Changes in visual and sensory-motor resting-state functional connectivity support motor learning by observing

Abstract

Motor learning occurs not only through direct first-hand experience but also through observation (Mattar AA, Gribble PL. Neuron 46: 153-160, 2005). When observing the actions of others, we activate many of the same brain regions involved in performing those actions ourselves (Malfait N, Valyear KF, Culham JC, Anton JL, Brown LE, Gribble PL. J Cogn Neurosci 22: 1493-1503, 2010). Links between neural systems for vision and action have been reported in neurophysiological (Strafella AP, Paus T. Neuroreport 11: 2289-2292, 2000; Watkins KE, Strafella AP, Paus T. Neuropsychologia 41: 989-994, 2003), brain imaging (Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ, Zilles K, Rizzolatti G, Freund HJ. Eur J Neurosci 13: 400-404, 2001; Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. Science 286: 2526-2528, 1999), and eye tracking (Flanagan JR, Johansson RS. Nature 424: 769-771, 2003) studies. Here we used a force field learning paradigm coupled with resting-state fMRI to investigate the brain areas involved in motor learning by observing. We examined changes in resting-state functional connectivity (FC) after an observational learning task and found a network consisting of V5/MT, cerebellum, and primary motor and somatosensory cortices in which changes in FC were correlated with the amount of motor learning achieved through observation, as assessed behaviorally after resting-state fMRI scans. The observed FC changes in this network are not due to visual attention to motion or observation of movement errors but rather are specifically linked to motor learning. These results support the idea that brain networks linking action observation and motor control also facilitate motor learning.

Functional Plasticity in Somatosensory Cortex Supports Motor Learning by Observing

“…If motor learning by observing involves similar neural circuitry as active motor learning, we should also see somatosensory functional plasticity and behavioral changes with observation. While previous work has shown that observing FF learning involves concurrent changes in sensory-motor resting-state functional connectivity [7] and sensed limb position [8], these studies did not directly test the role of the somatosensory system.…”

“…The videos have been described in detail elsewhere [7]. Briefly, the videos showed a top-down view of a tutor performing the reaching task using the right arm.…”

Functional Connectivity Between Somatosensory and Motor Brain Areas Predicts Individual Differences in Motor Learning by Observing

“…Using this same dataset, we have previously examined changes in resting-state FC from pre-observation (day 1 scan) to post-observation (day 2 scan). See McGregor and Gribble (2015) for details of FC changes from day 1 to day 2, and how they relate to observation-related gains in motor learning.…”

“…Here we tested the hypothesis that individual differences in brain function or structure can predict the extent to which individuals will learn to perform a novel sensory-motor task (FF reaching) from observation. Based on our previous work (McGregor and Gribble, 2015;McGregor et al, 2016), we expected that individual differences in brain function and structure within visual and sensory-motor brain networks would be predictive of motor learning by observing. On day 1, subjects performed baseline (no FF) reaches using a robotic arm and then underwent preobservation anatomical and resting-state functional magnetic resonance imaging (fMRI) scans.…”

Somatosensory Perceptual Training Enhances Motor Learning by Observing

“…McGregor and Gribble, 2015). We assessed changes in resting-state functional connectivity 470 from pre-to post-observation that were related to behavioral measures of motor learning by 471 observing.…”