Altered activation in the action observation system during synchronization in high loneliness individuals

Abstract

Lonely people tend to evaluate social exchanges negatively and to display difficulties in interactions. Interpersonal synchronization is crucial for achieving positive interactions, promoting affinity, closeness, and satisfaction. However, little is known about lonely individuals' ability to synchronize and about their brain activity while synchronizing. Following the screening of 303 participants, we recruited 32 low and 32 high loneliness participants. They were scanned while engaged in movement synchronization, using a novel dyadic interaction paradigm. Results showed that high loneliness individuals exhibited a reduced ability to adapt their movement to their partner's movement. Intriguingly, during movement adaptation periods, high loneliness individuals showed increased activation in the action observation (AO) system, specifically in the inferior frontal gyrus and the inferior parietal lobule. They did not show increased activation in the dorsomedial prefrontal cortex, which in the context of synchronization was suggested to be related to gap-monitoring. Based on these findings, we propose a model according to which lonely people may require stronger activation of their AO system for alignment, to compensate for some deficiency in their synchronization ability. Despite this hyperactivation, they still suffer from reduced synchronization capacity. Consequently, synchronization may be a relevant intervention area for the amelioration of loneliness.

Keywords: inferior frontal gyrus; inferior parietal lobule; interpersonal synchronization; mirror neuron system; social interaction.

Fig. 1

Illustration of the task design.

Fig. 2

Example of the zero-lag correlation scores calculated over time for one dyad. The blocks of random condition (left), free condition (middle), and sync condition (right) are presented. The X axis represents the time in seconds, and the Y axis is the zero-lag correlation score.

Fig. 3

Zero-lag synchronization periods parameter selection. First, the zero-lag correlation score threshold was identified using the median zero-lag correlation score in the sync condition (0.5). Then the zero-lag synchronization periods score was identified for all possible combinations of the three parameters—the zero-lag correlation score (0.5), synchronization durations, and maximal intermission. This was calculated for the sync, free, and random conditions. The goal was to identify a combination of values that best discriminates the sync or free conditions from the random condition. The charts display a “heat map” of the difference in zero-lag synchronization periods score between A) the sync and random condition and B) the free and random condition, for each combination of synchronization durations (in the y axis) and maximal intermission (in the x axis). Larger differences are yellow; smaller differences are blue. The best discrimination between the free and random condition (the largest difference in zero-lag synchronization periods) is marked in the red ellipse. The best discrimination between the sync and random condition (the largest difference in zero-lag synchronization periods) is marked in the blue ellipse. The selected value is based on a local maximum of discrimination in the sync > rand conditions and is marked by a dotted blue ellipse.

Fig. 4

High loneliness group had a lower following score in the sync condition. Following score was higher in the sync condition, compared to free and random condition. Error bars = 95% confidence level (cl).

Fig. 5

Brain activation in the sync condition > random condition contrast, during the total run duration, across loneliness groups. Contrast thresholded at P < 0.001 for the illustration. MNI coordinates of axial/coronal/sagittal view—(5, −40, 40).

Fig. 6

Brain activation in the free condition > random condition contrast, during the total run duration, across loneliness groups. Contrast thresholded at P < 0.001 for the illustration. MNI coordinates of axial/coronal/sagittal view—(5, −40, 40).

Fig. 7

Brain activation in the sync > random following periods contrast, thresholded at P < 0.001 for illustration. MNI coordinates of axial/coronal/sagittal view—(5, −40, 40).

Fig. 8

Whole-brain analysis of zero-lag synchronization periods in the sync > random contrast thresholded at P < 0.001 for illustration. MNI coordinates of axial/coronal/sagittal view—(5, −40, 40).

Fig. 9

High loneliness group presents a higher activation in the lIFG and rIPL during following periods. Error bars = 95% confidence level (cl).

Fig. 10

Proposed model of impaired synchronization in high loneliness individuals. The gap-monitoring system may be functioning properly; however, there appears to be hyperactivation of the AO system, potentially to compensate for the impaired ability. Despite this hyperactivation, lonely individuals still experience difficulties in adapting their movement.