Separate areas for mirror responses and agency within the parietal operculum

Abstract

There is common neural activity in parietal and premotor cortex when executing and observing goal-directed movements: the "mirror" response. In addition, active and passive limb movements cause overlapping activity in premotor and somatosensory cortex. This association of motor and sensory activity cannot ascribe agency, the ability to discriminate between self- and non-self-generated events. This requires that some signals accompanying self-initiated limb movement dissociate from those evoked by observing the action of another or by movement imposed on oneself by external force. We demonstrated associated activity within the medial parietal operculum in response to feedforward visual or somatosensory information accompanying observed and imposed finger movements. In contrast, the response to motor and somatosensory information during self-initiated finger and observed movements resulted in activity localized to the lateral parietal operculum. This ascribes separate functions to medial and lateral second-order somatosensory cortex, anatomically dissociating the agent and the mirror response, demonstrating how executed and observed events are distinguished despite common activity in widespread sensorimotor cortices.

Figure 1.

Neural activations associated with Observe, Execute, and Passive conditions are widely overlapping. During the observation of a finger tap versus a Rest condition (a), activity was observed in bilateral parietal operculum, anterior parietal, inferior frontal gyri, and visual cortices, including visual cortical area V5/middle temporal visual motion areas (all contrasts at FDR of 0.05, extent 20). Active finger tapping (b) was accompanied by additional activations in ipsilateral cerebellum, contralateral primary motor cortex, and supplementary motor area. Passively imposed finger movements also resulted in increased activity in similar areas, including contralateral somatosensory cortices, supplementary motor area, parietal operculum, and inferior frontal gyri (c). The Static condition involved observing a static hand against observing a static background that was accompanied by increased activity in visual cortices and bilateral inferior frontal gyri (highlighted). L, Left; R, right.

Figure 2.

Active movements are associated with right cerebellar activity compared with passive movements. Contrasting BOLD responses during blocks of active finger tapping with blocks of passive finger tapping reveals a right lateralized cerebellar activation that is specific to self-generated action (red; 4, −50, −20). The opposite contrast that identifies patterns of BOLD activity that are more correlated with passive rather than active finger tapping are seen in bilateral parietal operculum and left anterior parietal lobes (blue) corresponding to area 2 (n = 20; FDR of 0.01; k = 20; 48, −30, 26; 32, −36, 62; −52, −22, 50; −46, −28, 24). The consequential afferent input in both conditions is the same, and thus the presence of somatosensory processing in Passive with respect to Execute demonstrates that, during self-generated action, sensory processing is suppressed or “gated.”

Figure 3.

Distinct regions within parietal operculum encode mirror responses and agency. Inclusive masking was used to identify voxels common to both Observe and Active conditions with Static as a baseline condition. Clusters of 20 voxels or more that displayed this profile were defined as exhibiting a mirror response. Such mirror responses, seen in red, were observed in bilateral parietal operculum (inclusive masking at 0.00095; FDR of 0.05, spatial extent 20; at 62, −30, 20 and at −50, −28, 22). To highlight the networks that discriminates between internal and external agents, seen in blue, voxels active during externally originating events were contrasted with self-generated actions (Observe − Execute inclusively masked by Passive − Execute, inclusively masked at 0.00095; FDR of 0.05, spatial extent 20; peak activation at 46, −22, 22, which was used for region of interest analysis along with a symmetrical regions at −46, −22, 22). Graphs display mean contrast estimates at these peak coordinates for all conditions against Baseline condition. Regions of interest were taken using a sphere of 4 mm radius at each functional peak). Note that, in the lateral extent of parietal operculum, the mirror response, Execute is down with respect to Baseline and Static. Inset is taken from the probabilistic atlas used to localize these regions; in this image, green refers are OP1 (Eickhoff et al., 2006).