Associative white matter tracts selectively predict sensorimotor learning.

Human learning varies greatly among individuals and is related to the microstructure of major white matter tracts in several learning domains, yet the impact of the existing microstructure of white matter tracts on future learning outcomes remains unclear. We employed a machine-learning model selection framework to evaluate whether existing microstructure might predict individual differences in learning a sensorimotor task, and further, if the mapping between tract microstructure and learning was selective for learning outcomes. We used diffusion tractography to measure the mean fractional anisotropy (FA) of white matter tracts in 60 adult participants who then practiced drawing a set of 40 unfamiliar symbols repeatedly using a digital writing tablet. We measured drawing learning as the slope of draw duration over the practice session and measured visual recognition learning for the symbols using an old/new 2-AFC task. Results demonstrated that tract microstructure selectively predicted learning outcomes, with left hemisphere pArc and SLF3 tracts predicting drawing learning and the left hemisphere MDLFspl predicting visual recognition learning. These results were replicated using repeat, held-out data and supported with complementary analyses. Results suggest that individual differences in the microstructure of human white matter tracts may be selectively related to future learning outcomes.

Associative white matter tracts selectively predict sensorimotor learning.

Human learning is a complex phenomenon that varies greatly among individuals and is related to the microstructure of major white matter tracts in several learning domains, yet the impact of the existing myelination of white matter tracts on future learning outcomes remains unclear. We employed a machine-learning model selection framework to evaluate whether existing microstructure might predict individual differences in the potential for learning a sensorimotor task, and further, if the mapping between the microstructure of major white matter tracts and learning was selective for learning outcomes. We used diffusion tractography to measure the mean fractional anisotropy (FA) of white matter tracts in 60 adult participants who then underwent training and subsequent testing to evaluate learning. During training, participants practiced drawing a set of 40 novel symbols repeatedly using a digital writing tablet. We measured drawing learning as the slope of draw duration over the practice session and visual recognition learning as the performance accuracy in an old/new 2-AFC recognition task. Results demonstrated that the microstructure of major white matter tracts selectively predicted learning outcomes, with left hemisphere pArc and SLF 3 tracts predicting drawing learning and the left hemisphere MDLFspl predicting visual recognition learning. These results were replicated in a repeat, held-out data set and supported with complementary analyses. Overall, results suggest that individual differences in the microstructure of human white matter tracts may be selectively related to future learning outcomes and open avenues of inquiry concerning the impact of existing tract myelination in the potential for learning. Significance statement: A selective mapping between tract microstructure and future learning has been demonstrated in the murine model and, to our knowledge, has not yet been demonstrated in humans. We employed a data-driven approach that identified only two tracts, the two most posterior segments of the arcuate fasciculus in the left hemisphere, to predict learning a sensorimotor task (drawing symbols) and this prediction model did not transfer to other learning outcomes (visual symbol recognition). Results suggest that individual differences in learning may be selectively related to the tissue properties of major white matter tracts in the human brain.

Development of human hippocampal subfield microstructure and relation to associative inference.

The hippocampus is a complex brain structure composed of subfields that each have distinct cellular organizations. While the volume of hippocampal subfields displays age-related changes that have been associated with inference and memory functions, the degree to which the cellular organization within each subfield is related to these functions throughout development is not well understood. We employed an explicit model testing approach to characterize the development of tissue microstructure and its relationship to performance on two inference tasks, one that required memory (memory-based inference) and one that required only perceptually available information (perception-based inference). We found that each subfield had a unique relationship with age in terms of its cellular organization. While the subiculum (SUB) displayed a linear relationship with age, the dentate gyrus (DG), cornu ammonis field 1 (CA1), and cornu ammonis subfields 2 and 3 (combined; CA2/3) displayed non-linear trajectories that interacted with sex in CA2/3. We found that the DG was related to memory-based inference performance and that the SUB was related to perception-based inference; neither relationship interacted with age. Results are consistent with the idea that cellular organization within hippocampal subfields might undergo distinct developmental trajectories that support inference and memory performance throughout development.

Development of white matter tracts between and within the dorsal and ventral streams.

The degree of interaction between the ventral and dorsal visual streams has been discussed in multiple scientific domains for decades. Recently, several white matter tracts that directly connect cortical regions associated with the dorsal and ventral streams have become possible to study due to advancements in automated and reproducible methods. The developmental trajectory of this set of tracts, here referred to as the posterior vertical pathway (PVP), has yet to be described. We propose an input-driven model of white matter development and provide evidence for the model by focusing on the development of the PVP. We used reproducible, cloud-computing methods and diffusion imaging from adults and children (ages 5-8 years) to compare PVP development to that of tracts within the ventral and dorsal pathways. PVP microstructure was more adult-like than dorsal stream microstructure, but less adult-like than ventral stream microstructure. Additionally, PVP microstructure was more similar to the microstructure of the ventral than the dorsal stream and was predicted by performance on a perceptual task in children. Overall, results suggest a potential role for the PVP in the development of the dorsal visual stream that may be related to its ability to facilitate interactions between ventral and dorsal streams during learning. Our results are consistent with the proposed model, suggesting that the microstructural development of major white matter pathways is related, at least in part, to the propagation of sensory information within the visual system.

Visual-motor contingency during symbol production contributes to short-term changes in the functional connectivity during symbol perception and long-term gains in symbol recognition.

Letter production relies on a tight coupling between motor movements and visual feedback-each stroke of the letter is visually experienced as it is produced. Experience with letter production leads to increases in functional connectivity, a measure of neural communication, among visual and motor brain systems and leads to gains in letter recognition in preliterate children. We hypothesized that the contingency between the motor and visual experiences of the written form during production would result in both effects. Twenty literate adults were trained on four sets of novel symbols over the course of one week. Each symbol set was trained through one of four training conditions: drawing with ink, drawing without ink, watching a handwritten symbol unfold as if being drawn, and watching a static handwritten symbol. Contingency of motor and visual experiences occurred in the drawing with ink condition. The motor and visual experiences were rendered non-contingent in each of the other three conditions by controlling for visual or motor experience. Participants were presented with the trained symbols during fMRI scanning at three time points: one pre-training, one post-training, and one after a week-long no-training delay. Recognition was tested after each training session and after the third scan. We found that the contingency between visual and motor experiences during production changed the pattern of functional connectivity among visual, motor, and auditory neural communities and resulted in better recognition performance at post-training than at pre-training. Recognition gains were maintained after the no-training delay, but the functional connections observed immediately after training returned to their pre-training baselines. Our results suggest that behaviors that couple sensory and motor systems result in temporary changes in neural communication during perception that may not directly support changes in recognition.