Brain areas selective for both observed and executed movements

Abstract

When observing a particular movement a subset of movement-selective visual and visuomotor neurons are active in the observer's brain, forming a representation of the observed movement. Similarly, when executing a movement a subset of movement-selective motor and visuomotor neurons are active, forming a representation of the executed movement. In this study we used an fMRI-adaptation protocol to assess cortical response selectivity to observed and executed movements simultaneously. Subjects freely played the rock-paper-scissors game against a videotaped opponent, sometimes repeatedly observing or executing the same movement on subsequent trials. Numerous brain areas exhibited adaptation (repetition suppression) during either repeated observations or repeated executions of the same movement. A subset of areas exhibited an overlap of both effects, containing neurons with selective responses for both executed and observed movements. We describe the function of these movement representation areas in the context of the human mirror system, which is expected to respond selectively to both observed and executed movements.

Figure 1

Experimental design. A. Example experiment timeline, showing the simultaneously observed (green) and executed (orange) movement type in each trial. B. Each trial was sorted according to the movement preceding it into 8 categories: observed, executed, observed-then-executed, and executed-then-observed repeats and nonrepeats. We expected to find fMRI adaptation in repeat trials as compared with nonrepeat trials.

Figure 2

ROI Selection in a typical subject. Top Row. Identification of the junction between the anterior intraparietal sulcus and the post central sulcus. Middle Row. Functional activity from the imitation experiment is overlaid (purple). Bottom Row. Selection of the ROI to include only active voxels within a maximum diameter of 13 mm³ surrounding the anatomical land-mark.

Figure 3

Movement-selective (visual and motor) adaptation. Statistical maps of brain areas responding less to repeated than non-repeated movement observation (green) and execution (orange) of the RPS movements. Six areas in the left hemisphere (movements were performed with the right hand) exhibited either an overlap (yellow) or close proximity of both visual and motor adaptation: anterior intraparietal sulcus (aIFS), ventral premotor (vPM) cortex, anterior intraparietal sulcus (aIPS), superior intraparietal sulcus (sIPS), posterior intraparietal sulcus (pIPS), and an area within lateral occipital (LO) cortex. Black ellipses loosely outline areas of interest.

Figure 4

Imitation and movement observation. A&B. Maps of activity evoked by imitation, execution, and observation (same format as left hemisphere in Figure 3). Purple, brain areas with larger responses during imitation than observation and execution. Cyan, larger responses during observation than rest. Orange, larger responses during execution than rest. C. Maps of activity evoked by observation of faces, houses, and movement observation. Red, larger responses to faces than houses & object manipulation. Green, larger responses to houses than faces & object manipulation. Blue, larger responses to object manipulation than faces & houses. Black ellipses loosely outline areas of interest.

Figure 5

Region of interest (ROI) analysis. Top row. Visual and motor adaptation. Comparison of fMRI response amplitudes in four conditions: observed non-repeat (dark green), observed repeat (light green), executed non-repeat (dark orange), executed repeat (light orange). Bottom row. Cross-modal interactions. Comparison of fMRI response amplitudes in four conditions: observed-then-executed non-repeat (dark blue), observed-then-executed repeat (light blue), executed-then-observed non-repeat (dark purple), and executed-then-observed repeat (light purple). ROIs were defined in each subject individually (Figure 2). fMRI responses from the RPS experiment were averaged across voxels in each ROI, and across games and subjects. Error bars, SEM across subjects. Asterisks, statistically significant difference (p < 0.05, paired t-test, Bonferronni corrected).

Figure 6

Responses to trial outcomes. Orange, areas that responded more during winning trials than losing trials. A. Several cortical and sub-cortical areas exhibited larger responses to winning than losing (p < 0.05). B. The same results displayed with a stricter statistical threshold (p < 0.003). Only the ventral striatum and a small area of visual cortex survived at this higher threshold. The opposite comparison (lose > win) did not yield any statistically significant activation.

Figure 7

Region of interest (ROI) analysis of trial outcomes. Error bars, SEM across subjects. There were no statistically significant differences between different trial outcomes in any of the examined ROIs (p > 0.18, ANOVA run independently for each ROI).

Figure 8

Region of interest (ROI) analysis split according to trial outcomes. Top row. Visual adaptation. Comparison of fMRI response amplitudes in six conditions: observed non-repeat win, lose, and draw (all in dark green) and observed repeat win, lose, and draw (all in light green). Bottom row. Motor adaptation. Comparison of fMRI response amplitudes in six conditions: executed non-repeat win, lose, and draw (all in dark orange) and executed repeat win, lose, and draw (all in light orange). Error bars, SEM across subjects. See Behavioral and Outcome Analyses in Results section for statistical details.

Figure 9

Motor adaptation from a separate instructed-movement experiment A. Maps of motor activity and motor adaptation (same format as left hemisphere in Figure 3). Blue, areas that responded more during executed movement than baseline. Orange, areas that responded less during executed movement repeats than non-repeats. B. Region of interest (ROI) analysis of response amplitudes during instructed-movement. Error bars, SEM across subjects. Asterisks, statistically significant difference (p < 0.05, paired t-test, Bonferronni corrected).