Dissociating object directed and non-object directed action in the human mirror system; implications for theories of motor simulation

Abstract

Mirror neurons are single cells found in macaque premotor and parietal cortices that are active during action execution and observation. In non-human primates, mirror neurons have only been found in relation to object-directed movements or communicative gestures, as non-object directed actions of the upper limb are not well characterized in non-human primates. Mirror neurons provide important evidence for motor simulation theories of cognition, sometimes referred to as the direct matching hypothesis, which propose that observed actions are mapped onto associated motor schemata in a direct and automatic manner. This study, for the first time, directly compares mirror responses, defined as the overlap between action execution and observation, during object directed and meaningless non-object directed actions. We present functional MRI data that demonstrate a clear dissociation between object directed and non-object directed actions within the human mirror system. A premotor and parietal network was preferentially active during object directed actions, whether observed or executed. Moreover, we report spatially correlated activity across multiple voxels for observation and execution of an object directed action. In contrast to predictions made by motor simulation theory, no similar activity was observed for non-object directed actions. These data demonstrate that object directed and meaningless non-object directed actions are subserved by different neuronal networks and that the human mirror response is significantly greater for object directed actions. These data have important implications for understanding the human mirror system and for simulation theories of motor cognition. Subsequent theories of motor simulation must account for these differences, possibly by acknowledging the role of experience in modulating the mirror response.

Figure 1. Activity associated with observing and executing actions.

BOLD responses associated with observing and executing different types of action compared to a static baseline are displayed in the top panel (p<0.005, cluster threshold = 25). Significant activity associated with execution of an object directed action (Execute_Trans) are seen in sensorimotor cortices in both hemispheres and right cerebellum (a). Observing an object directed action (Observe_Trans) was associated with activity in bilateral premotor, superior parietal and lateral occipital areas associated with visual motion (b). Motor responses to execution of a non-object directed action (Execute_Intrans) are seen in similar regions to the motor responses to Execute_Trans (c), however the premotor and parietal activity seen during observation of a object directed action is absent when observing an non-object directed action (d). BOLD responses seen during observing a non-object directed action (Observe_Intrans) in lateral occipital areas only. All statistical parametric maps displays experimental conditions compared to a passive rest condition (Observe_Rest) and are thresholded at p<0.005 uncorrected, cluster extent threshold = 25.

Figure 2. Mirror responses: activity common to execution and observation.

Inclusive masking was used in order to look at significant activity common to both execution and observation conditions. BOLD responses to Observe_Trans+Execute_Trans were seen in premotor cortex, dorsal parietal cortex in both hemispheres and right lateral occipital cortex (a, orange). The same approach for Observe_Intrans+Execute_Intrans revealed significant activity in both contrasts in left occipital cortex only (a, blue). A direct comparison of activity common to execution and observation of an object directed actions more than an non-object directed action (Observe_Trans>Observe_Intrans)+(Execute_Trans>Execute_Intrans) allowed us to highlight voxels that are commonly activated in observing and executing an object-directed grasp more than executing and observing non-object directed movement. This analysis revealed significant activations in bilateral premotor and parietal cortices (b) (28 −48 56, −28 −52 58, 28 −14 56, −30 −4 60, −36 −38 52). The reverse comparison, (Observe_Intrans>Observe_Trans)+(Execute_Intrans>Execute_Trans), revealed no significant activity.

Figure 3. Individual overlaps for Observe and Execute in objected directed and non-object directed action.

A mask was used to restrict our analysis to regions significantly active in Observe and Execute conditions (voxels active for all four conditions, p<0,05; within an anatomically defined mask of premotor and parietal regions). These individual masks vary across individuals in widespread premotor and parietal cortices bilaterally (a). Regions of highest overlap are seen in green. The coordinates of peak overlap were −34 −59 64, 36 −42 52, −48 2 35, and −42, −9 58. Within these individual masks, we then looked at the mean correlation between Observe and Execute for the two difference action conditions; object directed and non-object directed. The mean correlation between Observe and Execute was highly significantly greater for object directed action compared to non-object directed action (b).

Figure 4. Whole brain analyses of spatial correlation.

In addition to the ROI analysis shown in Figure, we also carried out a brain wide search in order to see if there were any other cortical regions displaying a spatial correlation between Execute and Observe conditions. A spherical searchlight was applied to the whole brain and significant correlations were compared for Observe Object directed action and Execute Object directed action (Observe_Trans_Execute_Trans), and Observe Non-object directed action and Execute Non-object directed action (Observe_Intrans_Execute_Intrans). Figure (a) shows spatial correlations were greater for Observe_Trans_Execute_Trans compared to Observe_Intrans_Execute_Intrans in left frontal cortex, inferior frontal gyrus and postcentral gyrus (BA 3). The lower panel shows an anticorrelation in left postcentral sulcus that is present for Observe_Trans_Execute_Trans but not for Observe_Intrans_Execute_Intrans (b).