Brain-to-brain coupling: a mechanism for creating and sharing a social world

Abstract

Cognition materializes in an interpersonal space. The emergence of complex behaviors requires the coordination of actions among individuals according to a shared set of rules. Despite the central role of other individuals in shaping one's mind, most cognitive studies focus on processes that occur within a single individual. We call for a shift from a single-brain to a multi-brain frame of reference. We argue that in many cases the neural processes in one brain are coupled to the neural processes in another brain via the transmission of a signal through the environment. Brain-to-brain coupling constrains and shapes the actions of each individual in a social network, leading to complex joint behaviors that could not have emerged in isolation.

Figure 1. Two types of coupling

A) Stimulus-to-Brain Coupling B) Brain-to-Brain Coupling.

Figure 2

The 3 – 8 Hz rhythm of speech couples with the on-going auditory cortical oscillations that have a similar frequency band. A) Even in silence, there are on-going auditory cortical oscillations in the receiver’s brain. B) The signal-to-noise of this cortical oscillation increases when it is coupled to the auditory-only speech of the signaler. C) Finally, since in humans, the mouth moves at the same rhythmic frequency of the speech envelope, audiovisual speech can further enhance the signal-to-noise ratio of the cortical oscillation.

Figure 3. Speaker–listener brain-to-brain coupling

A) The speaker–listener neural coupling was assessed through the use of a general linear model in which the time series in the speaker’s brain are used to predict the activity in the listeners’ brains. B) The speaker–listener temporal coupling varies across brain areas. In early auditory areas (A1+) the speaker–listener brain coupling is time locked to the moment of vocalization (yellow). In posterior areas the activity in the speaker’s brain preceded the activity in the listeners’ brains (blue), whereas in the mPFC, dlPFC, and striatum the listeners’ brain activity preceded (red). C) The listeners’ behavioral scores and the extent of significant speaker–listener brain coupling was found to be strongly correlated (r = 0.54, p < 0.07). These results suggest that the stronger the neural coupling between interlocutors, the better the understanding. The extent of brain areas where the listeners’ activity preceded the speaker’s activity (red areas in Fig. 3B) provided the strongest correlation with behavior (r = 0.75, p < 0.01). These results provide evidence that prediction is an important aspect of successful communication. (Adapted from [49]).

Figure 4. Gesturer-observer brain-to-brain coupling

During gestural communication, in the game of charades, brain activity in the gesturer triggers muscle movements (gestures), that are seen by the receiver and which trigger activity in brain regions of the observer that are similar to those that caused the gestures in the gesturer. Brain-to-brain Granger causality can map such information transfer by calculating how much brain activity in the gesturer helps predict brain activity in the viewer.