Open-ended movements structure sensorimotor information in early human development

Abstract

Human behaviors, with whole-body coordination, involve large-scale sensorimotor interaction. Spontaneous bodily movements in the early developmental stage potentially lead toward acquisition of such coordinated behavior. These movements presumably contribute to the structuration of sensorimotor interaction, providing specific regularities in bidirectional information among muscle activities and proprioception. Whether and how spontaneous movements, despite being task-free, structure and organize sensorimotor interactions in the entire body during early development remain unknown. Herein, to address these issues, we gained insights into the structuration process of the sensorimotor interaction in neonates and 3-mo-old infants. By combining detailed motion capture and musculoskeletal simulation, sensorimotor information flows among muscle activities and proprioception throughout the body were obtained. Subsequently, we extracted spatial modules and temporal state in sensorimotor information flows. Our approach demonstrated that early spontaneous movements elicited body-dependent sensorimotor modules, revealing age-related changes in them, depending on the combination or direction. The sensorimotor interactions also displayed temporal non-random fluctuations analogous to those seen in spontaneous activities in the cerebral cortex and spinal cord. Furthermore, we found recurring state sequence patterns across multiple participants, characterized by a substantial increase in infants compared to the patterns in neonates. Therefore, early spontaneous movements induce the spatiotemporal structuration in sensorimotor interactions and subsequent developmental changes. These results implicated that early open-ended movements, emerging from a certain neural substrate, regulate the sensorimotor interactions through embodiment and contribute to subsequent coordinated behaviors. Our findings also provide a conceptual linkage between early spontaneous movements and spontaneous neuronal activity in terms of spatiotemporal characteristics.