Neural activity in macaque medial frontal cortex represents others’ choices

Abstract

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.

Coding of Self and Other’s Future Choices in Dorsal Premotor Cortex during Social Interaction

“…This differs from previous research (Cisek and Kalaska, 2004) that demonstrated similar pre-movement activity patterns in both the monkey and other's trials. However, the present findings are consistent with previous reports of other-selective cells in lateral and medial frontal areas (Falcone et al, 2016(Falcone et al, , 2017. Here, we demonstrate that not all neurons in frontal areas exhibit mirror-like properties, even in a brain area widely considered to predominantly contain neurons that ''mirror'' the actions of others.…”

“…Similar to our previous studies (Falcone et al, 2016(Falcone et al, , 2017, we found agent-related cells that, during the delay period, coded which actor was performing the task. This distinction is essential for establishing turn-taking, joint action, and understanding or predicting other agents' behavior.…”

“…Social life requires the ability to understand others' behavior and predict others' intentions. Many social behaviors in monkeys are similar to those observed in humans: they can monitor each other's actions (Fujii et al, 2007;Falcone et al, 2016Falcone et al, , 2017, cooperate (Haroush and Williams, 2015), learn from observation (Falcone et al, 2012a(Falcone et al, , 2012bMonfardini et al, 2014), and show altruistic behaviors (Chang et al, 2011).…”

“…Previous reports have described neurons involved in various aspects of social understanding: ''mirror'' neurons in the ventral premotor cortex (PMv) respond to both performed and observed actions (di Pellegrino et al, 1992;Rizzolatti et al, 1996), neurons in anterior cingulate and orbitofrontal cortex respond to others' reward (Azzi et al, 2012;Chang et al, 2013), and neurons in medial frontal areas represent others' actions or intentions (Yoshida et al, 2011(Yoshida et al, , 2012Falcone et al, 2017).…”

Human and macaque pairs employ different coordination strategies in a transparent decision game

“…For maximal comparability of the human and the monkey behavior, we developed a novel Dyadic Interaction platform in which two human or nonhuman primate subjects co-act in a shared workspace while sitting face-to-face (Figure 1A, B). Joint dyadic tasks have been previously implemented in a side-by-side setting with a shared or separate workspaces for each subject 3,36,37,71,72 , or in a table-like settings with opposing subjects acting in a horizontal workspace that is not in the line of sight between the subjects' faces 73,74 . Only few studies utilized face-to-face arrangement of the subjects, using a video projector and two semitransparent mirrors virtually placing the stimuli into the shared plane 75 interests.…”