Two brains in action: Joint-action coding in the primate frontal cortex

Abstract

Daily life often requires the coordination of our actions with those of another partner. After 50 years (1968 -2018) of behavioral neurophysiology of motor control, the neural mechanisms that allow such coordination in primates are unknown. We studied this issue by recording cell activity simultaneously from dorsal premotor cortex (PMd) of two male interacting monkeys trained to coordinate their hand forces to achieve a common goal. We found a population of "joint-action cells" that discharged preferentially when monkeys cooperated in the task. This modulation was predictive in nature, because in most cells neural activity led in time the changes of the "own" and of the "other" behavior. These neurons encoded the joint-performance more accurately than "canonical action-related cells", activated by the action per se, regardless of the individual versus interactive context. A decoding of joint-action was obtained by combining the two brains' activities, using cells with directional properties distinguished from those associated to the "solo" behaviors. Action observation-related activity studied when one monkey observed the consequences of the partner's behavior, i.e., the cursor's motion on the screen, did not sharpen the accuracy of joint-action cells' representation, suggesting that it plays no major role in encoding joint-action. When monkeys performed with a non-interactive partner, such as a computer, joint-action cells' representation of the other (non-cooperative) behavior was significantly degraded. These findings provide evidence of how premotor neurons integrate the timevarying representation of the self-action with that of a co-actor, thus offering a neural substrate for successful visuomotor coordination between individuals.The neural bases of intersubject motor coordination were studied by recording cell activity simultaneously from the frontal cortex of two interacting monkeys, trained to coordinate their hand forces to achieve a common goal. We found a new class of cells, preferentially active when the monkeys cooperated, rather than when the same action was performed individually. These "jointaction neurons" offered a neural representation of joint-behaviors by far more accurate than that provided by the "canonical action-related cells", modulated by the action per se regardless of the individual/interactive context. A neural representation of joint-performance was obtained by combining the activity recorded from the two brains. Our findings offer the first evidence concerning neural mechanisms subtending interactive visuomotor coordination between co-acting agents.

How Task Interactivity Shapes Action Observation

“…As a final neurobiological consideration, our results highlight that the very same lvPMc, belonging to the "mirror" motor system (Rizzolatti and Sinigaglia 2016), contributes to the deciphering of motor goals beyond mere low-level movement imitation. A recent neurophysiological study on nonhuman primates (Ferrari-Toniolo et al, 2019) showed that there is a population of left premotor neurons that preferentially discharge when a monkey cooperates with a partner to achieve a motor goal, independently of the specific visual input that the monkey receives at a given moment ( Ferrari-Toniolo et al, 2019): this is in line with our suggestion that that the activity of premotor regions might be shaped by social motor experience and acquire the possibility to code higher-order "joint" motor representations.…”

Brain-to-Brain Coupling in the Gamma-Band as a Marker of Shared Intentionality

“…Interestingly, this neural mechanism has recently been reported by Thornton et al (2019), who found that the adjustment of current social behavior based on the prediction of the other's future mental state, depended on the action of the medial prefrontal cortex. Similar findings have been found in pairs of monkeys that perform cooperative tasks (Ferrari-Toniolo et al, 2019). Specifically, a unique set of dorsal premotor neurons called "joint-action cells" was found to discharge preferentially during cooperative tasks involving interactive visuomotor coordination between co-acting monkeys.…”

Mechanisms for mutual support in motor interactions

“…Our and others’ previous results suggest that this interactivity-dependent modulation of action observation might depend on a modulation of the brain activity in fronto-parietal areas 51 – 59 , see also Ref. 60 . Specifically, in the present paradigm, the left ventral premotor cortex might play a critical role 16 , because it is responsible for goal predictions for hand movements in humans 61 , 62 and non-human primates 63 , 64 .…”