Incentive valence differentially engages open- and closed-loop basal ganglia circuits during movement initiation

Abstract

Incentives modulate voluntary movement, yet the circuitry channeling these signals into motor output remains unclear. Classical models emphasize a closed-loop circuit (CLC) linking dorsal putamen (PUTd) with motor cortex, but this pathway is anatomically segregated from affective processing regions. Anatomical and clinical evidence point to an alternative: an open-loop circuit (OLC) from ventral putamen (PUTv) that may route affective signals to motor cortex. Here, we conducted two experiments to test whether a functional OLC exists in humans and whether it is differentially engaged by incentive conditions. First, in 7 T resting-state fMRI (multi-echo), PUTv showed robust functional connectivity with both affective and motor regions, including the cingulate motor area (CMA), even after accounting for PUTd variance. This connectivity pattern supports the plausibility of an independent pathway linking affective basal ganglia regions to the motor cortex. Second, in 3 T task fMRI (incentivized reaching), jackpot (high-reward) and robber (high-loss avoidance) incentive conditions produced distinct behavioral and neural signatures. Jackpot produced a speed-accuracy trade-off, with faster movement initiation but more false starts. Neurally, this coincided with engagement (BOLD responses relevant for initiation speed) being reduced in CLC nodes but not in OLC. Robber, in contrast, eliminated engagement in both OLC and CLC nodes, instead recruiting stopping-related regions (e.g., STN), consistent with an avoidance phenomenology. Together, these findings support a versatile architecture for movement initiation that flexibly engages distinct cortico-subcortical circuits depending on incentive phenomenology, and offer a candidate mechanism through which affective salience and valence modulate voluntary movement. Significance StatementAffective signals profoundly influence movement, yet the mechanisms linking motivationally relevant contexts with motor behavior remain unclear. Combining ultra-high field (7 T) connectomics with task-based (3 T) neuroimaging, we provide the first systems-level evidence in humans for such a mechanism: a ventral putamen-centered open-loop circuit (OLC) connecting affective and motor areas, operating alongside the canonical dorsal putamen-centered closed-loop sensorimotor circuit (CLC). Critically, the phenomenological quality of incentive (how it is construed as reward versus threat) rather than magnitude alone, likely determines which circuit dominates during movement initiation. These findings help to explain paradoxical kinesia in Parkinsons disease, where affective contexts can bypass degraded sensorimotor circuits, and establish foundations for context-based therapeutic interventions.