Dissociable corticostriatal circuits underlie goal-directed vs. cue-elicited habitual food seeking after satiation: evidence from a multimodal MRI study

Abstract

The present multimodal MRI study advances our understanding of the corticostriatal circuits underlying goal-directed vs. cue-driven, habitual food seeking. To this end, we employed a computerized Pavlovian-instrumental transfer paradigm. During the test phase, participants were free to perform learned instrumental responses (left and right key presses) for popcorn and Smarties outcomes. Importantly, prior to this test half of the participants had been sated on popcorn and the other half on Smarties - resulting in a reduced desirability of those outcomes. Furthermore, during a proportion of the test trials, food-associated Pavlovian cues were presented in the background. In line with previous studies, we found that participants were able to perform in a goal-directed manner in the absence of Pavlovian cues, meaning that specific satiation selectively reduced responding for that food. However, presentation of Pavlovian cues biased choice toward the associated food reward regardless of satiation. Functional MRI analyses revealed that, in the absence of Pavlovian cues, posterior ventromedial prefrontal cortex tracked outcome value. In contrast, during cued trials, the BOLD signal in the posterior putamen differentiated between responses compatible and incompatible with the cue-associated outcome. Furthermore, we identified a region in ventral amygdala showing relatively strong functional connectivity with posterior putamen during the cued trials. Structural MRI analyses provided converging evidence for the involvement of corticostriatal circuits: diffusion tensor imaging data revealed that connectivity of caudate-seeded white-matter tracts to the ventromedial prefrontal cortex predicted responding for still-valuable outcomes; and gray matter integrity in the premotor cortex predicted individual Pavlovian cueing effects.

Keywords: Pavlovian-instrumental transfer; corticostriatal circuits; diffusion tensor imaging; goal-directed behavior; habitual behavior; magnetic resonance imaging.