Human posterior parietal cortex mediates hand-specific planning

Abstract

The processes underlying action planning are fundamental to adaptive behavior and can be influenced by recent motor experience. Here, we used a novel fMRI Repetition Suppression (RS) design to test the hypotheses that action planning unfolds more efficiently for successive actions made with the same hand. More efficient processing was predicted to correspond with both faster response times (RTs) to initiate actions and reduced fMRI activity levels - RS. Consistent with these predictions, we detected faster RTs for actions made with the same hand and accompanying fMRI-RS within bilateral posterior parietal cortex and right-lateralized parietal operculum. Within posterior parietal cortex, these RS effects were localized to intraparietal and superior parietal cortices. These same areas were more strongly activated for actions involving the contralateral hand. The findings provide compelling new evidence for the specification of action plans in hand-specific terms, and indicate that these processes are sensitive to recent motor history. Consistent with computational efficiency accounts of motor history effects, the findings are interpreted as evidence for comparatively more efficient processing underlying action planning when successive actions involve the same versus opposite hand.

Keywords: Action planning; Action priming; Grasping; Recent motor experience; Sensorimotor control; fMRI repetition suppression.

Figure 1. Methods

(A) Apparatus used to present objects. (B) Complete set of object rotation actions required, for either hand. (C) Experimental conditions and the timing of events within trials. Prime and probe events were defined as 5s periods, each beginning with 500ms illumination of objects and the workspace followed by task performance in the dark. Task performance involved reaching, grasping and rotating objects, which took approximately 2–3s to complete. An additional 2.5s delay period separated prime-probe events. (D) Prime and probe predictors used for the general linear model for the main analysis.

Figure 2. Non-grasp manipulation strategies

Shown are examples of non-grasp manipulation strategies used to perform object-rotation tasks. Most importantly, the movement characteristics are distinct for rotations away-from versus toward the acting hand. As such, the HR condition comprised successive actions with the same hand that involved distinct movements and object manipulation goals. The table inset shows which manipulation strategy was preferred for actions involving object rotations toward versus away from the acting hand per subject, expressed as the percentage of trials involving grasps. Almost all participants used non-grasps for rotations away from the hand, and many also used non-grasps for rotations toward the acting hand.

Figure 3. Probe response time results

(A) Group mean RTs for probe events as a function of Condition. Error bars reflect mean standard errors. (B) Post-hoc pairwise comparisons revealed hand repetition priming, evident as the mean difference between RTs for NR – HR conditions (left), as well as GR – HR conditions (middle). Conversely, there was no reliable evidence for (hand-independent) grasp repetition priming, shown as the mean difference between RTs for NR – GR conditions (right), not statistically different from zero. For each of these post-hoc comparisons, error bars reflect 95% confidence intervals based on the standard errors of the respective mean difference scores across individuals, Bonferroni corrected.

Figure 4. Repetition suppression for the IR condition

The contrast NR_PROBE > IR_PROBE yielded activity in bilateral posterior parietal cortex, dorsal and ventral premotor cortex, medial frontal cortex (including cingulate, supplementary, and pre-supplementary motor areas), secondary somatosensory cortex within the parietal operculum, basal ganglia, and left-lateralized dorsal lateral prefrontal and occipito-temporal cortex.

Figure 5. Repetition suppression for HR condition

The contrast of NR_PROBE > IR_PROBE ∧ (NR_PROBE + GR_PROBE) > HR_PROBE yielded significant fMRI-RS effects for the HR condition within left and right posterior parietal cortex and right-lateralized parietal operculum. At uncorrected thresholds, activity for this contrast was also evident in left dorsal precentral and bilateral cingulate cortices (Inline Supplementary Fig. 5). Similar results but at uncorrected thresholds were identified with the contrast NR_PROBE > IR_PROBE ∧ NR_PROBE > HR_PROBE (Inline Supplementary Fig. 2).

Figure 6. ROI results

Two additional analyses were performed on each of the areas showing fMRI-RS the HR condition as defined by the contrast: NR_PROBE > IR_PROBE ∧ (NR_PROBE + GR_PROBE) > HR_PROBE (Fig. 5). (A, B, C) For each area, event-related averaged percent BOLD signal change (%-BSC) values per condition are shown as a function of time. Notice how signal changes attributable to prime events closely overlap across conditions. Differences between conditions arise later in time, attributable to probe events. These aspects of time-course data are also shown at finer scales (see insets), to better illustrate condition differences. Error bars reflect standard errors of the means at each time point. (D, E, F) For each area, the mean difference scores between beta weights for right- versus left-handed actions are indicated. Error bars reflect 95% confidence intervals. All three areas show evidence of contralateral effector-specificity (p’s < 0.001).