SummaryOur brain continuously receives information over multiple timescales that are differently processed across areas. In this study, we investigated the intrinsic timescale of neurons in the dorsal premotor cortex (PMd) of two rhesus macaques while performing a non-match-to-goal task. The task rule was to reject the previously chosen target and select the alternative one. We defined the intrinsic timescale as the decay constant of the autocorrelation structure computed during a baseline period of the task. We found that neurons with longer intrinsic timescale tended to maintain a stronger spatial response coding during a delay period. This result suggests that longer intrinsic timescales predict the functional role of PMd neurons in a cognitive task. Our estimate of the intrinsic timescale integrates an existing hierarchical model (Murray et al., 2014), by assigning to PMd a lower position than prefrontal cortex in the hierarchical ordering of the brain areas based on neurons' timescales.

Predicting the behavior of others is a fundamental skill in primate social life. We tested the role of medial frontal cortex in the prediction of other agents’ behavior in two male macaques, using a monkey-human interactive task in which their actor-observer roles were intermixed. In every trial, the observer monitored the actor’s choice to reject it for a different one when he became the actor on the subsequent trial. In the delay period preceding the action, we identified neurons modulated by the agent’s identity, as well as a group of neurons encoding the agent’s future choice, some of which were neurons that showed differential patterns of activity between agents. The ability of these neurons to flexibly move from ‘self-oriented’ to ‘other-oriented’ representations could correspond to the “other side of the coin” of the simulative mirroring activity. Neurons that changed coding scheme, together with neurons exclusively involved in the prediction of the other agent’s choice, show a neural substrate for predicting or anticipating others’ choices beyond simulation.

Representing others' intentions is central to primate social life. We explored the role of dorsal premotor cortex (PMd) in discriminating between self and others' behavior while two male rhesus monkeys performed a non-match-to-goal task in a monkey-human paradigm. During each trial, two of four potential targets were randomly presented on the right and left parts of a screen, and the monkey or the human was required to choose the one that did not match the previously chosen target. Each agent had to monitor the other's action in order to select the correct target in that agent's own turn. We report neurons that selectively encoded the future choice of the monkey, the human agent, or both. Our findings suggest that PMd activity shows a high degree of self-other differentiation during face-to-face interactions, leading to an independent representation of what others will do instead of entailing self-centered mental rehearsal or mirror-like activities.

We investigated the spatial representation of covert attention and movement planning in monkeys performing a task that used symbolic cues to decouple the locus of covert attention from the motor target. In the three frontal areas studied, most spatially tuned neurons reflected either where attention was allocated or the planned saccade. Neurons modulated by both covert attention and the motor plan were in the minority. Such dual-purpose neurons were especially rare in premotor and prefrontal cortex but were more common just rostral to the arcuate sulcus. The existence of neurons that indicate where the monkey was attending but not its movement goal runs counter to the idea that the control of spatial attention is entirely reliant on the neuronal circuits underlying motor planning. Rather, the presence of separate neuronal populations for each cognitive process suggests that endogenous attention is under flexible control and can be dissociated from motor intention.

Rhesus monkeys performed two tasks, both requiring a choice between a red square and a blue circle. In the duration task, the two stimuli appeared sequentially on each trial, for varying durations, and, later, during the choice phase of the task, the monkeys needed to choose the one that had lasted longer. In the matching-to-sample task, one of the two stimuli appeared twice as a sample, with durations matching those in the duration task, and the monkey needed to choose that stimulus during the choice phase. Although stimulus duration was irrelevant in the matching-to-sample task, the monkeys made twice as many errors when the second stimulus was shorter. This across-task interference supports an order-dependent model of the monkeys' choice and reveals something about their strategy in the duration task. The monkeys tended to choose the second stimulus when its duration exceeded the first and to choose the alternative stimulus otherwise. For the duration task, this strategy obviated the need to store stimulus-duration conjunctions for both stimuli, but it generated errors on the matching-to-sample task. We examined duration coding in prefrontal neurons and confirmed that a population of cells encoded relative duration during the matching-to-sample task, as expected from the order-dependent errors.

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.

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Social neurophysiology has increasingly addressed how several aspects of self and other are distinctly represented in the brain. In social interactions, the self–other distinction is fundamental for discriminating one’s own actions, intentions, and outcomes from those that originate in the external world. In this paper, we review neurophysiological experiments using nonhuman primates that shed light on the importance of the self–other distinction, focusing mainly on the frontal cortex. We start by examining how the findings are impacted by the experimental paradigms that are used, such as the type of social partner or whether a passive or active interaction is required. Next, we describe the 2 sociocognitive systems: mirror and mentalizing. Finally, we discuss how the self–other distinction can occur in different domains to process different aspects of social information: the observation and prediction of others’ actions and the monitoring of others’ rewards.