Implicit sequence-specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: an fMRI study

Abstract

Implicit motor learning is preserved after stroke, but how the brain compensates for damage to facilitate learning is unclear. We used a random effects analysis to determine how stroke alters patterns of brain activity during implicit sequence-specific motor learning as compared to general improvements in motor control. Nine healthy participants and nine individuals with chronic, right focal subcortical stroke performed a continuous joystick-based tracking task during an initial functional magnetic resonance images (fMRI) session, over 5 days of practice, and a retention test during a separate fMRI session. Sequence-specific implicit motor learning was differentiated from general improvements in motor control by comparing tracking performance on a novel, repeated tracking sequence during early practice and again at the retention test. Both groups demonstrated implicit sequence-specific motor learning at the retention test, yet substantial differences were apparent. At retention, healthy control participants demonstrated increased blood oxygenation level dependent (BOLD) response in left dorsal premotor cortex (PMd; BA 6) but decreased BOLD response left dorsolateral prefrontal cortex (DLPFC; BA 9) during repeated sequence tracking. In contrast, at retention individuals with stroke did not show this reduction in DLPFC during repeated tracking. Instead implicit sequence-specific motor learning and general improvements in motor control were associated with increased BOLD response in the left middle frontal gyrus BA 8, regardless of sequence type after stroke. These data emphasize the potential importance of a prefrontal-based attentional network for implicit motor learning after stroke. This study is the first to highlight the importance of the prefrontal cortex for implicit sequence-specific motor learning after stroke.

Figure 1

Lesion location (outlined in red) for the nine participants of the ST group.

Figure 2

(A) Depiction of the target and participants' position representations as well as the joystick used by the participant during the tracking task (see methods for details). (B) Examples of the random and repeated tracking sequences that comprised the 20 s blocks during Days 2–6, the different shaded lines represents a separate block. (C) An example of the time course of the behavioral task during fMRI acquisition on Days 1 and 7. For the early practice and retention testing the random and repeated sequences were presented in separate 150 s blocks with the order of presentation counterbalanced across fMRI acquisition scans. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 3

Tracking performance (average RMSE) for both the HC and ST groups during early practice (fMRI No. 1), learning (Days 2–6) and at retention (fMRI No. 2) for the random and repeated sequences. Bars indicate standard error.

Figure 4

Anterior (top) and lateral (bottom) views of areas demonstrating significant Group × Sequence interaction at retention (Day 7). See Table III for interpretation. The color scale reflects t‐values. MFS, middle frontal sulcus; CS, central sulcus; MFG, middle frontal gyrus; SFG, superior frontal gyrus; MTG, middle temporal gyrus; PoCG, postcentral gyrus.

Figure 5

Plot of the mean percent signal change during random and repeated tracking for (A) the area of the DLPFC and (B) the area of the PMd that demonstrated significant Group × Sequence interactions at the retention test (Day 7).

Figure 6

Anterior (top) and lateral (bottom) views of areas demonstrating significant main effect of Group during early practice (Day 1: red/yellow) and at retention (Day 7: blue/green). See Table IV for interpretation. The color scale reflects t‐values. MFS, middle frontal sulcus; CS, central sulcus; MFG, middle frontal gyrus; preCG, precentral gyrus; IFG, inferior frontal gyrus.