Neural representation of others during action observation in posterior medial prefrontal cortex

Abstract

Making decisions based on the actions of others is critical to daily interpersonal interactions. We investigated the representations of other’s actions at single neural level in posterior medial prefrontal cortex (pmPFC) in two monkeys during the observation of actions of another agent, in a social interaction task. Each monkey separately interacted with a human partner. The monkey and the human alternated turns as actor and observer. The actor was required to reach one of two visual targets, avoiding the previously chosen target, while the observer monitored that action. pmPFC neurons decoupled in most cases self from others during both the execution and the observation of explicit actions. pmPFC neurons showed selective directional tuning specific for the agent who was executing the task. Moreover, we assessed the relationship of the response coding between the periods immediately before and after the action, by using a cross-modal decoding analysis. We found neural network stability from the action anticipation period to the observation of other’s actions, suggesting a strong relationship between the anticipation and the execution of an action. When the monkey was the actor, the population coding appeared dynamic, possibly reflecting a goal-action transformation unique to the monkey’s own action execution.

Simultaneous oscillatory encoding of “hot” and “cold” information during social interactions in the monkey medial prefrontal cortex

“…The near-perfect performance of the monkeys after both the Good and Bad agents’ turns confirms the monkeys’ ability to effectively remember the last choice made by the human agent during the observer role. Thus, while the early anti-correlated beta-gamma activity can be considered a neural correlate of the anticipated target choice during the delay period, as shown in our previous studies, 14 , 15 the opposite beta-gamma modulation, which lasts longer during partner reaching, may still reflect memory of the partner choice. 50 The observation that the beta band encoded information about the target chosen by the human partner during the beginning of the subsequent trial provides further support for this hypothesis.…”

“…In our previous work, during the Nonmatch-to-goal task, mPFC single neurons showed a robust activation both when monkeys performed the task and observed a human agent performing the task. 14 , 15 Here, for all the artifact-free channels, we checked whether the voltage at targets presentation differed between the two conditions in which the monkey was the Actor and the Observer. Each channel was considered visually selective if its voltage was modulated by > 2SD from baseline for 50 ms immediately after the targets were presented (see STAR Methods ; Figure 3 B).…”

“…In recent neurophysiological studies, including our own, it has been shown that the medial prefrontal cortex (mPFC) has neurons that play a role in social behavior, 7 , 14 , 15 , 16 , 17 monitoring reward outcomes and values, 7 , 17 , 18 , 19 and in representations of self and other. 20 This brain area is also associated with more analytical cognitive functions including decision-making, 21 , 22 conflict monitoring, 23 working memory (WM), 24 , 25 , 26 attention, 27 , 28 and in the selection of response tactics.…”

“…In this task, monkeys switched the Actor and the Observer social role with a human agent in different trials. 14 , 15 Critically, the monkeys could be engaged in two distinct types of interaction depending on the human partner they were interacting with: the ‘Good Agent’ who always made correct choices, and the ‘Bad Agent’ who always chose incorrectly. This allowed for the investigation of the monkeys’ interactions in different relational contexts with different human partners that could either align with or conflict with the monkeys’ own goals and intentions.…”

Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex

“…Such persistent activity has also been observed in relation to several other cognitive processes in addition to short-term memory 13 . However, further evidence has challenged this view by demonstrating a more dynamic coding than previously thought 23,24,28,29,71 . More recent studies have also shown that these coding schemes are not even mutually exclusive in a given brain area, but rather that they can coexist 48 and be associated with distinct neuronal populations [50][51][52] , undermining the idea of rigid categorical separation and laying the foundations for conceiving mixed and heterogeneous representations in the prefrontal cortex.…”