex has been linked with emotion, cognition, memory, and motor functions while the posterior aspect has been specifically associated with memory and pain perception Burianova et al. Moreover, non-human primate Amiez et al. Of particular interest to this study is the function of the anterior cingulate in responding to monetary incentives Akitsuki et al. Significant atrophy and dysfunction of the cingulate has been reported after TBI Yount et al. In addition to supporting general cognitive flexibility and allowing both shifting and focused attention, the cingulum bundle is important in learning and memory in adolescents with mild TBI Wu et al. Advanced neuroimaging techniques, such as DTI Fellgiebel et al. The orbitofrontal region and orbitofrontal-amygdala system has been shown to be involved in a number of functions including emotion and motivation in non-human primate Barbas, a , b ; Schultz et al. Functional neuroimaging and brain lesion studies have revealed lateralized functions of the orbital frontal in that the left orbital frontal is involved in positive or reward-related affect whereas the right orbital frontal is involved in negative or punishment-related affect Eddington et al. Recent work supports the concept that motivation can alter top-down modulation of executive functions Gazzaley et al. In a recent fMRI study, Szatkowska and colleagues reported that verbal working memory performance n -back paradigm was modulated by the orbital frontal cortex; structural equation modeling revealed that under the low motivation no money condition, the left and right orbital frontal positively increased the activation of the dorsolateral prefrontal cortex, but in the high motivation condition monetary incentive , the right orbital frontal cortex exerted a strong negative influence on the activation of the left dorsolateral prefrontal cortex. The uncinate fasciculus is a principal white matter tract connecting the temporal pole and other anterior temporal areas to the inferior region of the frontal lobe Bracht et al. The uncinate fasciculus has been identified as a critical part of the temporal-neocortical memory system Squire and Zola-Morgan, Reduced structural integrity of the uncinate fasciculus has been related to episodic and working memory performance in healthy adults Charlton et al. The integrity of the uncinate fasciculus is also positively related to performance on verbal- and visual-based tasks of episodic memory in healthy children and adolescents Mabbott et al. Despite considerable evidence of shared and unique neural networks involved in PM, very few studies to date have explored the relation between EB-PM performance and neuropathological changes following TBI in children and adolescents. To address this gap, we investigated EB-PM in children and adolescents with moderate-to-severe TBI and concurrent MRI at 3 months post-injury in a prospective cohort using the same experimental methodology as that reported previously McCauley et al. In our study of the neural correlates of EB-PM, motivation was varied using two levels of monetary incentive i. The OI participants were included to control for risk factors predisposing children to traumatic injury and to equate for other nonspecific factors e. All participants were fluent in English, the product of full-term births i. Child assent was obtained in accordance with current federal regulations. Participants were recruited prospectively from consecutive admissions to American College of Surgeons Level-1 trauma centers in Houston, Dallas, and Miami as part of a longitudinal study of the neurobehavioral outcomes of children following moderate-to-severe TBI. All participants underwent magnetic resonance imaging MRI without sedation on Philips 1. All scanners were in a similar range on Weisskoff testing and this was considered acceptable through consensus of the neuroradiologists on the study. Transverse multislice spin echo, single shot, echo planar imaging EPI sequences were used Diffusion was measured along 15 directions no. To improve the signal-to-noise ratio, each high b-value image was acquired twice and averaged, with the low b image acquired once. All data were carefully inspected for any artifacts or irregularities that may have compromised its accuracy or reliability. ROIs were created using established protocols detailed in previous publications and described briefly below. After ROIs were created, automated Philips three-dimensional fiber tracking tool Hoogenraad, was utilized to determine fiber tracks passing through the cingulum bundle, orbital frontal white matter, and uncinate fasciculus. The algorithm for fiber tracking is based upon the fiber assignment by continuous tracking FACT method Mori et al. Two experienced raters independently measured FA twice for the right and left sides of the three target structures in a subset of 11 participants with TBI and 11 participants with OI. Intra- and inter-rater reliabilities were calculated using Shrout-Fleiss reliability statistics Shrout and Fleiss, to obtain intra-class correlation coefficients ICCs that were all above 0. Our methods for defining the cingulum bundle have been presented previously Wilde et al. In brief, the ROI originated from the cingulum bundle and was created on FA color maps in the left and right parasagittal planes. Using the automatic 3D ROI algorithm function, two to three seed points were placed linearly along the cingulum bundle in the right and parasagittal planes separately. The multi-ROI fiber tracking function was used to select fibers that were common to the three ROIs, and the software provided the statistics including the mean FA and ADC for the selected fibers comprising the cingulum bundle. Methods used by our group to measure the orbital frontal and interrater reliability coefficients have been previously presented Levin et al. In short, ROIs were drawn in the coronal plane on a slice just anterior to the first slice where the genu of the corpus callosum was visible. A line extending from the interhemispheric fissure at a point just inferior to the corpus callosum to the lateral orbital sulci formed the superior boundary of the orbital frontal region all WM inferior to this line. In brief, our method isolated fibers traversing the two ROIs that comprise the uncinate fasciculus. The first ROI was demarcated on the coronal slice just anterior to the first visible slice of the genu of the corpus callosum and incorporated all WM in the cerebral hemisphere. The second ROI was delineated on a coronal slice at the level of anterior commissure to include WM in the temporal lobes. The study used a crossover design with two motivation conditions, each lasting one hour with no wash-out interval between motivation conditions. Briefly, the extrinsic motivation conditions involved the monetary units of either dollars high motivation or pennies low motivation ; participants were told that all payments would occur after the task was completed. A randomization table was used to randomize motivation condition order sequence across participants. Instructions for each condition were administered at the beginning of the first and second hours periods of testing. The scoring algorithm for the EB-PM task was: 2 points for realizing the delayed intention PM component and 2 additional points for recalling the correct phrase retrospective memory component or RM. Correct responses were awarded 4 points, and responses with incorrect RM content e. A maximum of 12 points was available in each of the two conditions. No performance feedback was given until after both conditions had been completed. Cash payments were made at the end of the testing session, well after completing the EB-PM task. All analyses were conducted with SAS software for Windows v9. The participant variable was treated as a random effect to account for correlation between multiple measures within the same participant. Other main effects of interest included age-at-test, socioeconomic composite index, gender, group TBI vs. OI , laterality left vs. No other between-group comparisons for continuous variables were significant, including the socioeconomic composite index. Results of the EB-PM task itself in a subsample partially overlapping the group in this study at the same time point have been previously presented McCauley et al. Least-squares means LS-means and standard errors SE are presented. Older Age-at-Test was associated with higher FA. Error bars depict standard errors. Significant correlations were found in the TBI group under the high motivation condition for the right and left orbital frontal white matter with FA positive , and the left orbital frontal with ADC negative. Finally, a significant correlation was found in the TBI group for FA in the right uncinate fasciculus under the high and low motivation conditions. After adjusting for the number of correlations performed within each motivation condition i. To determine the relative contribution of each of the ROIs to EB-PM performance, three linear regression models were performed in the TBI group; models did not include the OI group given the absence of significant brain-behavior correlations. Given this, we explored a set of models with the EB-PM score as the dependent variable with Age-at-Test as a covariate under the two motivation conditions separately; parallel analyses were conducted for FA and ADC. For ADC, no model was significant under either motivation condition. None of the overall F -tests of the models using FA were significant. Analyses were then conducted using ADC and, again, no model produced a significant overall F -test. This is consistent with prior studies that found similar patterns of DTI metrics in the cingulum bundle Kraus et al. We found partial support for our second hypothesis that the DTI metrics of the three ROIs would be correlated with EB-PM performance under both high and low motivation conditions; brain-behavior relations using FA were only significant under the high motivation condition, and only one ROI left orbital frontal was significant using ADC. These results suggest that WM tract integrity becomes crucial when the individual is motivated to increase effort and that the loss of WM integrity may present an upper limit in terms of potentially achievable performance levels. Our primary goal in this study was to determine whether behavior was related to FA and ADC in specific regions in a population of TBI patients with different degrees of cognitive dysfunction and WM alteration in these areas rather than to undertake this investigation in neurologically intact participants, which would require more subjects and would reach beyond the scope of the current study. Of the models assessed, only FA under the high motivation condition had a significant overall F -test; further, only FA of the right uncinate fasciculus was significant under the low motivation condition. While not initially anticipated, this is not inconsistent given brain-behavior correlations addressing our first hypothesis, which only reached significance under the high motivation condition. These results also suggest that the integrity of the fiber tracts is most crucial under high task demand conditions created as a response to the high level of extrinsic reward for performance. The significant role played by the left cingulum bundle in mediating the response to motivators monetary incentives, in particular has been clearly demonstrated Akitsuki et al. Similarly, the function of the orbital frontal in motivated behavior is well-known Elliott et al. Our results are consistent with previous research demonstrating the greater role of the left relative to the right orbital frontal white matter in mediating positive or reward-related affect and emotion-related learning Eddington et al. These results demonstrate that WM structures known to be important in PM and episodic memory i. While there are no published studies directly evaluating the role of the uncinate fasciculus in PM, its function in episodic and working memory processes is well-established in both healthy and neurologically impaired populations Charlton et al. Our results lend supporting evidence to this speculation given the significant contribution that the right and left uncinate fasciculi make to high-motivated EB-PM functioning, and even the role the right uncinate fasciculus plays in low motivation performance. Regarding the effects of demographic variables on EB-PM performance, no gender effect was found, which is consistent with studies of normal adults Einstein and McDaniel, ; Kidder et al. This is similar to findings of McCauley and colleagues McCauley et al. There are some limitations in this study that should be addressed. Retrospective memory was not assessed due to the design of the longitudinal study. This was unfortunate as it could have demonstrated the degree to which impaired retrospective memory abilities may have accounted for impaired EB-PM performance in these children. Studies have found that PM and retrospective memory are clearly dissociable Maylor et al. The close relation of these two memory categories has been demonstrated in early development, but they reportedly diverge very rapidly thereafter Guajardo and Best, ; Ruther and Best, However, studies in adult TBI have produced contradictory findings concerning the relation between retrospective memory and PM Groot et al. Future work will be required to determine to what extent PM in children with TBI relies on intact retrospective memory capabilities; therefore, generalizing discrepant adult TBI results to children with TBI is not advised. K23 HD to S. NS to H. The information in this article has never been published before, either electronically or in print. I would like to extend my personal appreciation to Drs. Mark McDaniel and Harvey Levin, who graciously served as mentors on a K mentored patient-oriented research career development award. We also thank the participants and their families for their interest and willingness to take part in this research. None of the authors have financial or other relationships that could be construed as a conflict of interest with respect to the content of this article. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Medical Rehabilitation Research or the National Institutes of Health. As a library, NLM provides access to scientific literature. J Neurotrauma. Find articles by Stephen R McCauley. Find articles by Elisabeth A Wilde. Find articles by Erin D Bigler. Find articles by Zili Chu. Find articles by Ragini Yallampalli. Find articles by Margaret B Oni. Find articles by Trevor C Wu. Find articles by Marco A Ramos. Find articles by Claudia Pedroza. Find articles by Jill V Hunter. Find articles by Harvey S Levin. Copyright , Mary Ann Liebert, Inc. Open in a new tab. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. 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Click here to access the corresponding ESC CardioMed chapters. Keywords. Guidelines • Anti-arrhythmic drugs • Cardiac magnetic resonance • Cardiomyopathies •.
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