Emotion for Motion: Characterizing the Open-Loop Pathway for Affect-Driven Motor Responding
Emotions can be a powerful moving force, often with physiological and behavioral consequences. Facilitatory effects of emotion-induced action tendencies are evident in paradoxical kinesia (PK), a condition wherein individuals with Parkinson’s Disease are able to move fluidly under surprising or emotionally arousing circumstances. PK often occurs in response to salient experiences, suggesting a modulatory role of saliency-encoding subcortical regions (amygdala, ventral striatum, and ventral putamen) on primary motor function, which form the little-understood ‘open-loop’ pathway. Here, we employed a threat-of-shock paradigm in the MRI scanner to (a) test whether emotional arousal facilitates movement via the open-loop pathway; and (b) characterize amygdala-connected prefrontal (PFC) involvement in tracking emotional arousal experienced during goal-relevant threat.
Goal-relevant anticipatory threat was induced via a countdown procedure to shock administration, which could be avoided via time-sensitive motor action. Shock intensity and controllability were orthogonally manipulated: in ‘controllable’ trials, participants made a motor response to avoid ‘mild’ or ‘unpleasant’ shocks; in ‘uncontrollable’ trials, a shock was always received. First, we examined open-loop circuitry involvement during threat-motivated escape. Goal-relevant threat induced changes in emotional arousal and motor action: self-reported emotional arousal was highest in controllable-unpleasant trials, which also produced the highest motor performance accuracy . Suggesting open-loop involvement, basolateral amygdala activation was greater in controllable-unpleasant (vs. uncontrollable-unpleasant) trials. Given recent work suggesting that the frontopolar cortex integrates amygdala-originated signals and goal-relevant information for the control of motivated behavior, we examined whether changes in subjectively-experienced emotional arousal during threat anticipation were tracked in PFC. A parametric modulation model indicated that the frontopolar cortex tracked trial-wise changes in subjectively-experienced arousal during threat anticipation activation across all conditions. Our results unveil robust facilitatory effects of emotion on motor action, which rely in part on the ‘open-loop’ circuitry. These results also indicate that changes in subjectively experienced arousal during goal-relevant threat are tracked by amygdala-interconnected frontopolar cortex.