Striatal and Pallidal Activation during Reward Modulated Movement Using a Translational Paradigm

Abstract

Objective Human neuroimaging studies of reward processing typically involve tasks that engage decision-making processes in the dorsal striatum or focus upon the ventral striatum's response to feedback expectancy. These studies are often compared to the animal literature; however, some animal studies include both feedback and nonfeedback events that activate the dorsal striatum during feedback expectancy. Differences in task parameters, movement complexity, and motoric effort to attain rewards may partly explain ventral and dorsal striatal response differences across species. We therefore used a target capture task during functional neuroimaging that was inspired by a study of single cell modulation in the internal globus pallidus during reward-cued, rotational arm movements in nonhuman primates. Methods In this functional magnetic resonance imaging study, participants used a fiberoptic joystick to make a rotational response to an instruction stimulus that indicated both a target location for a capture movement and whether or not the trial would end with feedback indicating either a small financial gain or a neutral outcome. Results Portions of the dorsal striatum and pallidum demonstrated greater neural activation to visual cues predicting potential gains relative to cues with no associated outcome. Furthermore, both striatal and pallidal regions displayed a greater response to financial gains relative to neutral outcomes. Conclusions This reward-dependent modulation of dorsal striatal and pallidal activation in a target-capture task is consistent with findings from reward studies in animals, supporting the use of motorically complex, tasks as translational paradigms to investigate the neural substrates of reward expectancy and outcome in humans.

Neural Mechanisms Underlying Time Perception and Reward Anticipation

“…Animal studies and human neuroimaging studies (including subjects with cocaine addiction) suggest that while ventral striatum neurons respond to reward processing, dorsal striatum activate during the timing and other cognitive processes like spatial learning ( van der Meer et al, 2010 ; Coull et al, 2011 ; Tau et al, 2014 ). On the other hand, it is also reported that the reward processing and reward based temporal learning activates both ventral and/or dorsal striatum ( Delgado et al, 2000 ; Bischoff-Grethe et al, 2015 ; Tomasi et al, 2015 ). It was proposed that differences in response requirements might explain the differential activation of ventral/dorsal striatum ( Bischoff-Grethe et al, 2015 ).…”

“…On the other hand, it is also reported that the reward processing and reward based temporal learning activates both ventral and/or dorsal striatum ( Delgado et al, 2000 ; Bischoff-Grethe et al, 2015 ; Tomasi et al, 2015 ). It was proposed that differences in response requirements might explain the differential activation of ventral/dorsal striatum ( Bischoff-Grethe et al, 2015 ).…”

Altered reward expectancy in individuals with recent methamphetamine dependence

“…Participants used a fiber optic joystick (Current Designs, Philadelphia, PA) to control a gray square cursor. A joystick, rather than a button press, was chosen because it engages greater movement control in terms of musculature, which may contribute to the dorsal striatal response during movements elicited by reward anticipation often reported in animal reward processing studies (Bischoff-Grethe et al, 2015; Hollerman et al, 1998; Kawagoe et al, 1998). Three square targets were presented on a black background.…”

The human subthalamic nucleus and globus pallidus internus differentially encode reward during action control

“…Local field potential recordings from the GPi in humans showed correlation between pallidal LFP amplitude and reward expectation [Schroll et al, ]. Finally, functional neuroimaging has shown greater neural activation in the human pallidum in response to rewards as compared to response to neutral stimuli [Bischoff‐Grethe et al, ].…”