Separating Visual and Motor Components of Motor Cortex Activation for Multiple Reach Targets: A Visuomotor Adaptation Study

Ethologically inspired models of movement preparation view the sensorimotor system as sampling information from the environment in a parallel fashion in preparation for multiple potential actions. In support, the configuration of the physical workspace, manipulated by the number or spatial separation of potential targets, has been shown to modulate sensorimotor neural activity. It is unclear, however, whether this modulation is driven by the sensory layout of the workspace or through the associated motor plans. Here, we combine a delayed-movement pre-cuing task with visuomotor adaptation to address this question in human subjects while recording MEG. By dissociating visual and motor coordinates of two targets using visuomotor adaptation, the task was designed to evaluate, in a selective fashion, the effects of visual and movement target separation on movement preparatory activity. The results did not allow the intended comparison due to an unanticipated effect of the direction of visuomotor adaptation on baseline oscillatory power in beta and low-gamma bands. Fortuitously, this effect was dependent on whether the adaptation direction decreased or increased the angular separation between alternative movements. That is, there was a sustained reduction of oscillatory power, which was stronger at small compared with large target separation. These results support a direct influence of movement target separation on motor cortex neural activity, mediated by lateral interactions between simultaneously active motor plans. The results further demonstrate a novel effect of visuomotor adaptation on motor cortex oscillatory activity, with properties that support the local nature of learned changes in visuomotor mapping.

Significance statement: There is growing evidence that the motor cortex routinely prepares for different movements simultaneously, each suited to a possible course of events in the immediate environment. The preparatory motor cortex activity for different movements can be seen as a competition between groups of neurons. This competition is influenced by how similar the alternative movements are; for example, in terms of direction, determined by the proximity of alternative movement goals. This study investigates whether the proximity of alternative reach goals has a direct influence on motor cortex activity (in the form of brain oscillations) or if it has an effect only through conscious evaluation of the separation between targets. We establish that there is a direct effect, supporting the biased competition model of action selection.