Contributions of the parietal cortex to increased efficiency of planning-based action selection

Abstract

Response selection is foundational to adaptive behavior, and considerable attention has been devoted to investigating this behavior under conditions in which the mapping between stimuli and responses is fixed. Results from prior studies implicate the left supramarginal gyrus (SMg), premotor and prefrontal cortices, as well as the cerebellum in this essential function. Yet, many goal-directed motor behaviors have multiple solutions with flexible mappings between stimuli and responses whose solutions are believed to involve prospective planning. Studies of selection under conditions of flexible mappings also reveal involvement of the left SMg, as well as bilateral premotor, superior parietal cortex (SPL) and pre-supplementary motor (pre-SMA) cortices, along with the cerebellum. This evidence is, however, limited by exclusive reliance on tasks that involve selection in the absence of overt action execution and without complete control of possible confounding effects related to differences in stimulus and response processing demands. Here, we address this limitation through use of a novel fMRI repetition suppression (FMRI-RS) paradigm. In our prime-probe design, participants select and overtly pantomime manual object rotation actions when the relationship between stimuli and responses is either flexible (experimental condition) or fixed (control condition). When trials were repeated in prime-probe pairs of the experimental condition, we detected improvements in performance accompanied by a significant suppression of blood oxygen-level dependent (BOLD) responses in: left SMg extending into and along the length of the intraparietal sulcus (IPS), right IPS, bilateral caudal superior parietal lobule (cSPL), dorsal premotor cortex (dPMC), pre-SMA, and in the lateral cerebellum. Further, region-of-interest analyses revealed interaction effects of fMRI-RS in the experimental versus control condition within left SMg and cerebellum, as well as in bilateral caudal SPL. These efficiency effects cannot be attributed to the repetition of stimulus or response processing, but instead are planning-specific and generally consistent with earlier findings from conventional fMRI investigations. We conclude that repetition-related increases in the efficiency of planning-based selection appears to be associated with parieto-cerebellar networks.

Keywords: Action selection; fMRI repetition suppression.

Figure 1

Experimental setup

Figure 2. Experimental task

Example trials for Rule and Plan condition. One trial includes two events of the same condition (Rule or Plan). The shape of the fixation-cross indicates what task to execute; here: x=Rule, diamond=Plan. One trial consists of 15 sec fixation, followed by 2.5 sec prime event requiring the first response. Then 2.5 sec fixation cue are presented before the probe event starts, which requires the second response. Responses are over- or underhand postures, which are predetermined by the stimulus configuration (Rule condition) or selected based on the end-state comfort (Plan condition). In the Plan condition participants had to choose the most comfortable way to rotate the disk and align the same colored circle cue with the arrow. In the Rule condition subjects had to insert their hand with the thumb towards the same colored circle as the arrow, then rotate the disk to align the same colored circle cue with the arrow. The displayed example trials with correct responses show repeated events (a./b.) or changed events (c./d). By using similar stimuli and actions for both conditions, we controlled for effects of stimulus and response, but manipulate the approach for action selection.

Figure 3. Behavioral response times

Planning is apparent through significantly prolonged RT in the Plan- compared to the Rule condition. Priming occurs in both tasks, showing faster responses to the probe for repeated events. (Error bars: 95% Confidence Interval)

Figure. 4

A. Contrast between the experimental Plan and the control Rule condition. Activations bilaterally along the intraparietal sulcus and adjacent angular (Ang) and supramariginal (SMg) gyri are prominent. B. Repetition suppression of neural activity. The Plan repetition suppression effects are appear bilaterally in the posterior parietal cortex, dPMC, pre-SMA and cerebellum. The left IPS and SMg are accentuated. As described in the text, we failed to detect any regions exhibiting greater RS for the Rule condition.

Figure 5. Condition overlay of repetition suppression maps (Plan Change > Plan Repeated and Rule Change > Rule repeated)

Overlap is prominent in the left IPS, whereby results for the Rule condition are uncorrected for multiple comparisons.

Figure 6. The figure displays percent signal change in selected ROIs separately per condition (Plan, Rule) and trialtype (Congruency: Repeat, Change)

Percent signal change from the resting baseline within anatomical ROIs which were further delimited by the Rule + Plan vs baseline contrast. The interaction effect of condition × congruency was found to be significant in the left SMG (p<.05). Further effects were found in the cerebellum and bilateral cSPL (p<.07). The interaction results demonstrate planning specific efficiency effects. Errorbars represent 95% CI.