Effective connectivity of the human mirror neuron system during social cognition

Abstract

The human mirror neuron system (MNS) can be considered the neural basis of social cognition. Identifying the global network structure of this system can provide significant progress in the field. In this study, we use dynamic causal modeling (DCM) to determine the effective connectivity between central regions of the MNS for the first time during different social cognition tasks. Sixty-seven healthy participants completed fMRI scanning while performing social cognition tasks, including imitation, empathy and theory of mind. Superior temporal sulcus (STS), inferior parietal lobule (IPL) and Brodmann area 44 (BA44) formed the regions of interest for DCM. Varying connectivity patterns, 540 models were built and fitted for each participant. By applying group-level analysis, Bayesian model selection and Bayesian model averaging, the optimal family and model for all experimental tasks were found. For all social-cognitive processes, effective connectivity from STS to IPL and from STS to BA44 was found. For imitation, additional mutual connections occurred between STS and BA44, as well as BA44 and IPL. The results suggest inverse models in which the motor regions BA44 and IPL receive sensory information from the STS. In contrast, for imitation, a sensory loop with an exchange of motor-to-sensory and sensory-to-motor information seems to exist.

Keywords: Bayesian model selection; dynamic causal modeling; fMRI; mirror neuron system; social cognition.

Fig. 1.

Imitation Task. (A) Overview over the four conditions imitation, observation, execution and control, with exemplary stimuli. In all conditions except control, half of the stimuli showed angry, the other half fearful facial expressions or word cues. The control condition served as a motor control without emotional information. (B) Task flow with presentation times. At the beginning of each block, a cue word served as an instruction. In the experimental blocks, four stimuli with a duration of 5 s were presented, in the control blocks, two stimuli with 3 s duration.

Fig. 2.

Empathy task. (A) Overview over the four conditions personal distress, cognitive empathy, affective empathy and control with exemplary stimuli. In all empathy conditions, half of the stimuli showed angry, the other half fearful facial expressions or word cues. The control condition showing a circle of different sizes served as a visual control that also required rating on a visual analog scale. (B) Task flow with presentation times. At the beginning of each block, the cue question was presented. In the experimental blocks, four stimuli with a duration of 3 s were presented, in the control blocks, two stimuli with 3 s duration.

Fig. 3.

ToM task. (A) Overview over the four conditions ToM, emotion recognition, neutral face processing and control, with exemplary stimuli. Faces in the ToM and emotion recognition condition showed angry and fearful expressions, in the neutral face processing condition neutral expressions, and geometric figures served as stimuli in the control condition. (B) Task flow with presentation times. The stimuli are presented in pseudo-randomized order in an event-related design.

Fig. 4.

Model space. Schemata of parameters that made up the models included in four families. Solid lines show the connections that always are present, and dashed lines the connections that can be present or not. The modulatory input can be exerted on these interregional connections. Family 1 consists of four sub-families, and family 4 includes two sub-families. For each family, we assumed visual input external input always integrates into the STS region.

Fig. 5.

Family level inference performed on models within the families in Figure 1. All experiments demonstrate that family 1 has the highest expected and exceedance probability, in which the models within this family have forward connections from STS to IPL and BA44.

Fig. 6.

BMA results for all three tasks for the winning family 1. Here, we illustrate only the parameters which are significantly > 0. The values for external inputs (Matrix C), which are not reported in Tables 2 and 3, are shown here (all parameters are in Hz).