Interleaved practice enhances skill learning and the functional connectivity of fronto-parietal networks

Abstract

Practice of tasks in an interleaved order generally induces superior learning compared with practicing in a repetitive order, a phenomenon known as the contextual-interference (CI) effect. Increased neural activity during interleaved over repetitive practice has been associated with the beneficial effects of CI. Here, we used psychophysiological interaction (PPI) analysis to investigate whether the neural connectivity of the dorsal premotor (PM) and the dorsolateral prefrontal (DLPFC) cortices changes when motor sequences are acquired through interleaved practice. Sixteen adults practiced a serial reaction time task where a set of three 4-element sequences were arranged in a repetitive or in an interleaved order on 2 successive days. On Day 5, participants were tested with practiced sequences to evaluate retention. A within-subjects design was used so that participants practiced sequences in the other condition (repetitive or interleaved) 2-4 weeks later. Functional magnetic resonance images were acquired during practice and retention. On Day 2 of practice, there was greater inter-regional functional connectivity in the interleaved compared with the repetitive condition for both PM-seeded and DLPFC-seeded connectivity. The increased functional connectivity between both seeded regions and sensorimotor cortical areas correlated with the benefit of interleaved practice during later retention. During retention, a significant PPI effect was found in DLPFC-seeded connectivity, with increased DLPFC-supplementary motor area connectivity correlated with the benefits of interleaved practice. These data suggest that interleaved practice benefits learning by enhancing coordination of sensorimotor cortical regions, and superior performance of sequences learned under CI is characterized by increased functional connectivity in frontal cortex.

Figure 1

Participants practiced serial reaction time sequence learning tasks (A) in both a repetitive and an interleaved order (B). Participants practiced tasks for two consecutive days with the retention tests of trained and untrained sequences taking place on Day 5. Imaging data were acquired concurrently while the participants practiced the tasks. During repetitive practice, participants performed the same sequence repeatedly for the same scan run. 2 weeks after practice and retention for one training order, participants returned to practice a different set of three sequences in the other condition (e.g., repetitive practice → interleaved practice).

Figure 2

Mapping the modulatory effects of learning on cerebral functional networks. To detect the difference in functional connectivity of the brain between repetitive and interleaved practices in sequence learning, at every voxel of the brain, the functional BOLD time series was regressed against that of the right premotor cortex (upper row) or the right dorsal lateral prefrontal cortex (DLPFC, lower row), with the interleaved or repetitive condition as the interaction term, and between‐participant variability as the random‐effects variable. The resulting significance maps are displayed in neurological orientation, with the MNI coordinate (in mm) at the bottom. Colored regions, where voxel t‐values are positive, indicate that the interaction effects of interleaved practice had significantly greater interaction effects than repetitive practice on the functional relationship between that region and the premotor (upper row) or DLPFC (lower row) cortex, corrected for multiple comparisons using the topological false discovery rate (FDR) method. On Day 1 (A and D), modulatory effects of practice conditions were not significant, evaluated using either the premotor cortex or DLPFC as the seed region. On Day 2, interleaved practice led to higher correlations between the premotor cortex with sensorimotor planning regions, including the cerebellum, the medial frontal, and posterior parietal areas (B). Higher correlations between DLPFC and the caudate, the precentral and postcentral gyri, and the posterior parietal areas (E), were also associated with interleaved practice. On Day 5, modulatory effects of practice on the premotor cortex disappeared (C), but still remained with connectivity between DLPFC and other frontal regions, although the significance was attenuated (F). These results suggest that more brain regions with strong functional linkage need to be recruited during the acquisition phase of motor learning in the interleaved than repetitive practice conditions.

Figure 3

Interaction effect of practice conditions on functional connectivity between the right premotor area and other brain regions. BOLD activities, corrected for head movements, in the primary motor area (M1, A), cerebellum [CB, (B)], the inferior parietal [IPL, (C)], and superior parietal areas [SPL,(D)], were plotted against the right premotor activities, respectively under the interleaved (black dots) and repetitive practice conditions (red dots) on Day 2 for a typical participant. Regression slopes with respect to these four ROIs were all significantly greater under the interleaved than repetitive practice condition. These findings indicate that on the second day of practice, interleaved tasks evoked stronger premotor modulation on brain regions involved in sensorimotor integration and error corrections.

Figure 4

Differences in the connectivity of the right DLPFC circuit for a typical participant practicing in the interleaved (black dots) and repetitive (red dots) conditions on Day 2. The Regression slope of BOLD activities between the right DLPFC and the supplementary motor area [SMA, (A)], the caudate nucleus (B), the inferior parietal [IPL, (C)] and the superior parietal areas [SPL, (D)], and the superior medial frontal area [SMF, (E)], is higher in the interleaved practice, showing a stronger functional connectivity in the interleaved than the repetitive condition. These findings indicate that on Day 2, interleaved practice induced more DLPFC modulation on prefrontal, parietal, and subcortical regions, suggesting the stronger demand for attention, executive function, and task switching during interleaved practice.

Figure 5

Differences in the connectivity of the right DLPFC circuit between the interleaved (black dots) and repetitive practices (red dots) on Day 5. The participant selected for demonstration and the experimental settings are the same as Fig. 4, except that the BOLD responses were measured on Day 5. Similar to Day 2 (as shown in Fig. 4), regression slopes with respect to retention testing were higher following the interleaved practice, measured between the BOLD responses for the right DLPFC and the supplementary motor area [SMA, (A)], the caudate nucleus (B), the inferior parietal area [IPL, (C)], and the superior medial frontal area [SMF, (E)]. However, the interaction effect of the interleaved practice almost disappeared for connectivity between the DLPFC and the superior parietal regression [SPL, (D)]. These findings indicate that successful retrieval of the practiced sequences, especially the performance following interleaved practice, requires more DLPFC modulation on prefrontal areas of the brain.

Figure 6

Greater interaction effects of practice conditions are associated with greater learning benefit. The x‐axis indicates the difference in regression slopes of the interleaved minus the repetitive practice condition, for BOLD activities between the ROI pair. Higher x‐values mean a greater interaction effect of the interleaved practice. Learning benefit is represented by the difference in the response time (RT) between the interleaved and the repetitive practices, measured on the retention testing on Day 5 and displayed on the y‐axis. Here, we used the difference in RT of the repetitive minus the interleaved practice (note that this is opposed to the “interleaved minus repetitive” difference in the x‐axis), as we already knew that the interleaved practice led to better learning performance (Lin et al., 2011), and preferred the same direction for data in the x‐ and y‐axes. Our results show that greater differences in regression slopes for BOLD activities between the interleaved and repetitive practices, no matter measured during practice (Day 2, A and B) or retention testing (Day 5, C), correlate to greater learning benefit. This also indicates that when one practices sequences in an interleaved order, stronger connectivity within the cortical motor network is required for successful sequence retrieval. PM, dorsal premotor area; M1, primary motor area; DLPFC, dorsolateral prefrontal cortex; SPL, superior parietal area; SMA, supplementary motor area.