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

Abstract

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. 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. 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. 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.

Keywords: Functional magnetic resonance imaging; Pallidum; Reward; Skeletomotor; Striatum; Translational.

Figure 1

Examples of the two behavioral trial types. A) For the Feedback Cue, the white stimulus predicting future feedback is presented; upon extinguishing, the participant uses the fiberoptic joystick to move to the previously lit target's position and holds during the delay period. Feedback is provided with either a green filled target, indicating the participant earned 20 cents for the trial, or a yellow target, indicating the participant did not earn any money for this trial. B) For the Nonfeedback Cue, the gray stimulus indicating no feedback for this trial is presented; upon extinguishing, the participant uses the joystick to move to the target's location. C) The timeline for a typical trial.

Figure 1

Examples of the two behavioral trial types. A) For the Feedback Cue, the white stimulus predicting future feedback is presented; upon extinguishing, the participant uses the fiberoptic joystick to move to the previously lit target's position and holds during the delay period. Feedback is provided with either a green filled target, indicating the participant earned 20 cents for the trial, or a yellow target, indicating the participant did not earn any money for this trial. B) For the Nonfeedback Cue, the gray stimulus indicating no feedback for this trial is presented; upon extinguishing, the participant uses the joystick to move to the target's location. C) The timeline for a typical trial.

Figure 2

A) Response time in relation to Cue stimuli (Feedback Cue, Nonfeedback Cue) across 8 runs. Overall, response initiation was slower for the Nonfeedback Cues relative to the Feedback Cues. B) Movement duration in relation to Cue stimuli (Feedback Cue, Nonfeedback Cue) across 8 runs. Participants exhibited longer movement durations for the Nonfeedback Cues relative to the Feedback Cues. Error bars indicate standard errors.

Figure 3

Differences in response to Feedback and Nonfeedback Cues. A) Upper panel: The contrast of Feedback Cues > Nonfeedback Cues revealed effects within several a priori predicted regions, including the medial caudate. Lower panel: The contrast of Nonfeedback Cues > Feedback Cues revealed differences within the posterior putamen and posterior pallidum. B) Average percent signal change extracted from a priori selected regions of interest for Feedback Cues and Nonfeedback Cues. Anterior subregions (medial caudate) tended to be more responsive to Feedback Cues, whereas posterior subregions (putamen) were more responsive to Nonfeedback Cues. Error bars indicate standard errors.

Figure 4

Differences in response to Positive Outcomes and Neutral Outcomes. A) The contrast of Positive Outcomes > Neutral Outcomes revealed effects within several a priori predicted regions, including medial caudate. B) Average percent signal change extracted from a priori selected regions of interest for Positive Outcomes and Neutral Outcomes. Overall, regions of interest were more responsive for Positive Outcomes than for Neutral Outcomes. Error bars indicate standard errors.