A modular architecture for trial-by-trial learning of redundant muscle activity patterns in novel sensorimotor tasks

Abstract

The coordination of the multiple degrees-of-freedom of the human body may be simplified by muscle synergies, motor modules which can be flexibly combined to achieve various goals. Studies investigating adaptation to novel relationships between muscle activity and task outcomes found that altering the recruitment of such modules is faster than the learning of their structures de novo. However, how learning new synergy recruitments or new synergy structures may occur remains unclear. While trial-by-trial learning of novel sensorimotor tasks has been successfully modeled at the level of task variables, few models accounted for the redundancy of the motor system, particularly at the muscular level. However, these models either did not consider a modular architecture of the motor system, or assumed a priori knowledge of the sensorimotor task. Here, we present a computational model for the generation of redundant muscle activity where explicitly defined modules, implemented as spatial muscle synergies, can be updated together with their recruitment coefficients through an error-based learning process dependent on a forward model of the sensorimotor task, which is not assumed to be known a priori. Our model can qualitatively reproduce the experimental observations of slower learning and larger changes in the structure of the muscle activity under sensorimotor tasks that require the learning of novel patterns of muscle activity, providing further insights into the modular organization of the human motor system. Author summaryIt has been proposed that muscles are recruited in modules, called muscle synergies, rather than on a muscle-by-muscle basis. This modular organization was shown to affect the learning of novel tasks, where simulated remapping of the forces generated by the muscles ("virtual surgeries") that make the synergies ineffective are more difficult to learn. Previous models of trial-by-trial learning in a modular architecture have assumed prior knowledge of the motor task (in particular, how to modify the muscles / synergies recruitment given an error), which might not be the case for tasks in which novel patterns of muscle activity are required. In contrast, models which assumed no prior knowledge of the task have not investigated the role of modularity. Here, we propose a computational model of the trial-by-trial adaptation of muscle synergies, their recruitment, and the concurrent learning of the internal model of the musculoskeletal system responsible for error correction. Our results show that this model replicates experimental observations of slower learning and larger changes in the structure of the muscle activity in sensorimotor tasks that require the learning of novel patterns of muscle activity, providing insight into learning-related changes of muscle activity in novel sensorimotor tasks.