The spatiotemporal profile of diffusion MRI based measures of microstructural changes in white matter evoked by learning novel visual scenes

The ability to learn throughout our lifetime is known to be mediated by structural changes in the brain. However, the spatiotemporal dynamics of such changes during learning are unclear. Here, we trained 10 naïve, adult rhesus monkeys (Macaca mulatta) in two tasks sequentially. The monkeys were first trained to criterion (90%) in the “one-place” task, a visuomotor task which required the monkey to reach and touch an object on a computer screen. Next, the monkeys were trained to touch a target foreground object placed in an artificial visual “scene” composed of multiple geometric elements. The monkeys learned several unique scenes concurrently; the identity and location of the target object differed across scenes, but was fixed within scenes. We acquired multishell advanced Diffusion MRI (dMRI) images from the monkeys across two timepoints (before training and after reaching criterion in one or both tasks) using a Bruker 4.7T MRI system. Behaviorally, the monkeys showed wide individual variability in their ability to learn the different tasks. Whole brain analyses of white matter revealed significant changes in measures of water diffusivity (Radial (RD), Axial (AD), Parenchymal (PD)) but not measures of anisotropy (Fractional, Linear, Planar), between the timepoints. Interestingly, the decrease in PD, a measure of tissue density without freewater contamination, was correlated with faster learning of the visual scenes task. Analysis comparing monkeys that mastered the scenes task and those that did not, indicated a focal change in RD along the crus of the fornix. Further examination revealed that a decrease in diffusivity measures in the crus, possibly due to an increase in restricted/hindered water diffusion, tends to be correlated with faster scene learning. Overall, the pattern of changes in the dMRI measures suggest that prolonged learning of complex visual scenes evokes global as well as local changes in white matter microstructure.