Neural mechanisms of human communicative innovations

Even when communicative conventions are not available (e.g. a common language in a noisy pub), humans can quickly generate novel communicative actions and grasp their implied meaning at the first occurrence. Given the vast number of possible causal structures (meanings) underlying a novel communicative action, how can a communicator select a communicative action whose intended meaning is likely to be recognized by an addressee, on its first instance? In this study, we build on the hypothesis that the communicator solves this action selection problem by predicting the intention that the addressee is likely to attribute to the communicator’s action (1), using the communicator’s own intention recognition system, and taking knowledge and beliefs of the addressee into account. We used magnetoencephalography (MEG) to capture the neural dynamics evoked during a live interaction between pairs of subjects. Each pair (N=24) was asked to jointly create a goal configuration of two geometrical tokens, using the movements of the tokens on a game board as the only available communicative channel. Following our hypothesis, we focused on cerebral processes with spatial and spectral features shared across planning and understanding the communicative action, isolating neural resources common to both communicative elements, and independent from sensory inputs and motor outputs. Communication-related effects were also distinguished from activity evoked during a control task involving the same stimuli, responses, joint attention, and between-subjects dependencies, but no communicative necessities. During communicative interactions, two brain regions exhibited significantly stronger power, most pronounced around 55-85 Hz, resulting from broad-band up-regulated neural activity in ventromedial prefrontal cortex and the right temporal cortex. This effect was strongly right-lateralized, emerged already before the occurrence of a particular communicative problem, and well before the observation of communicative actions. These findings sharpen our understanding of the mechanisms supporting human communicative behavior by showing how portions of temporal and ventral prefrontal cortex support both production and comprehension of novel communicative actions with neural activity that predate in time the occurrence of observable communicative events, offering a novel perspective on the implementation of the computations occurring during communicative behavior. 1. Noordzij ML, et al. (2009) Brain mechanisms underlying human communication. Front Hum.Neurosci. 3:14.