Oculomotor functional connectivity associated with motor sequence learning

Abstract

Acquisition of learned motor sequences involves saccades directed toward the goal to gather visual information prior to reaching. While goal-directed actions involve both eye and hand movements, the role of brain areas controlling saccades during motor sequence learning is still unclear. This study aimed to determine whether resting-state functional connectivity of oculomotor regions is associated with behavioral changes resulting from motor sequence learning. We investigated connectivity between oculomotor control regions and candidate regions involved in oculomotor control and motor sequence learning. Twenty adults had brain scans before 3 days of motor task practice and after a 24-hour retention test, which was used to assess sequence-specific learning. During testing, both saccades and reaches were tracked. Stronger connectivity in multiple oculomotor regions prior to motor task practice correlated with greater sequence-specific learning for both saccades and reaches. A more negative connectivity change involving oculomotor regions from pre- to post-training correlated with greater sequence-specific learning for both saccades and reaches. Overall, oculomotor functional connectivity was associated with the magnitude of behavioral change resulting from motor sequence learning, providing insight into the function of the oculomotor system during motor sequence learning.

Keywords: motor sequence learning; oculomotor connectivity; resting-state functional connectivity; saccades.

Fig. 1

Experimental design. Participants practiced an implicit motor sequence learning task over 3 consecutive days (24 h apart; ~15 min per day), and a retention test to assess sequence-specific motor learning was completed 24 h after the last practice session on day 4. MRI scans were acquired ~1 h prior to testing on day 1 and ~1 h after the retention test on day 4.

Fig. 2

Pro- and antisaccade KINARM task. Participants were cued to look toward a left or right peripheral visual stimulus (A. pro-saccade trial) or in the opposite direction (B. anti-saccade trial). The bullseye represents the location of gaze fixation at the following stages: cue, gap, and peripheral target. Arrows are presented here to represent the direction in which participants had to direct their gaze. Both the bullseye and arrows were not visible to the participant.

Fig. 3

Overlay of localizer scan activation maps. Activation maps from each participant (n = 20) derived from anti- > prosaccade contrast analyses are overlaid. Red areas in the heat map (the most central parts) represent regions with the greatest overlap between individual maps.

Fig. 4

ROIs used in rsFC analyses. ROI spheres representing oculomotor control regions (A) include: l/rFEF (yellow/dark yellow), SEF (dark red), l/rPEF (orange/red). ROI spheres representing candidate regions of oculomotor control and motor learning (B) include: l/rFEF (yellow/orange), striatum (black), and SMA (red).

Fig. 5

Pretraining connectivity results. Results showing significant, P-uncorrected, correlations between oculomotor rsFC and sequence-specific learning for saccades (A) and reaches (B). Overall, stronger baseline rsFC correlated with a greater magnitude of sequence-specific learning (RT change).

Fig. 6

Change (post–pretraining) in connectivity results. Results showing significant, P-uncorrected, correlations between change in oculomotor rsFC (post–pretraining) and sequence-specific learning for saccades (A); a more negative change in rsFC, from pre- to post-training, correlated with a greater magnitude of learning for saccades. Results showing significant, P-uncorrected, correlations between change in rFEF-rStriatum rsFC (post–pretraining) and sequence-specific learning for reaches (B); a more negative change in rsFC, from pre- to post-training, correlated with a greater magnitude of learning for reaches.

Fig. 7

Summary of connectivity findings. Stronger baseline connectivity (prior to motor training) correlated with greater behavioral change associated with motor learning (A). A decrease in connectivity from pre- to post-training correlated with greater behavioral change associated with motor learning (B). Left panel shows connectivity correlations with saccades, and the right panel shows connectivity correlations with reaches. Dotted lines indicate FDR-corrected results (P < 0.05). Solid lines indicate P-uncorrected results (P < 0.05).

Fig. 8

Resting-state networks showing increased functional connectivity after motor sequence learning. Significant, FWER-corrected RSNs at post- > pretraining are shown: (A) rVisual RSN (centered at max voxel: X = 34, Y = 29, Z = 43), and (B) rFP RSN (centered at max voxel: X = 44, Y = 49, Z = 50).