The resting human brain and motor learning

Abstract

Functionally related brain networks are engaged even in the absence of an overt behavior. The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see [1] for review, [2-4]) or electrical [5, 6] signals, is unclear. Two major proposals are that resting state activity supports introspective thought or supports responses to future events [7]. An alternative perspective is that the resting brain actively and selectively processes previous experiences [8]. Here we show that motor learning can modulate subsequent activity within resting networks. BOLD signal was recorded during rest periods before and after an 11 min visuomotor training session. Motor learning but not motor performance modulated a fronto-parietal resting state network (RSN). Along with the fronto-parietal network, a cerebellar network not previously reported as an RSN was also specifically altered by learning. Both of these networks are engaged during learning of similar visuomotor tasks [9-22]. Thus, we provide the first description of the modulation of specific RSNs by prior learning--but not by prior performance--revealing a novel connection between the neuroplastic mechanisms of learning and resting state activity. Our approach may provide a powerful tool for exploration of the systems involved in memory consolidation.

Figure 1

Experimental Design and Performance during the Visuomotor Task (A) The experiment began with a dummy task and a baseline rest condition (REST₁, 11 min) followed by the visuomotor task (11 min). Then participants completed a second dummy task before the final rest condition (REST₂, 11 min). The dummy task display was of point light displays of human whole-body movements, or scrambled versions that showed the same individual dot motions, but with random positions. The visuomotor task display shows the central start location, a target and the cursor. (B) In the visuomotor task the relative angle of the cursor motion compared to the joystick gradually increased with each block, for the test group (dashed group), but remained veridical for the control group. The mean direction of joystick movement with respect to the target (solid line, ±1 SEM) steadily increased for the test group (black) and remained constant for the control group (gray).

Figure 2

A Fronto-Parietal Resting State Network that Increased in Strength after Exposure to the Visuomotor Adaptation, but Not Performance This independent component was identified as reliable across the participants in each group and across both rest blocks. The fronto-parietal network (A, C) closely corresponds to a previously identified RSN . The strength of the fronto-parietal network during rest was increased after motor learning (B), but not after motor performance (D).

Figure 3

Resting State Activity within the Cerebellum Increased in Strength after Exposure to the Visuomotor Adaptation Task This independent component (A) was reliably identified across the combined data for both rest sessions in the test group across, and significantly differed between the two rests (B). The absence of this network in previous reports on resting state networks and its absence in the control group suggests that activation of this network may have been driven by the motor learning experience.