Report

Teaser, summary, work performed and final results

Periodic Reporting for period 2 - HUMO (What is everybody doing? Social prediction, categorization, and monitoring in the Prefrontal Cortex of the Macaque adopting a new human-monkey (H-M) interactive paradigm.)

Teaser

Primates live in social groups in which they face cognitive problems that they must learn to deal with if they want to survive and procreate. They need to understand the meaning of other individuals’ behavioural signs and they need to learn and maintain in memory the...

Summary

Primates live in social groups in which they face cognitive problems that they must learn to deal with if they want to survive and procreate. They need to understand the meaning of other individuals’ behavioural signs and they need to learn and maintain in memory the knowledge of their previous interactions with their group mates. All this knowledge is needed to deal with the dominant status of other individuals and to develop alliance in the competitive-cooperative “social field” in which they live. In their “social field” primates need to: (1) recognize other individuals; (2) understand and predict their behaviour; (3) remember the previous interaction with them to develop a direct relationship with them and (4) understand third party relationships. This knowledge enables to make predictions on what the group mates are going to do in a variety of social contexts. It can be also advantageous to assign the group mates to cognitive categories related to kinship based on long term affiliation, cooperative or uncooperative behaviour, or to dominance categories based on their dominance rank. Why is it important to study the Frontal Pole cortex (FPC), area 10, in monkeys?
The FPC in humans has a homologous area in other primates, but not in other mammals that means that the frontal pole of non-human primates and humans derives from a common ancestor and therefore cannot be studied by adopting other animal models. In humans, the Frontal Pole continues to develop during childhood and adolescence and it has been suggested that its abnormal development might result in a variety of disorders such as autism spectrum disorders, attention deficit and hyperactivity disorder (ADHD), and schizophrenia.
In the first part of our project, we are recording the activity of the neurons of the FPC in the context of a social interactive task, specifically in a task requiring both the monitoring and the evaluation of the choices of other agents. Elucidating the function of area 10 can be crucial to understand the neural basis of social cognition and also to understand its importance in giving an evolutionary advantage to primates.
We are also testing the hypothesis that the monitoring role of this area can have a role in learning. Its signal could implement a mechanism for single-trial learning, both for individual learning, and likely also for observation learning. Single-trial learning can be considered a unique primate ability. We believe that the representation of goals around the time of the feedback of an action could contribute, in the FPC, to create the necessary linkage between learned events and outcome (correct and errors) for generating fast learning in one trial.
This hypothesis is in line with the result of a past neuropsychological study that showed that monkeys with PFC lesions were impaired in the one trial learning typical of object-in-place scenes task. In this task, monkeys see a series of images in the background, called scenes. Two letters are presented always in the same place for each scene and many scenes are sequentially presented with different letters. The monkey’s task is to learn which letter of the two presented are correct in each scene. To understand the role of FPC in learning we are currently recording in area 10 of two monkeys during an object-in-place scenes learning task to investigate the neural correlate of learning based on single events. We are also interested in the observational learning aspect that is the neural substrate of learning from other individuals as a human agent or a computer.

Work performed

In behavioural neurophysiology we correlate the neural activity of single neurons with the behavior of an animal that performs a task in a very controlled experimental setup. In this project we are performing a neurophysiological experiment using behaving animals, and particularly non-human primates, that requires an extensive period of training. Thus, the beginning of the project started with the habituation of three macaque monkeys to the experimenter they will work with and a phase of conditioning to come in the lab and begin to interact with the touchscreen.
We first trained them to perform a behavioral task, already used in the laboratory, the Non-Match-To-Goal (NMTG) task. In this task, the monkeys face a touchscreen and two objects appear. The monkeys have to choose between the two objects, the one discarded in the previous trial. The NMTG designation referred to this process, in which the requirement is to keep in memory the previous choice to reject that for an alternative goal choice in the next trial. The monkeys are also trained to perform an “interactive” version of the task. Indeed, in some trials, a human partner, set aside the monkey performing the task, performing himself some trials. After these human trials, the monkeys have to retake the turn and chose the correct target considering the human previous choice. Using this paradigm, we are able to study and compare the difference between performing and observing a task performed by another agent. Our laboratory already studied a number of cortical areas while the monkeys performed the NMTG task and continue to investigate and study other cortical areas, as the area 10, the frontal pole, the most anterior part of the primate brain, using the same paradigm to understand better the circuitry of brain areas involved in decision-making in social contexts.
The second line of the project uses a different task, because we want to address a different question. Indeed, the literature on the frontal pole is scarce. Any advance in the knowledge of the role of this area will be important, but there is at least one indication from previous studies that confers to this area a role in quick learning, that it is called “one-trial learning”. To study this process in neurophysiology, we trained the same three monkeys to perform an “Object-In-Place” (OIP) learning task. During this task, the monkeys face 5 successive scenes problems on the touchscreen. The problem requires to choose between two visual objects (alphanumeric characters) displayed on a background composed of multiple colored abstract shapes that create a unique scene for the animals. In each scene, one object is rewarded by apple sauce given to the monkey and the other object is unrewarded instead. During the first presentation of each problem, the monkeys have to choose randomly one of the two presented. Each problem is presented six times and the monkeys have to learn as quickly as possible which object of each problem is the correct one to maximize the amount of reward they receive. We also implemented different versions of the OIP task in which a human partner performed the first problems, to study the social observational learning, or in which a computer performed the first problems, to study the non-social observational learning. We collected a large amount of behavioral data and our results confirmed that the OIP task is appropriate to study the one-trial learning. Furthermore, we brought the demonstration that old-world monkeys, like rhesus macaques, can learn in one trial not only individually but also in social and non-social observational (with a computer “partner”) contexts.
Given this encouraging behavioral results, we moved forward to the electrophysiological part. Under anesthesia, all three monkeys were implanted bilaterally with 2 matrices or arrays of recording electrodes. Each matrix contained 96 electrodes. On the total of 6 implanted matrices, we recorded the activity from 4 j

Final results

In the past years few studies have focused on social cognition in monkeys (beyond the tasks studying the representation of the reward for self and others) using interactive tasks because of the intrinsic difficulties of using monkey-monkey (M-M) paradigms and many laboratories abandoned from the start the idea of pursuing this line of research or examined only very simple forms of social interactions. Moreover, previous behavioural studies have provided negative results on the ability of monkeys to learn from humans, although they could learn from conspecifics, discouraging future studies from adopting human -monkey (H-M) paradigms.
Since then, we have presented the first evidence that monkeys can learn from human models, provided that the human model received a reward through a vicarious reward mechanism and that monkeys are able to take turns with humans and monitoring the human behaviour. The paucity of M-M studies reflects two main obstacles: first the difficulty to train two monkeys to perform joint tasks, and second the difficulty to control the behaviour of one monkey as an independent variable to study the behavior of the other monkey. On the contrary, the behaviour of a human partner can be used as the independent variable to manipulate experimentally and we proposed in the project to use a H-M paradigm in which a monkey interacts with human (independent variable) to investigate in a controlled experimental set up the cognitive functions underlying social behaviour. In one previous neurophysiological study, we had shown that the Frontal Pole cortex encoded a monkey’s goals, not when they were established, but much later when the feedback about whether the goal chosen was the correct one arrived. This finding suggested that the FPC plays an important role in monitoring or evaluating the goals of our actions. The primary question to answer in this subproject is whether the monitoring activity observed in the FPC is specific to the monkeys own goals or applies to others as well.
The NMTG task, with an interactive component, was designed to study this process and to address this issue. The NTMG interactive aspect of the task will be used to test the hypothesis that FPC monitors both self-generated decisions and other agent’s decisions. The NMTG task requires the monkeys, in order to receive a reward, to switch either from their immediate previous goal or from the human partner’s goal to a new goal.