Developmental Differences in Cortical Activation During Action Observation, Action Execution and Interpersonal Synchrony: An fNIRS Study

Abstract

Interpersonal synchrony (IPS) is an important everyday behavior influencing social cognitive development; however, few studies have investigated the developmental differences and underlying neural mechanisms of IPS. functional near-infrared spectroscopy (fNIRS) is a novel neuroimaging tool that allows the study of cortical activation in the presence of natural movements. Using fNIRS, we compared cortical activation patterns between children and adults during action observation, execution, and IPS. Seventeen school-age children and 15 adults completed a reach to cleanup task while we obtained cortical activation data from bilateral inferior frontal gyrus (IFG), superior temporal sulcus (STS), and inferior parietal lobes (IPL). Children showed lower spatial and temporal accuracy during IPS compared to adults (i.e., spatial synchrony scores (Mean ± SE) in children: 2.67 ± 0.08 and adults: 2.85 ± 0.06; temporal synchrony scores (Mean ± SE) in children: 2.74 ± 0.06 and adults: 2.88 ± 0.05). For both groups, the STS regions were more activated during action observation, while the IFG and STS were more activated during action execution and IPS. The IPS condition involved more right-sided activation compared to action execution suggesting that IPS is a higher-order process involving more bilateral cortical activation. In addition, adults showed more left lateralization compared to the children during movement conditions (execution and IPS); which indicated greater inhibition of ipsilateral cortices in the adults compared to children. These findings provide a neuroimaging framework to study imitation and IPS impairments in special populations such as children with Autism Spectrum Disorder.

Keywords: development; fNIRS; imitation; interpersonal synchrony; lateralization.

Figure 1

Experimental setup (A,B) and task sequence (C). 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 general linear model (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 the start of stimulation. Data have been averaged across trials and participants.

Figure 4

Regional differences (A: Watch; B: Do; C: Together) in average HbO₂ concentration. *Indicates a significant difference between regions.

Figure 5

Task-related and hemispheric differences for typically developing (TD) child (A) and adult (B) in average HbO₂ concentration. *Indicates a significant difference. Arrows highlight hemispheric differences.

Figure 6

Group differences in average HbO₂ concentration. *Indicates a significant difference between groups.

Figure 7

A visual representation of task-related, hemispheric, and group differences in channel activation (HbO₂) during the stimulation period compared to its own baseline in both groups and all conditions.