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The superior longitudinal fasciculus and its functional triple-network mechanisms in brooding.

ABSTRACT: Brooding, which refers to a repetitive focus on one's distress, is associated with functional connectivity within Default-Mode, Salience, and Executive-Control networks (DMN; SN; ECN), comprising the so-called "triple-network" of attention. Individual differences in brain structure that might perseverate dysfunctional connectivity of brain networks associated with brooding are less clear, however. Using diffusion and functional Magnetic Resonance Imaging, we explored multimodal relationships between brooding severity, white-matter microstructure, and resting-state functional connectivity in depressed adults (N?=?32-44), and then examined whether findings directly replicated in a demographically-similar, independent sample (N?=?36-45). Among the fully-replicated results, three core findings emerged. First, brooding severity is associated with functional integration and segregation of the triple-network, particularly with a Precuneal subnetwork of the DMN. Second, microstructural asymmetry of the Superior Longitudinal Fasciculus (SLF) provides a robust structural connectivity basis for brooding and may account for over 20% of its severity (Discovery: adj. R²?=?0.18; Replication: adj. R²?=?0.22; MSE?=?0.06, Predictive R²?=?0.22). Finally, microstructure of the right SLF and auxiliary white-matter is associated with the functional connectivity correlates of brooding, both within and between components of the triple-network (Discovery: adj. R²?=?0.21; Replication: adj. R²?=?0.18; MSE?=?0.03, Predictive R²?=?0.21-0.22). By cross-validating multimodal discovery with replication, the present findings help to reproducibly unify disparate perspectives of brooding etiology. Based on that synthesis, our study reformulates brooding as a microstructural-functional connectivity neurophenotype.

SUBMITTER: Pisner DA

PROVIDER: S-EPMC6664225 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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The superior longitudinal fasciculus and its functional triple-network mechanisms in brooding.

Pisner D A DA Shumake J J Beevers C G CG Schnyer D M DM

NeuroImage. Clinical 20190719

Brooding, which refers to a repetitive focus on one's distress, is associated with functional connectivity within Default-Mode, Salience, and Executive-Control networks (DMN; SN; ECN), comprising the so-called "triple-network" of attention. Individual differences in brain structure that might perseverate dysfunctional connectivity of brain networks associated with brooding are less clear, however. Using diffusion and functional Magnetic Resonance Imaging, we explored multimodal relationships bet ...[more]

PMID: 31352219

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Project description:AimTo understand the relationship between cognition and white-matter structure in adolescents born preterm without obvious brain injury.MethodsThirty-two adolescents from a longitudinal study of child development were selected according to risk of developmental disorders at birth (born at term: eight males, five females; median age 16y 1mo, interquartile range 10mo; low risk preterm: four males, five females, median age 16y, range 4mo; high risk preterm: three males, seven females, median age 16y 2mo, range 1y 2mo) and reading ability (good: three males, eight females, median age 16y, range 7mo; average: six males, three females, median age 16y 10mo, range 1y; poor: six males, six females, median age 16y, range 6mo). Preterm birth was defined as a gestational age of 36 weeks or less and a birthweight of 1600g or less. All participants had normal clinical neuroimaging findings. We examined fractional anisotropy, radial diffusivity, and volume of three major white-matter fasciculi. The relationship between structural measures and birth risk, hemisphere, and cognitive ability (attention, lexical and sublexical decoding, auditory phonological awareness, and processing speed) were analysed using mixed-model regression.ResultsLeft-hemisphere superior longitudinal fasciculus (SLF) fractional anisotropy and radial diffusivity were linked to reading-related skills (fractional anisotropy vs letter-word identification, r((30))=-0.37, p<0.05; fractional anisotropy vs phoneme reversal, r((30))=-0.34, p=0.05; radial diffusivity vs letter-word identification, r((30))=0.31, p<0.10; radial diffusivity vs phoneme reversal, r((30))=0.40, p<0.05), whereas right-hemisphere SLF fractional anisotropy was related to attention skills (fractional anisotropy vs inattentiveness, r((30))=-0.38, p<0.05). SLF volume decreased as these skills declined for adolescents born preterm (volume vs phoneme reversal, r((17))=0.58, p<0.01; volume vs inattentiveness, r((17))=-0.69, p<0.01), but not for those born at term.InterpretationThe relationship between cognitive skills and SLF volume suggests that in adolescents born preterm, cryptic white-matter injury may exist, possibly related to oligodendrocyte or axonal loss, despite normal clinical neuroimaging.

Project description:BackgroundWearable devices have been found effective in training ankle control in patients with neurological diseases. However, the neural mechanisms associated with using wearable devices for ankle training remain largely unexplored. This study aimed to investigate the ankle tracking performance and brain white matter changes associated with ankle tracking learning using a wearable-device system and the behavior-brain structure relationships in middle-aged and older adults.MethodsTwenty-six middle-aged and older adults (48-75 years) participated in this study. Participants underwent 5-day ankle tracking learning with their non-dominant foot using a custom-built ankle tracking system equipped with a wearable sensor and a sensor-computer interface for real-time visual feedback and data acquisition. Repeated and random sequences of target tracking trajectories were both used for learning and testing. Ankle tracking performance, calculated as the root-mean-squared-error (RMSE) between the target and actual ankle trajectories, and brain diffusion spectrum MR images were acquired at baseline and retention tests. The general fractional anisotropy (GFA) values of eight brain white matter tracts of interest were calculated to indicate their integrity. Two-way (Sex × Time) mixed repeated measures ANOVA procedures were used to investigate Sex and Time effects on RMSE and GFA. Correlations between changes in RMSE and those in GFA were analyzed, controlling for age and sex.ResultsAfter learning, both male and female participants reduced the RMSE of tracking repeated and random sequences (both p < 0.001). Among the eight fiber tracts, the right superior longitudinal fasciculus II (R SLF II) was the only one which showed both increased GFA (p = 0.039) after learning and predictive power of reductions in RMSE for random sequence tracking with its changes in GFA [β = 0.514, R2 change = 0.259, p = 0.008].ConclusionsOur findings implied that interactive tracking movement learning using wearable sensors may place high demands on the attention, sensory feedback integration, and sensorimotor transformation functions of the brain. Therefore, the SLF II, which is known to perform these brain functions, showed corresponding neural plasticity after such learning, and its plasticity also predicted the behavioral gains. The SLF II appears to be a very important anatomical neural correlate involved in such learning paradigms.

Dataset Information

The superior longitudinal fasciculus and its functional triple-network mechanisms in brooding.

Publications

The superior longitudinal fasciculus and its functional triple-network mechanisms in brooding.

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