Brain white matter correlates of learning ankle tracking using a wearable device: importance of the superior longitudinal fasciculus II

Abstract

Background Wearable 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. Methods Twenty-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. Results After 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]. Conclusions Our 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.

Brain white matter pathways of resilience to chronic back pain: a multisite validation

“…(57) Similarly, a recent study showed that SLF II underwent plastic changes after learning of tracking movement tasks requiring both top-down attentional processes and bottom-up somatosensory feedback to adjust one’s own movement, and the degree of this plasticity predicted task-related success. (58) Since the constant adaptation of motor control in these tasks is dependent on spatial awareness and proprioception, the integrity of the SLF II appears crucial to their intact functioning. Proprioception, which is a bottom-up somatic signal closely related to visuospatial processing, is critical for recognizing one’s own body position and hence the awareness of the physical self.…”

“…The data set obtained through the OpenPain.org online database (collected in Chicago, from now on, we refer to this data set as "Chicago data set") had 58…”