Joint actions (JA) are an essential component of animal behavior as they require to coordinate with others in space and time. The optimization of mutual motor adaptations must be based on the simultaneous analysis and integration of signals across multiple temporal scales. In this context, a JA motor plan has to incorporate cues specifying partners’ actions (bottom-up) and prior knowledge (top-down). Therefore, the motor system must be “prepared” to predict – from minimal kinematic cues – which effect the partner’s action will have and to rapidly integrate this data with prior information. From a neurophysiological perspective, the behavioral co-regulation emerging during JA can be reduced to a continuous and dynamic process of action selection and execution. In fact, the integration of bottom-up and top-down information to deliver the most appropriate course of action boils down to the fine equilibrium between excitatory and inhibitory signals in sensorimotor circuits. We designed a transcranial magnetic stimulation (TMS) protocol to investigate the neurophysiological fingerprints of the two inferential processes (top-down and bottom-up) naturally at play during human motor coordination.

Here we used a typical bimanual task – reaching/grasping for a bottle – and adapted it to become a unimanual JA task: the participant is asked to hold a bottle (JA) while the other member of the dyad (the confederate) has to reach either for the JA-bottle or for another bottle stabilized by a mechanical clamp (No_JA). We manipulated priors’ availability (K vs. No_K) to introduce the necessity for the participant to differently weight top-down or bottom-up processing. In summary, the confederate could reach the bottle either held by the participant (JA) or the mechanical clamp (no_JA), and the participant could either know (K) or not know (no_K) the target bottle in advance. In no_K trials, the participant could only rely on partner’s kinematic cues to decode which bottle he was pointing toward and, therefore, whether it was a JA or a no_JA trial. In K trials, by contrast, this information was provided explicitly by prior information. We use single pulse TMS to investigate corticospinal excitability (CSE) and cortical silent period (cSP) from participants’ opponens pollicis (OP). TMS was delivered at four timings: rest, onset of confederate’s movement, pre-shaping, grasping.

Our results show that JA generally produce larger CSE and longer cSPs. At the same time, the two neurophysiological indexes seem to reflect two temporally dissociable processes. CSE was modulated early on before the action started if prior information about confederate’s choice is available. Differently, cSP modulation emerged during the reaching action -regardless prior information- only when kinematic features are accessible. These two indexes could thus reflect the concurrent elaboration of contextual priors (top-down) and the online sampling of kinematic cues (bottom-up). 

Here, by showing a temporal dissociation between excitatory and inhibitory indexes and differential dependence on prior information and partner’s kinematics, we present new evidence that specific neurophysiological modulations may represent the fingerprints of the natural unfolding of top-down and bottom-up complementary inferential processes which contribute to the optimization of social motor interaction.