Cortical Activation during Action Observation, Action Execution, and Interpersonal Synchrony in Adults: A functional Near-Infrared Spectroscopy (fNIRS) Study

Abstract

Introduction: Humans engage in Interpersonal Synchrony (IPS) as they synchronize their own actions with that of a social partner over time. When humans engage in imitation/IPS behaviors, multiple regions in the frontal, temporal, and parietal cortices are activated including the putative Mirror Neuron Systems (Iacoboni, 2005; Buxbaum et al., 2014). In the present study, we compared fNIRS-based cortical activation patterns across three conditions of action observation ("Watch" partner), action execution ("Do" on your own), and IPS (move "Together"). Methods: Fifteen typically developing adults completed a reach and cleanup task with the right arm while cortical activation was examined using a 24-channel, Hitachi fNIRS system. Each adult completed 8 trials across three conditions (Watch, Do, and Together). For each fNIRS channel, we obtained oxy hemoglobin (HbO₂) and deoxy hemoglobin (HHb) profiles. Spatial registration methods were applied to localize the cortical regions underneath each channel and to define six regions of interest (ROIs), right and left supero-anterior (SA or pre/post-central gyri), infero-posterior (IP or angular/supramarginal gyri), and infero-anterior (IA or superior/middle temporal gyri) regions. Results: In terms of task-related differences, the majority of the ROIs were more active during Do and Together compared to Watch. Only the right/ipsilateral fronto-parietal and inferior parietal cortices had greater activation during Together compared to Do. Conclusions: The similarities in cortical activation between action execution and IPS suggest that neural control of IPS is more similar to its execution than observational aspects. To be clear, the more complex the actions performed, the more difficult the IPS behaviors. Secondly, IPS behaviors required slightly more right-sided activation (vs. execution/observation) suggesting that IPS is a higher-order process involving more bilateral activation compared to its sub-components. These findings provide a neuroimaging framework to study imitation and IPS impairments in special populations such as infants at risk for and children with ASD.

Keywords: action execution; action observation; autism; fNIRS; imitation; interpersonal synchrony; mirror neuron system.

Figure 1

Experimental setup (A–C) and task sequence (D). Written permission for publication of participant pictures has been taken.

Figure 2

Probe placement (A,B) and spatial registration output (C,D). Written permission for publication of participant pictures has been taken.

Figure 3

Data processing workflow: (A) Filter, wavelet and GLM of NIRS signal and (B) Trial-by-trial view and Average view of Oxy Hb (HbO₂), Deoxy Hb (HHb), and Total Hb (HbT) profiles for a given channel. (W, D, T) from 5 s before to 24 s after start of stimulation. Data have been averaged across trials and participants.

Figure 4

Second to second blocked HbO₂ data per condition and channel. Pink vertical line denotes the start of the stimulation period and the following 240 frames across the stimulation (11–13 s) and post-baseline (13–11 s) period. The sampling frequency of the fNIRS system was 10 Hz (i.e., 10 data frames per second were collected).

Figure 5

Average HbO₂ concentration data is plotted in three ways: (A) Hemispheric differences: Only Left IP > Right IP. (B) Regional differences: Left IA > IP, Right IA > IP, Left IA > SA and a similar trend for Right IA > SA. (C) Task-related differences: Do and Together > Watch, for all ROIs. Together > Do for two ROIs, Right SA, and Right IP. ^*Indicate significant differences.

Figure 6

A visual representation of task-related channel activation; channel activation during the stimulation period is compared to its own baseline. HbO₂ values on Y-axis range from 0 indicated by blue to 0.1 indicated by red and shades in between. During Watch condition (A), channels 11, 23, and 24 representing the STS region are more active than other channels. Multichannel activation during the Do and Together condition vs. the Watch condition (B,C) vs. (A). During the Together condition (C), right channels 14, 15, 16, and 18 are more active vs. Do (B).