Fronto-temporal white matter connectivity predicts reversal learning errors

Abstract

Each day, we make hundreds of decisions. In some instances, these decisions are guided by our innate needs; in other instances they are guided by memory. Probabilistic reversal learning tasks exemplify the close relationship between decision making and memory, as subjects are exposed to repeated pairings of a stimulus choice with a reward or punishment outcome. After stimulus-outcome associations have been learned, the associated reward contingencies are reversed, and participants are not immediately aware of this reversal. Individual differences in the tendency to choose the previously rewarded stimulus reveal differences in the tendency to make poorly considered, inflexible choices. Lesion studies have strongly linked reversal learning performance to the functioning of the orbitofrontal cortex, the hippocampus, and in some instances, the amygdala. Here, we asked whether individual differences in the microstructure of the uncinate fasciculus, a white matter tract that connects anterior and medial temporal lobe regions to the orbitofrontal cortex, predict reversal learning performance. Diffusion tensor imaging and behavioral paradigms were used to examine this relationship in 33 healthy young adults. The results of tractography revealed a significant negative relationship between reversal learning performance and uncinate axial diffusivity, but no such relationship was demonstrated in a control tract, the inferior longitudinal fasciculus. Our findings suggest that the uncinate might serve to integrate associations stored in the anterior and medial temporal lobes with expectations about expected value based on feedback history, computed in the orbitofrontal cortex.

Keywords: decision making; diffusion imaging; hippocampus; orbitofrontal cortex; reversal learning; uncinate fasciculus.

FIGURE 1

Behavioral performance on the Iowa Gambling Task (IGT). Group performance is plotted across test blocks (top). IGT net score reflects the sum of disadvantageous deck choices subtracted from the sum of advantageous deck choices. Error bars represent standard error of the mean. Specific to the reversal phase, the total number of reversal errors committed is plotted for each participant (bottom) to display the individual variability among participants.

FIGURE 2

Tractography delineating the uncinate fasciculus (UF; red) and inferior longitudinal fasciculus (ILF; purple) in a sample participant (left). Scatter plots of residuals from the linear regression analyses (right) illustrating the relationship between individual differences in reversal errors and mean left axial diffusivity (AD) of the respective white matter tracts.