Reciprocal Fronto-Parietal Interactions Support Motor Anticipation during Sequential Reaching

Abstract

Motor planning is a highly flexible process that adapts to changing behavioral demands. Frontal and parietal circuits are considered as critical nodes that support planning processes. However, it remains unclear whether the coordination of motor and parietal areas is preserved or adjusted in response to varying behavioral contexts. To address this open question, we trained two rhesus macaques to perform a visually-guided sequential reaching task, in which they could adapt their behavior to varying degrees of target predictability within the sequence. Analysis of eye and hand movements revealed distinct visuomotor strategies that were reflected in corresponding neural activity patterns. During motor anticipation, the direction of the upcoming reach toward predictable targets could be decoded from preparatory neural activity prior to target onset both in motor regions (PMd/M1) and parietal area 7A, whereas during reactive movements directional information emerged only after target onset. Using feature-specific information transfer analysis, we found that information about the upcoming movement direction was transmitted between 7A and PMd/M1 through bidirectional interactions. This pattern of interactions was preserved during motor anticipation and shifted earlier in time with respect to target onset. Our findings thus support a reciprocal fronto-parietal network that flexibly adjusts the timing of preparatory activity as different strategies are employed under varying behavioral constraints. Contrary to classical hierarchical models predicting serial activation across parietal and motor areas, parietal-to-motor interactions did not precede motor-to-parietal interactions, consistent with a heterarchical organization of cortical processing during flexible motor planning.