Inter-individual variation in fronto-temporal connectivity predicts the ability to learn different types of associations

Abstract

The uncinate fasciculus connects portions of the anterior and medial temporal lobes to the lateral orbitofrontal cortex, so it has long been thought that this limbic fiber pathway plays an important role in episodic memory. Some types of episodic memory are impaired after damage to the uncinate, while others remain intact. Because of this, the specific role played by the uncinate fasciculus in episodic memory remains undetermined. In the present study, we tested the hypothesis that the uncinate fasciculus is involved in episodic memory tasks that have high competition between representations at retrieval. To test this hypothesis, healthy young adults performed three tasks: Experiment 1 in which they learned to associate names with faces through feedback provided at the end of each trial; Experiment 2 in which they learned to associate fractals with cued locations through feedback provided at the end of each trial; and Experiment 3 in which unique faces were remembered in a paradigm with low retrieval competition. Diffusion tensor imaging and deterministic tractography methods were used to extract measures of uncinate fasciculus microstructure. Results revealed that microstructural properties of the uncinate, but not a control tract, the inferior longitudinal fasciculus, significantly predicted individual differences in performance on the face-name and fractal-location tasks. However, no relationship was observed for simple face memory (Experiment 3). These findings suggest that the uncinate fasciculus may be important for adjudicating between competing memory representations at the time of episodic retrieval.

Keywords: Associative memory; Diffusion imaging; Faces; Limbic; Orbitofrontal cortex; Proper names; Temporal pole; Uncinate fasciculus; White matter.

Figure 1

(a) Schematics of the associative learning tasks. In Experiment 1 (left), participants learned face-name pairs, while in Experiment 2 (right), they learned fractal-asterisk location pairs. (b) Behavioral performance plotted across learning blocks for each experiment. The blue line depicts mean accuracy (percent correct) for each learning block. Error bars represent standard error of the mean. The green and red lines depict learning curves for the participants with the highest and lowest performance, respectively. (c) Overall learning accuracy (percent correct on the last learning block) is plotted for each participant to display the individual variability among participants. The numbers on the x-axis are a rank for each participant. (d) Learning rate (change in accuracy from Block 1 to Block 2) is plotted for each participant. The x-axis again represents a rank order of participants.

Figure 2

(a) Tractography delineating the uncinate fasciculus (UF; red) and inferior longitudinal fasciculus (ILF; purple) in a sample participant. (b) Scatter plots of residuals from the linear regression analyses illustrating the relationship between individual differences in overall learning on the face-name task (y-axis) and mean fractional anisotropy (FA) of the left UF (left) and left ILF (right). A significant effect was observed only in the UF. (c) Scatter plots of the residuals from the linear regression analyses illustrating the relationship between individual differences in overall learning on the face-name task and mean axial diffusivity (AD) of the left UF (left) and the left ILF (right). A significant effect was observed only in the UF. (d) Scatter plots of the residuals from the linear regression analyses illustrating the relationship between individual differences in learning rate on the fractal-asterisk task and mean AD of the right UF (left) and the right ILF (right). A significant effect was observed only in the UF.