Mapping the information flow from one brain to another during gestural communication

Abstract

Both the putative mirror neuron system (pMNS) and the ventral medial prefrontal cortex (vmPFC) are deemed important for social interaction: the pMNS because it supposedly "resonates" with the actions of others, the vmPFC because it is involved in mentalizing. Strictly speaking, the resonance property of the pMNS has never been investigated. Classical functional MRI experiments have only investigated whether pMNS regions augment their activity when an action is seen or executed. Resonance, however, entails more than only "going on and off together". Activity in the pMNS of an observer should continuously follow the more subtle changes over time in activity of the pMNS of the actor. Here we directly explore whether such resonance indeed occurs during continuous streams of actions. We let participants play the game of charades while we measured brain activity of both gesturer and guesser. We then applied a method to localize directed influences between the brains of the participants: between-brain Granger-causality mapping. Results show that a guesser's brain activity in regions involved in mentalizing and mirroring echoes the temporal structure of a gesturer's brain activity. This provides evidence for resonance theories and indicates a fine-grained temporal interplay between regions involved in motor planning and regions involved in thinking about the mental states of others. Furthermore, this method enables experiments to be more ecologically valid by providing the opportunity to leave social interaction unconstrained. This, in turn, would allow us to tap into the neural substrates of social deficits such as autism spectrum disorder.

Fig. 1.

Between-brain Granger causality during active guessing. (A) Time series X in the guesser's brain is stimulus-aligned with Y in the gesturer's brain. The fixation periods between words (blue) are discarded. The guesser typically responded before the recorded 90 s. Response (red) and postresponse (gray) periods were thus removed. 15 TR at onset and 5 TR at offset of each guessing period were trimmed to remove transients. (B) Two regressions are compared at autoregressive order 3 (Materials and Methods): one including only the past of X itself, and one additionally considering the past of Y. The residual error (variance) reduction from σ²(ε) to σ²(ε′) quantifies how much Y G-causes X. (C) Reverse regressions are compared, and differential, directed influences exist if one variable helps more in predicting the other (SI Discussion).

Fig. 2.

Results of second-level bbGCM. Granger analyses executed separately for the left and right seed are shown together. The right side represents the guesser's brain showing t values of the paired t test between gesturer→guesser and guesser→gesturer G causality (random effects, n = 18). Upper four rows: differential G causality originating from the seeds on the left. Bottom row: summary of all seeds (solid colors, left) and bbGCMs (right) with an outline of the pMNS according to a traditional GLM (33) for visual orientation. BbGCM maps are statistically thresholded at P < 0.05 corrected for multiple comparisons by using a Monte Carlo simulation-based cluster-size threshold adjustment (44, 45). MTG, middle temporal gyrus; PMd, dorsal premotor cortex; PMv, ventral premotor cortex; LH, left hemisphere; RH, right hemisphere.

Fig. 3.

Specificity of G causality. (A) t values for (gesturer→passive observer) − (passive observer→gesturer) differential G causality. (B) Same as A but for the original active guessing condition as in Fig. 2. (C) Paired t test of B–A. (D) t values for (gesturer→random guesser) − (random guesser→gesturer) differential G causality. (E) Paired t test for B–D. All maps are statistically thresholded at P < 0.05 corrected for multiple comparisons by using a Monte Carlo simulation-based cluster-size threshold adjustment (44, 45), and represent the summary of the results for the eight seed regions. See Figs. S1–S5 for similar maps separate for each seed.