Differential contribution of between and within-brain coupling to movement synchronization

Abstract

A fundamental characteristic of the human brain that supports behavior is its capacity to create connections between brain regions. A promising approach holds that during social behavior, brain regions not only create connections with other brain regions within a brain, but also coordinate their activity with other brain regions of an interaction partner. Here we ask whether between-brain and within-brain coupling contribute differentially to movement synchronization. We focused on coupling between the inferior frontal gyrus (IFG), a brain region associated with the observation-execution system, and the dorsomedial prefrontal cortex (dmPFC), a region associated with error-monitoring and prediction. Participants, randomly divided into dyads, were simultaneously scanned with functional near infra-red spectroscopy (fNIRS) while performing an open-ended 3D hand movement task consisting of three conditions: back-to-back movement, free movement, or intentional synchronization. Results show that behavioral synchrony was higher in the intentional synchrony compared with the back-to-back and free movement conditions. Between-brain coupling in the IFG and dmPFC was evident in the free movement and intentional synchrony conditions but not in the back-to-back condition. Importantly, between-brain coupling was found to positively predict intentional synchrony, while within-brain coupling was found to predict synchronization during free movement. These results indicate that during intentional synchronization, brain organization changes such that between-brain networks, but not within-brain connections, contribute to successful communication, pointing to shift from a within-brain feedback loop to a two-brains feedback loop.

Keywords: hyperscanning; interbrain coupling; movement synchronization.

FIGURE 1

(a) Task setting. Participants are seated facing each other. Each participant is holding a Razer Hydra game controller in his/her hand. The device tracks motion and orientation of hands. It is held by the participant's hand and allows any type of movement including circular movements, movement away and towards the body as well as movements to the right and left sides of the body. (b) Measures of between‐brain and intra‐brain coupling. Solid lines represent intra‐brain network and dashed lines represent between‐brain networks. Our model holds that intentional synchronization relies on between‐brain networks rather than within‐brain networks.

FIGURE 2

Illustration of the task design.

FIGURE 3

The level of behavioral synchrony, encoded by color, of a specific dyad in the different conditions during the Razer task. The x‐axis represents time, while the y‐axis represents the time lag between participants synchronized motion (i.e., lag 0 indicates no time delay between participants' synchronized movements, lag ± indicates participants performed synchronized motion with time difference). The colors represent the correlation between participants' movements. Colors scaling to deep yellow/blue indicate higher correlation, and thus, greater synchronization between individuals' movements. Red marks indicate sync periods. This graph indicates synchrony is greater during IS condition compared with all other conditions.

FIGURE 4

fNIRS channel placement against anatomical brain areas: All available channels, right‐side view (a); All available channels, frontal view (b); rIFG coverage (c); dmPFC coverage (d); and lIFG coverage (e). Channels (marked as yellow lines) are formed between Transmitters (red dots), and adjacent receivers (blue dots). The black lines indicate the approximate brain areas corresponding to each channel.

FIGURE 5

Behavioral synchrony levels between Real and Pseudo group assignment in the BB, IS, and FM conditions, for Total Sync.

FIGURE 6

Between‐brain coherence in the R.IFG and dmPFC in the IS condition, showing significant difference from back‐to‐back condition.

FIGURE 7

Predicted IBS levels between Real and Pseudo group assignment in the IS and FM conditions.

FIGURE 8

Prediction of Total Sync by WTC in each Condition in each ROI pairing.

FIGURE 9

Within‐brain levels between in the BB, IS, and FM conditions.

FIGURE 10

Prediction of Total Sync by within‐brain WTC in each Condition in each ROI pairing.

FIGURE 11

Within‐ and between‐brain coupling strength in the IS condition. Regression t‐values are represented by color coding. Positive correlations are in green, negative correlations are in red. The numbers represent regression slope values.