Mental Simulation of Action in the Service of Action Perception

Abstract

We used the quantitative 14 C-deoxyglucose method to map the activity pattern throughout the frontal cortex of rhesus monkeys, which either grasped a three-dimensional object or observed the same grasping movements executed by a human. We found that virtually the same frontal cortical networks were recruited for the generation and the perception of action, including the primary motor cortex (MI/F1), premotor cortical areas (F2, F5, and F6), the primary (SI) and supplementary (SSA) somatosensory cortex, medial cortical areas (8m and 9m), and the anterior cingulate. The overlapping networks for action execution and action observation support the notion that mental simulation of action could underlie the perception of others' actions. We suggest that the premotor and the somatotopic MI/F1 activations induced by action observation reflect motor grasp of the observed action, whereas the somatotopic SI and the SSA activations reflect recruitment of learned sensory-motor associations enabling perceptual understanding of the anticipated somatosensory feedback. We also found that the premotor activations were stronger for action observation, in contrast to the primary somatosensory-motor ones, which were stronger for action execution, and that activations induced by observation were bilateral, whereas those induced by execution were contralateral to the moving forelimb. We suggest that these differences in intensity and lateralization of activations between the executive and the perceptual networks help attribute the action to the correct agent, i.e., to the "self" during action execution and to the "other" during action observation. Accordingly, the "sense of agency" could be articulated within the core components of the circuitry supporting action execution/observation.

The Spinal Substrate of the Suppression of Action during Action Observation

“…Recent imaging studies using the 14 C-deoxyglucose ( 14 C-DG) method demonstrated that the areas activated in the brain of an actor performing a grasping movement and those of an observer watching the performance of the very same movement by another subject are virtually the same. This common neural network involves the forelimb representations of the primary motor and somatosensory cortices; several premotor and cingulate areas; extensive regions of the posterior, lateral, and medial parietal; and the intraparietal cortex (Raos et al, 2004(Raos et al, , 2007Evangeliou et al, 2009). These findings support the notion that we understand observed actions by mentally simulating them.…”

“…For this reason, we provide quantitative description of the behavior of the monkeys during the critical period of the first 10 min. The oculomotor performance of some of the monkeys, either as instantaneous eye position averaged over all trials or as threedimensional histograms of the dwell time of the line of sight as a function of eye position, during the critical 10 first minutes of the 14 C-DG experiment was presented previously (Raos et al, 2007;Evangeliou et al, 2009). Presently, the oculomotor and skeletomotor performance are briefly reported.…”

“…Experimental protocols were approved by the institutional animal use committee. A detailed description of the surgical procedures, the recording of eye position, and EMG was reported previously (Raos et al, 2004(Raos et al, , 2007Evangeliou et al, 2009). All surgical procedures were performed under general anesthesia and aseptic conditions.…”

“…Normalization of LCGU values was based on the averaged unaffected area of the spinal gray-matter value pooled across all monkeys (Raos et al, 2004(Raos et al, , 2007Evangeliou et al, 2009). To normalize metabolic activity, LCGU values were multiplied with a factor that was separately determined for each spinal cord.…”

“…Because side-to-side differences in normal monkeys rise up to 7% (Kennedy et al, 1978), only differences Ͼ7% were considered for statistical treatment. To determine statistical significant differences, we relied on Student's unpaired t test (Raos et al, 2004(Raos et al, , 2007Evangeliou et al, 2009).…”