Tract-Specific White Matter Correlates of Age-Related Reward Devaluation Deficits in Macaque Monkeys.

Daniel T Gray,Carol A Barnes,Lavanya Umapathy,Sara N Burke,Theodore P Trouard

doi:10.17756/jnpn.2018-023

Abstract

Aim:Cognitive aging is known to alter reward-guided behaviors that require interactions between the orbitofrontal cortex (OFC) and amygdala. In macaques, OFC, but not amygdala volumes decline with age and correlate with performance on a reward devaluation (RD) task. The present study used diffusion magnetic resonance imaging (dMRI) methods to investigate whether the condition of the white matter associated with amygdala-OFC connectivity changes with age and relates to reward devaluation.Methods:Diffusion-, T1- and T2-weighted MRIs were acquired from adult and aged bonnet macaques. Using probabilistic tractography, fractional anisotropy (FA) estimates from two separate white matter tracts associated with amygdala-OFC connectivity, the uncinate fasciculus (UF) and amygdalofugal (AF) pathways, were obtained. Performance measures on RD and reversal learning (RL) tasks were also acquired and related to FA indices from each anatomical tract.Results:Aged monkeys were impaired on both the RD and RL tasks and had lower FA indices in the AF pathway. Higher FA indices from the right hemisphere UF pathway correlated with better performance on an object-based RD task, whereas higher FA indices from the right hemisphere AF were associated with better performance on an object-free version of the task. FA measures from neither tract correlated with RL performance.Conclusions:These results suggest that the condition of the white matter connecting the amygdala and OFC may impact reward devaluation behaviors. Furthermore, the observation that FA indices from the UF and AF differentially relate to reward devaluation suggests that the amygdala-OFC interactions that occur via these separate tracts are partially independent.

Highlights

The ability to revalue reinforced stimuli according to changing biological or psychological needs is a critical component of adaptive, reward-driven behaviors since it affords animals the ability to select advantageous action plans when presented with competing cues
Higher fractional anisotropy (FA) indices from the right hemisphere uncinate fasciculus (UF) pathway correlated with better performance on an object-based reward devaluation (RD) task, whereas higher FA indices from the right hemisphere AF were associated with better performance on an object-free version of the task
These results suggest that the condition of the white matter connecting the amygdala and orbitofrontal cortex (OFC) may impact reward devaluation behaviors

Summary

Introduction

The ability to revalue reinforced stimuli according to changing biological or psychological needs is a critical component of adaptive, reward-driven behaviors since it affords animals the ability to select advantageous action plans when presented with competing cues. If similar lesions are restricted to the dorsolateral or ventrolateral prefrontal cortices, monkeys are not different from controls when tested on reward devaluation tasks [7, 8], indicating that the OFC, in particular, is the primary prefrontal cortical area underlying devaluation function. In agreement with these lesion studies, OFC area 11/13 volumes were shown to correlate with reward devaluation performance, but not with performance on a reversal learning task [1] - a behavior that remains intact following lesions to the amygdala-OFC network [4, 8, 10]. Within the context of reward devaluation, the amygdala is thought to update reward-value information, while the OFC appears to use this information to represent and update outcome expectancies used to guide decision making behavior [4, 11]

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