On the neuronal processing of movement dynamics

Abstract

The thesis collects five essays on how neurons in four motor areas of the frontal lobe process the movement dynamics. In the experiments described, monkeys executed visually instructed reaching movements while holding the handle of a robotic arm. Motors attached to the robot allowed turning on and off perturbing forces that deviated the hand of the monkeys. After some exposure, the monkeys adapted to the perturbation. The experiments were designed to dissociate the activity related to the desired kinematics from that related to the dynamics. Furthermore, the experiments dissociated the activity related to motor performance (desired kinematics and dynamics) from that related to motor learning (learning a new dynamics). The thesis describes the following results. 1. During motor execution, the movement dynamics is processed across multiple areas. Specifically, dynamics-related activity is found in all areas projecting to the spinal cord under study, namely the primary motor cortex (M1), supplementary motor area (SMA), dorsal premotor (PMd), and ventral premotor area (PMv). 2. Dynamics-related activity is also present during motor planning in both PMd and SMA, but not in M1 and PMv. This suggests that the dynamics is processed "upstream" of M1. The activity of SMA reflects during motor planning a kinematics-to-dynamics transformation. Neuronal correlates of that transformation are observed both at the level of the population and for single cells. 3. Extensive neuronal plasticity is observed in these areas when monkeys learn a new dynamics. The activity of single neurons modifies as monkeys adapt to the force, and changes outlast the exposure to the perturbation.

(cont.) With respect to M1, comparison of the movement-related activity recorded prior to, during, and after exposure to the perturbing force reveals a double level of neuronal coding. As a population, neurons in M1 display changes that mirror the changes observed in the EMG of muscles. In a statistical sense, the population activity of M1 after re-adaptation is not distinguishable from that before exposure to the force. Thus, the population activity of M1 reflects motor performance. However, single neurons maintain -after re-adaptation -trace of the adaptation experience. Thus, the activity of M1 neurons also reflects motor learning.