Functionally Specific Changes in Resting-State Sensorimotor Networks after Motor Learning

Abstract

Motor learning changes the activity of cortical motor and subcortical areas of the brain, but does learning affect sensory systems as well? We examined in humans the effects of motor learning using fMRI measures of functional connectivity under resting conditions, and found persistent changes in networks involving both motor and somatosensory areas of the brain. We developed a technique that allows us to distinguish changes in functional connectivity that can be attributed to motor learning from those that are related to perceptual changes that occur in conjunction with learning. Using this technique, we identified a new network in motor learning involving second somatosensory cortex, ventral premotor cortex and supplementary motor cortex whose activation is specifically related to perceptual changes that occur in conjunction with motor learning. We also found changes in a network comprising cerebellar cortex, primary motor and dorsal premotor cortex that were linked to the motor aspects of learning. In each network, we observed highly reliable linear relationships between neuroplastic changes and behavioral measures of either motor learning or perceptual function. Motor learning thus results in functionally specific changes to distinct resting-state networks in the brain.

Sensorimotor adaptation changes the neural coding of somatosensory stimuli

“…Thus, in effect, the functional role of the observed sensory change is that, in combination with motor learning, the two act together to keep motor and sensory systems in register. The present findings complement the results of recent studies in which we have used fMRI under resting-state conditions to assess changes that occur in association with motor learning in the functional connectivity between the brain's sensory and motor regions (Vahdat et al 2011). In that work, it was observed that changes in brain networks that occur in conjunction with learning can be partitioned into those that are primarily motor in nature and those that reflect the perceptual changes that occur in combination with motor learning.…”

“…The SEP changes observed in the present study follow the same pattern as psychophysical measures of perceptual change (Ostry et al 2010, Vahdat et al 2011. Both SEP magnitudes and measures of sensed limb position vary with the extent of learning, and neither is observed to change in the context of passive movement that does not involve learning.…”

“…Bernier et al (2009) report that an SEP reduction occurs early in visuomotor learning, but it dissipates quickly, such that SEPs are back to baseline levels well before the end of the training. A further reason for thinking that the effects that we have seen here are not simply the persistence of a sensory suppression mechanism is that sensory suppression is typically associated with a reduction in acuity, rather than shifts in perceptual boundaries that are observed in conjunction with motor learning (Cressman and Henriques 2009; Haith et al 2008;Ostry et al 2010;Vahdat et al 2011). Cortical motor areas are densely interconnected with somatosensory cortex.…”

“…While this remains a possibility for the data presented here, other observations suggest that the present results are substantially cortical in nature. In particular, changes in somatosensory perceptual function are observed in the context of identical motor learning paradigms that do not involve reflex elicitation (Cressman and Henriques 2009;Haith et al 2008;Vahdat et al 2011). Moreover, there are changes in resting-state cortical somatosensory networks following motor learning under conditions where there is no experimental task at all (Vahdat et al 2011).…”

“…A change in somatosensory function in association with motor learning would seem to be a natural by-product of this anatomical connectivity. However, apart from behavioral studies (Cressman and Henriques 2009;Haith et al 2008;Ostry et al 2010;Wong et al 2011) and a recent analysis of changes to resting-state networks in association with motor learning (Vahdat et al 2011), there is little direct evidence that motor learning produces changes in sensory systems. Here we show that motor learning indeed alters the response of somatosensory areas of the brain.…”