When anticipation is not enough: a mixture of robust and adaptive feedback control strategies improve reaching in dynamic environments

Abstract

Successful goal-directed movements depend on the central nervous systems (CNS) ability to handle diverse physical interactions. The CNS is thought to handle different dynamical contexts through three mechanisms: (i) trial-by-trial adaptation when forces are predictable, (ii) a model-free robust control strategy, and (iii) online adaptation of feedback responses. While each has been studied independently, their relative contributions and the possibility that they are recruited to different extents across contexts is unknown. Here, we quantified all three strategies within the same individuals to examine how CNS exploits them under varying environmental conditions. Participants (19 female, 15 male) performed reaching tasks while interacting with robot-generated force-fields that were either consistent or varied unpredictably. Trial-by-trial adaptation was measured using standard force channels to isolate anticipatory compensation. Robust control was assessed through movement velocity and corrective force magnitude. Online adaptive control was quantified by the temporal alignment between commanded and measured forces within a movement. Results showed that participants improved anticipatory compensation in consistent environments and relied on both robust and online adaptation when perturbations were unpredictable. Crucially, markers of robust control dominated the early movement phase, whereas online adaptation dominated later corrections. This temporal dissociation was confirmed by electromyographic recordings. Markers of robust and online adaptive feedback strategies also statistically predicted participants ability to adapt across trials in consistent environments, revealing a common trait linking online control and adaptation. These findings reveal a rich and flexible combination of control mechanisms, offering a new framework for understanding the neurophysiological bases of reaching control. Significance StatementHuman reaching control is a complex behavior resulting from several mechanisms that orchestrate feedback responses to mechanical perturbations and adaptation to changes in the environment. Here we combine previously studied paradigms to highlight within the same groups of healthy volunteers that three major components are recruited to different extents dependent on the context: unpredictable environment promote concomitant use of robust control and online adaptation whereas predictable environments recruit standard adaptation based on anticipatory compensation. Remarkably, individuals adaptive capabilities correlated across consistent and inconsistent environments, suggesting a key involvement of adaptive mechanisms in both online control and trial-by-trial adaptation. Robust control, online adaptation, and anticipatory compensation are dissociable behaviorally, and are used to varying levels as a result of individual traits.