Directed Neural Network Dynamics in Sensorimotor Integration: Divergent Roles of Frontal Theta Band Activity Depending on Age.

Abstract

Sensorimotor integration processes are crucial for daily-life activities, such as grasping objects or driving a car. Theta band activity (TBA) in distributed brain networks is likely essential to perform sensorimotor integration successfully. Directed communication in these brain networks is shaped by brain maturation during adolescence. This study investigates how age-related effects attributable to brain maturation influence directed communication in a theta-associated sensorimotor integration network. We conducted an EEG study with a continuous pursuit-tracking task performed by an adult group (n = 41) and an adolescent group (n = 30), each including both sexes. Both groups show elevated theta-band activity during higher sensorimotor demands. Yet, the adult group outperformed the adolescent group, particularly during higher demands. Further analyses revealed that this is likely due to enhanced directed connectivity between frontal areas and the ventral processing stream in adults, which likely enables effective integration of visual and motor information. Adolescents rely on frontal TBA signaling surprise and prediction error, with no input from ventral stream areas. This might cause lower performance during higher demands. Across age, TBA appears to serve distinct functions during sensorimotor integration. Age-related processes transform the neural processes underlying complex sensorimotor integration.Significance Statement This study shows how brain development affects tasks like grasping or driving, where vision and movement must work together. The results suggest that adults who performed better in sensorimotor integration yield a stronger information transfer between brain regions that integrate visual and motor information, while adolescents lack an input from such areas. This difference in brain communication could explain why adolescents struggle with more complex tasks, highlighting how brain maturation improves sensorimotor integration.