Every day we interact with the world around us in many ways, monitoring each other's actions to cooperate and learn from others. Various abilities are necessary for complex social behavior, and many of these are shared between humans and monkeys; among these abilities, monkeys indeed represent a valid model among animals to study social interaction due to the complexity of their social life and hierarchical social structures. For this reason, we want to investigate whether the Frontal Pole (FP, Broadmann Area 10), a prefrontal area involved in the monitoring of self-generated actions (Tsujimoto et al. 2010), play a role also in the monitoring of other's actions. To achieve that, we want to analyze neurophysiological data collected in the past two years from two rhesus monkeys while they performed a task interacting with a social agent.
Two monkeys were implanted with chronic arrays to record the extracellular activity of single neurons in the FP. After the implant, the monkeys performed a social variant of a Non-match-to-go task (NMTG) designed to investigate social interaction. In the classical version of the NMTG task, four different geometrical figures are presented in pairs in each trial. One of the two object was the one presented in the previous trial, while the other one was chosen between the other possible three. The rule required to select the object of the couple that was not selected in the previous trial. In the social variant the monkeys had to perform the task interacting with a human agent, alternating between the roles of actor and observer. This version of the NMTG allows the confrontation between execution and observation condition between two social agents that alternates during an interactive task. Furthermore, the monkeys performed an additional control condition during which they cooperate with an inanimate agent (a cursor moving on the screen) that mimics the action of the human agent.
Our project presents different innovative aspects. First, we aim to expand the little knowledge about the FP single cells' properties due to the shortage of neurophysiological studies which investigated this area; to date, our knowledge of FP functions comes mainly from imaging or lesion studies in human and monkeys. Neurophysiological studies of the FP are made more difficult by the inaccessibility of this area, that lies beneath the frontal sinus, making it difficult to place electrodes to directly record the neural activity. To date, only one study (Tsujimoto et al. 2010) overcome these limitations and investigated the activity of single neurons in this area. Our project stands in thematic continuity with the findings of this work, aiming to expand the study of the action monitoring from the individual to the social domain. Furthermore, differently from the previous study, the use of chronic implants and multiples electrodes allowed the collection of a wider range of neural data, not limited only to the single neurons' activity, but also to different population signals such as multi-unit activity or local field potentials. Finally, we will analyse the activity of neurons during the computer control condition, in which the monkeys interact with an inanimate agent such as a cursor moving on the screen. Using two different observational conditions, with the human agent or with the computer agent, can help to dissociate specific other-related signals from signals that could represent the inaction of the actor during the observation. This is an important control condition that lacked in our previous studies which adopted the same task to investigate interaction with a social agent.
Investigating how dedicated representation of others are formed in brain it is also very meaningful from a clinical point of view. Failure of the ability to distinguish between stimuli related to self or originating in the environment has been associated with some of the symptoms of schizophrenia. Patients with schizophrenia make errors of agency, attributing external events to themselves, or perceiving self-produced tactile stimuli as having been externally produced. In individuals with autism spectrum disorder (ASD), failure in false-belief tasks has been associated with a deficit in the process of distinguishing between two different perspectives, i.e., related to the self or to others. Studies which investigate how the representation of others are formed in the brain may then help to better understand some of these common psychiatric disorders.