On the role of object information in action observation: an fMRI study

Abstract

Observing other people's actions activates a network of brain regions that is also activated during the execution of these actions. Here, we used functional magnetic resonance imaging to test whether these "mirror" regions in frontal and parietal cortices primarily encode the spatiomotor aspects or the functional goal-related aspects of observed tool actions. Participants viewed static depictions of actions consisting of a tool object (e.g., key) and a target object (e.g., keyhole). They judged the actions either with regard to whether the objects were oriented correctly for the action to succeed (spatiomotor task) or whether an action goal could be achieved with the objects (function task). Compared with a control condition, both tasks activated regions in left frontoparietal cortex previously implicated in action observation and execution. Of these regions, the premotor cortex and supramarginal gyrus were primarily activated during the spatiomotor task, whereas the middle frontal gyrus was primarily activated during the function task. Regions along the intraparietal sulcus were more strongly activated during the spatiomotor task but only when the spatiomotor properties of the tool object were unknown in advance. These results suggest a division of labor within the action observation network that maps onto a similar division previously proposed for action execution.

Figure 1.

Example stimuli for correct actions in the 3 stimulation conditions and the respective mismatches. For illustration purposes, instruments and goal objects are combined in one frame but were presented separately in the experiment (see Fig. 2). Left column (insertion action condition): coin inserted into vending machine with correct orientation, coin inserted into vending machine with incorrect orientation, and safety belt inserted into the vending machine. Middle column (tool action condition): hole puncher applied to paper in correct orientation, hole puncher applied to paper in incorrect orientation, and sponge being applied to paper. Right column (object control condition): compact disc and music cassette with same orientations, compact disc and music cassette with different orientations, and compact disc and jar of honey.

Figure 2.

Schematic illustration of the design of the experiment, showing from top to bottom: runs within the experiment, blocks within runs, trials within the blocks, and the course of each trial.

Figure 3.

The upper panel shows areas activated more strongly in the 2 action observation conditions (tool action and insertion action) than in the object control condition (thresholded at P < 0.001, as used for the ROI analysis). The lower 3 panels show the beta estimates in the 3 experimental conditions (tool action, insertion action, object control) and the two tasks (space, function). Left panel: region in the mFG with a selective engagement in spatial and functional tasks requiring object-based action knowledge. Middle panel: premotor and supramarginal regions showing a stronger response for spatiomotor judgments in both action observation conditions. Right panel: intraparietal regions showing stronger responses for spatiomotor judgments in the tool action condition, in particular.

Figure 4.

Regions showing significant changes in effective connectivity with the mFG (a) and cIPS (b) between the space task in the tool action condition, where the space task depended on object use, and in the insertion action condition, where the space task was independent from object use (thresholded at P < 0.001, as used for the ROI analysis). Note that (b) also shows an additional cluster in the right IPL with enhanced connectivity to the cIPS that did, however, not pass correction for multiple comparisons at FDR (q < 0.05). Dotted circles show the approximate positions of the reference regions (a, mFG; b, cIPS, see also Fig. 3). mTG, middle temporal gyrus.