Sensorimotor adaptation changes the neural coding of somatosensory stimuli

Abstract

Motor learning is reflected in changes to the brain's functional organization as a result of experience. We show here that these changes are not limited to motor areas of the brain and indeed that motor learning also changes sensory systems. We test for plasticity in sensory systems using somatosensory evoked potentials (SEPs). A robotic device is used to elicit somatosensory inputs by displacing the arm in the direction of applied force during learning. We observe that following learning there are short latency changes to the response in somatosensory areas of the brain that are reliably correlated with the magnitude of motor learning: subjects who learn more show greater changes in SEP magnitude. The effects we observe are tied to motor learning. When the limb is displaced passively, such that subjects experience similar movements but without experiencing learning, no changes in the evoked response are observed. Sensorimotor adaptation thus alters the neural coding of somatosensory stimuli.

Fig. 1.

Experimental setup to study motor learning. A: subjects moved the handle of a robot arm to a single visual target. Vision of the arm was occluded. In the force-field condition, the robot applied forces to the handle that varied with movement velocity. B: scalp map showing EEG electrode locations.

Fig. 2.

Behavioral results for the force-field learning group and the passive control condition. A: experimental sequence. Somatosensory evoked potentials (SEPs) were obtained before and after training (gray vertical bars). All subjects produced active movements in baseline trials (gray and black). The main experimental manipulation involved a force-field training sequence (red). Learning was assessed using the mean perpendicular deviation (PD) of the hand from a line joining movement start and end points. A group of control subjects was tested in a passive condition (cyan) in which subjects held the handle of the robot arm while the robot reproduced the entire series of movements of subjects in the force-field training condition. B: mean hand paths for the force-field training (left) and passive-movement (right) conditions. C: SEPs were elicited as subjects held the handle of the robot arm. The limb was perturbed laterally using a sequence of servo-position controlled displacements (upper panel). The lower panel shows that subject applied forces sensed at the robot handle were closely matched to the commanded forces that displaced the arm.

Fig. 3.

Motor learning changes sensory evoked responses at electrode locations above contralateral somatosensory cortex. A and B: mean somatosensory evoked responses (SEPs) at electrode location C3 before and after training for force-field learning (A) and passive movement (B). Changes to the first peak are observed following force-field learning, but not under passive movement conditions. C: Z-scores for the first positive peak of the SEP averaged over subjects decrease reliably following force-field learning, but not after passive movement. D–F: SEP changes with learning at electrode location CP3 are similar to those in the upper panel.

Fig. 4.

Topographic probability maps showing electrode locations at which evoked responses change reliably following training. Activation differences following learning (given as t values, thresholded at P < 0.01) are shown at times associated with the first positive and later negative peaks of the SEP. A: force-field learning results in reliable changes in activation at the first peak of the SEP at electrode locations over contralateral somatosensory cortical areas (upper panel). There are no changes in the passive movement condition (lower panel). B: force-field learning also results in changes in activation at the second peak of the SEP at bilateral electrode locations over premotor areas (upper panel). Passive training leads to changes in activation over posterior parietal cortex (lower panel). C: subjects that learned more showed a greater reduction in SEP magnitude.

Fig. 5.

Scalp topographic maps averaged over subjects at the first positive peak of the somatosensory evoked response. A: scalp voltage distribution before motor learning. B: voltage distribution after learning.