Reach plans for grasping vs. placing objects evoke different neural dynamics within a shared cortico-cerebellar mechanism

Abstract

Many reach studies treat grasping as the endpoint of a reach, but grasping often initiates a sequence of actions, ending with placing the object. Grasping and placing both require object-specific encoding, but placing has different computational demands, introduced by the intent, sensory feedback, and tolerance for spatial error when alignment is required. Recent neuroimaging work suggests that object placement shares similar cortico-cerebellar networks with grasp, with modest increases in network segregation and cerebellar activity. Here, we ask whether Grasp and Place are better distinguished by their spatiotemporal dynamics in both behaviour and scalp-recorded EEG activity. Using high-density EEG and motion tracking, 31 participants performed alternating Grasp/Place movements of a 3D object from/toward an oriented target/template. Place movements were initiated faster but executed more slowly and with greater endpoint-orientation precision than Grasp, indicating distinct control strategies. ERP and microstate analyses revealed that Grasp and Place shared a peri-movement polarity switch, from posterior negativity/frontal positivity during preparation to posterior positivity/frontal negativity during execution. This shared pattern was amplified during Place preparation and prolonged during Place execution, with stronger expression of preparatory medial frontal/cerebellar and execution-related posterior/cerebellar microstate dynamics. Finally, SVM decoding indicated that task-specific information was primarily encoded in low-frequency EEG activity (below 6 Hz). These results confirm that grasping and placing recruit similar cortico-cerebellar mechanisms, yet different spatiotemporal dynamics are employed to support the distinct computational demands of these behaviours. Significance Statement Grasping is often considered the endpoint of reaching, but in normal behavior, grasping is usually the first step in a sequence of object manipulations that ends with placing the object. Here, we used motion tracking and electroencephalography to directly compare spatially matched Grasp and Place movements and their cortical dynamics. We found that Place and Grasp utilize different control principles that are reflected in the EEG signals: a shared fronto-parietal polarity switch with differing strengths and timing. Microstate and source localization analysis further traced this to different temporal recruitment patterns of cortico-cerebellar clusters, primarily coded in low-frequency activity. These findings provide important insights into how the brain can adjust the spatiotemporal dynamics of similar networks to produce different motor behaviors.