Predicting and memorizing observed action: differential premotor cortex involvement

Abstract

Many studies have shown the involvement of the premotor cortex in action observation, recognizing this region as the neural marker of action simulation (i.e., internal modeling on the basis of the observer's own motor repertoire). So far, however, we have remained unaware of how action simulation differs from more general action representation in terms of premotor activation. The present fMRI experiment is the first to demonstrate how premotor structures contribute to action simulation as opposed to other action-related cognitive tasks, such as maintaining action representations. Using similar stimuli, a prediction condition requiring internal simulation of transiently occluded actions was compared to three different action-related control tasks differing solely in task instructions. Results showed right pre-SMA activation as a correlate of maintaining action representations in general. Moreover, the prediction condition was most efficient in activating the left pre-SMA and left PMd. These results suggest that the conjoint activation of the pre-SMA and PMd reflects a core neural driver of action simulation.

Figure 1

Experimental conditions. Panels show four conditions (Prediction, Freezing, Detection, and Counting) employing the same video‐clips. The bars on the bottom of each panel represent ongoing video presentation during which black boxes repeatedly occluded the whole screen for 1 s in Prediction, Freezing, and Counting conditions. On average, a 60‐s video was occluded five times. In Detection, instead of occlusions, a border surrounding the display changed color for 1 s. With every new video, the task changed and this was announced visually. In the conditions Prediction, Freezing and Detection, the observation of the ongoing course of the action was required. In Prediction, participants indicated whether the action continued with coherent timing after each occluder. In Freezing, they memorized the last frame before occlusion to judge whether the video continued from the same position. When the border was colored in Detection, participants were asked to detect occasional disruptions in the smoothness of the ongoing action. In these three conditions, yes/no response‐buttons were pressed as soon as possible after the offset of occlusions or colored borders. The depicted scenes are taken from a video‐clip to illustrate two single trials for each condition. The pictures on the left show an incoherent continuation in Prediction, a mismatch in Freezing, and a disrupted action in Detection. The examples depicted on the right illustrate accurate trials for each condition. The Counting condition did not draw attention to the action. Instead, participants counted occlusions and indicated whether a clip contained more or fewer than five of these.

Figure 2

Effects related to the maintenance of an internal reference. Depicted statistical maps (group‐averaged, n = 18) show results obtained in conjunction analyses using the logical combination method [Joseph et al., 2002] to integrate (A) contrasts of the Prediction condition with Counting (P > C) and Detection (P > D), (B) contrasts of the Freezing condition with Counting (F > C) and Detection (F > D) and (C) all contrasts of the Prediction condition and the Freezing condition with control conditions ((P > C) ∩ (P > D) ∩ (F > C) ∩ (F > D)). Z‐maps were thresholded at z = 2.58 (P < 0.05 corrected). The pre‐SMA was activated during maintenance of an internal reference in the Prediction condition (A) and also in the Freezing condition (B) which explains its activation in the conjunction analysis (C). Lateral premotor areas (PMd and PMv) were only activated when contrasting the Prediction condition with control conditions (A). See Table I for detailed information on coordinates and z‐scores and for anatomical abbreviations.

Figure 3

Brain correlates of active, internal action prediction. Group‐averaged (n = 18) statistical maps show significant activation in the left pre‐SMA (x = −9, y = 16, z = 42) and left PMd (x = −24, y = 1, z = 51) in the Prediction condition as opposed to the Freezing condition. Z‐maps were thresholded at z = 2.58 (P < 0.05 corrected). The bar diagrams show percent signal changes (PSC) in the activated clusters. Separate bars represent the experimental conditions. The crossing of the category axis is aligned to null‐events. In addition to the differences between Prediction and Freezing, as revealed in statistical maps, Freezing differed significantly from Detection and Counting with regard to pre‐SMA activation. In the PMd, a significant difference was found between Freezing and Counting. Significant differences are indicated by asterisks; ** P < 0.01; * P < 0.05). Anatomical abbreviations: pre‐SMA, presupplementary motor area; PMd, dorsal premotor cortex.