Structural Gray Matter Changes in the Hippocampus and the Primary Motor Cortex on An-Hour-to-One- Day Scale Can Predict Arm-Reaching Performance Improvement

Recent studies have revealed rapid (e.g., hours to days) training-induced cortical structural changes using magnetic resonance imaging (MRI). Currently, there is great interest in studying how such a rapid brain structural change affects behavioral improvement. Structural reorganization contributes to memory or enhanced information processing in the brain and may increase its capability of skill learning. If the gray matter (GM) is capable of such rapid structural reorganization upon training, the extent of volume increase may characterize the learning process. To shed light on this issue, we conducted a case series study of 5-day visuomotor learning using neuroanatomical imaging, and analyzed the effect of rapid brain structural change on motor performance improvement via regression analysis. Participants performed an upper-arm reaching task under left-right mirror-reversal for five consecutive days; T1-weighted MR imaging was performed before training, after the first and fifth days, and 1 week and 1 month after training. We detected increase in GM volume on the first day (i.e., a few hours after the first training session) in the primary motor cortex (M1), primary sensory cortex (S1), and in the hippocampal areas. Notably, regression analysis revealed that individual differences in such short-term increases were associated with the learning levels after 5 days of training. These results suggest that GM structural changes are not simply a footprint of previous motor learning but have some relationship with future motor learning. In conclusion, the present study provides new insight into the role of structural changes in causing functional changes during motor learning

Simultaneous processing of information on multiple errors in visuomotor learning.

The proper association between planned and executed movements is crucial for motor learning because the discrepancies between them drive such learning. Our study explored how this association was determined when a single action caused the movements of multiple visual objects. Participants reached toward a target by moving a cursor, which represented the right hand's position. Once every five to six normal trials, we interleaved either of two kinds of visual perturbation trials: rotation of the cursor by a certain amount (±15°, ±30°, and ±45°) around the starting position (single-cursor condition) or rotation of two cursors by different angles (+15° and -45°, 0° and 30°, etc.) that were presented simultaneously (double-cursor condition). We evaluated the aftereffects of each condition in the subsequent trial. The error sensitivity (ratio of the aftereffect to the imposed visual rotation) in the single-cursor trials decayed with the amount of rotation, indicating that the motor learning system relied to a greater extent on smaller errors. In the double-cursor trials, we obtained a coefficient that represented the degree to which each of the visual rotations contributed to the aftereffects based on the assumption that the observed aftereffects were a result of the weighted summation of the influences of the imposed visual rotations. The decaying pattern according to the amount of rotation was maintained in the coefficient of each imposed visual rotation in the double-cursor trials, but the value was reduced to approximately 40% of the corresponding error sensitivity in the single-cursor trials. We also found a further reduction of the coefficients when three distinct cursors were presented (e.g., -15°, 15°, and 30°). These results indicated that the motor learning system utilized multiple sources of visual error information simultaneously to correct subsequent movement and that a certain averaging mechanism might be at work in the utilization process

Results of the single-cursor trials in experiments 1 and 2.

<p>Both experiments are shown in the same panel, but the lines are disconnected between 10° and 15° because the data originated from different experiments. The data from −45° to −15° and 15° to 45° were adopted from experiment 1 and those from −10° to 10° were adopted from experiment 2. A: Aftereffects of the single-cursor trials for each rotation. The asterisks indicate significant directional shifts from baseline (**<i>P</i><0.01). B: The error sensitivity to the imposed rotations (<i>K_s</i>) decayed as the magnitude of rotation increased. The error bars indicate ±1 SE.</p

Averaged aftereffects of the double-cursor trials in experiments 1 (left) and 2 (right).

<p>The black circles in each panel indicate the aftereffects of the single-cursor trials for comparison. A, B: The aftereffects when two cursors were rotated in the same direction. The red and blue plots indicate the aftereffects of the double-cursor trials. An aftereffect is plotted at the center of two rotational angles (e.g., the aftereffect for the combination of −45° and 30° is plotted at 7.5° on the horizontal axis). C, D: The aftereffects when 1 cursor was not rotated. The open circles indicate the aftereffects of the double-cursor trials. The plot position corresponds to the rotated cursor (e.g., the aftereffect for the combination of 0° and 30° is plotted at 30° on the horizontal axis). E, F: The aftereffects when the cursors were rotated in the opposite directions. The green, red, and blue plots indicate the aftereffects of the double-cursors trials. An aftereffect is plotted at the center of 2 rotational angles. The asterisks indicate significant directional shifts from baseline (*<i>P</i><0.05; **<i>P</i><0.01). The statistical significance of the single-cursor trials is not shown. The error bars indicate ±1 SE.</p

Aftereffects of all the single- and double-cursor trials in experiment 1.

<p>The cell at the junction of the row labeled −15 and the column labeled 30 shows the aftereffect of a double-cursor trial when two cursors were rotated by −15° and 30°. The cell at the junction of the row labeled −45 and the column labeled −45 shows the aftereffect of a single-cursor trial when the cursor was rotated by −45°. The upper value of each cell indicates the mean and the value in parentheses indicates 1 SE. The asterisks indicate significant directional shifts from baseline (*<i>P</i><0.05; **<i>P</i><0.01).</p

Aftereffects of all of the single- and double-cursor trials in experiment 2.

<p>The format is the same as that in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0072741#pone-0072741-t001" target="_blank">Table 1</a>.</p

The aftereffects of experiment 3.

<p>The black bars indicate the aftereffects of the single-cursor trials of the labeled rotations, and the white bars indicate the aftereffects of the triple-cursor trials when the labeled rotations were simultaneously imposed. The data for 0° are not shown in the lower row because the average of the standardized baseline movement directions is always 0°. The asterisks indicate significant directional shifts from baseline [*<i>P</i><0.05; **<i>P</i><0.01; (*)<i>P</i><0.05 in one-tailed tests]. The error bars indicate ±1 SE.</p

Aftereffects of all the single- and triple-cursor trials in experiment 3.

<p>The combinations of the three rotation angles of the cursors are shown in the first three rows (the blank in the second and third row indicates the single-cursor trial). The upper value of each cell of the aftereffect indicates the mean and the number in parentheses indicates 1 SE. The asterisks indicate significant directional shifts from baseline (*<i>P</i><0.05; **<i>P</i><0.01).</p