Brain changes following four weeks of unimanual motor training: Evidence from behavior, neural stimulation, cortical thickness, and functional MRI

Abstract

Although different aspects of neuroplasticity can be quantified with behavioral probes, brain stimulation, and brain imaging assessments, no study to date has combined all these approaches into one comprehensive assessment of brain plasticity. Here, 24 healthy right-handed participants practiced a sequence of finger-thumb opposition movements for 10 min each day with their left hand. After 4 weeks, performance for the practiced sequence improved significantly (P < 0.05 FWE) relative to a matched control sequence, with both the left (mean increase: 53.0% practiced, 6.5% control) and right (21.0%; 15.8%) hands. Training also induced significant (cluster p-FWE < 0.001) reductions in functional MRI activation for execution of the trained sequence, relative to the control sequence. These changes were observed as clusters in the premotor and supplementary motor cortices (right hemisphere, 301 voxel cluster; left hemisphere 700 voxel cluster), and sensorimotor cortices and superior parietal lobules (right hemisphere 864 voxel cluster; left hemisphere, 1947 voxel cluster). Transcranial magnetic stimulation over the right ("trained") primary motor cortex yielded a 58.6% mean increase in a measure of motor evoked potential amplitude, as recorded at the left abductor pollicis brevis muscle. Cortical thickness analyses based on structural MRI suggested changes in the right precentral gyrus, right post central gyrus, right dorsolateral prefrontal cortex, and potentially the right supplementary motor area. Such findings are consistent with LTP-like neuroplastic changes in areas that were already responsible for finger sequence execution, rather than improved recruitment of previously nonutilized tissue. Hum Brain Mapp 38:4773-4787, 2017. © 2017 Wiley Periodicals, Inc.

Brain changes following four weeks of unimanual motor training: Evidence from fMRI‐guided diffusion MRI tractography

“…Second, we controlled for variable diffusion tensor fitting by demonstrating a lack of change in corticospinal tracts in the untrained hemisphere, and replicating results using an alternative tensor‐fitting algorithm. Finally, and critically, the changes reported were consistent with changes in TMS measures, and backed by increases in skill performance, cortical thickness changes, and altered fMRI activation in the sensorimotor cortex and superior parietal lobule [Sale et al, ].…”

“…Previously, we reported cortical thickness changes in the right (trained) dlPFC in the region of Brodmann's area 9 [Sale et al, ]. Top‐down control of motor output, for error‐correction, is predominantly associated with activation of the dlPFC, as well as the caudate nucleus [Chevrier et al, ; Kübler et al, ].…”

“…Top‐down control of motor output, for error‐correction, is predominantly associated with activation of the dlPFC, as well as the caudate nucleus [Chevrier et al, ; Kübler et al, ]. The dlPFC is thought to connect strongly with premotor areas, including the supplementary motor area (SMA; [Lu et al, ])—a region which displayed changes in fMRI, cortical thickness, and TMS measures after training in the present cohort [Sale et al, ]. For these reasons, we measured FA in connections between the middle frontal lobe and SMA, and the middle frontal lobe and caudate nucleus, with diffusion tractography.…”

“…Furthermore, the present results yielded relatively clear‐cut biological interpretations, and we believe generate a number of testable predictions for future work. This is due in part to concurrent changes that were detected in a number of independent measures, including TMS‐induced motor‐evoked potentials [Sale et al, ]. We also performed a series of subanalyses to confirm results were not a reflection of participant selection, tensor fitting algorithms, voxel exclusion criteria, tractography seeding biases, or variable region‐of‐interest placement.…”

Response Hand and Motor Set Differentially Modulate the Connectivity of Brain Pathways During Simple Uni-manual Motor Behavior

“…The thalamus in addition to its role as an attention relay (Saalmann & Kastner, 2011), helps regulate and coordinate activity across motor regions (Ahissar & Oram, 2013), suggesting that the M1 ←→ thalamus sub-network is an important motor-attention functional loop. Both the SMA and the parietal cortex have been implicated in command-related signaling of basic hand movements (Rathelot, Dum, & Strick, 2017), and their responses (Sale et al, 2017) and inter-regional interactions are known to underpin motor learning. As Figure 4 and Figure X demonstrates, the combination of responding with the dominant effector while establishing a motor set (periodic condition) induces greater uFC and dFC in these sub-networks, implying that the condition evokes representations of handedness.…”