Determining monkey free choice long before the choice is made: the principal role of prefrontal neurons involved in both decision and motor processes

When choices are made freely, they might emerge from pre-existing neural activity. However, whether neurons in the prefrontal cortex (PF) show this anticipatory effect and, if so, in which part of the process they are involved is still debated. To answer this question, we studied PF activity in monkeys while they performed a strategy task. In this task when the stimulus changed from the previous trial, the monkeys had to shift their response to one of two spatial goals, excluding the one that had been previously selected. Under this free-choice condition, the prestimulus activity of the same neurons that are involved in decision and motor processes predicted future choices. These neurons developed the same goal preferences during the prestimulus presentation as they did later in the decision phase. In contrast, the same effect was not observed in motor-only neurons and it was present but weaker in decision-only neurons. Overall, our results suggest that the PF neuronal activity predicts upcoming actions mainly through the decision-making network that integrate in time decision and motor task aspects

Interference between space and time estimations: from behavior to neurons

Influences between time and space can be found in our daily life in which we are surrounded by numerous spatial metaphors to refer to time. For instance, when we move files from one folder to another in our computer a horizontal line that grows from left to right informs us about the elapsed and remaining time to finish the procedure and, similarly, in our communication we use several spatial terms to refer to time. Although with some differences in the degree of interference, not only space has an influence on time but both magnitudes influence each other. Indeed, since our childhood our estimations of time are influenced by space even when space should be irrelevant and the same occurs when estimating space with time as distractor. Such interference between magnitudes has also been observed in monkeys even if they do not use language or computers, suggesting that the two magnitudes are tightly coupled beyond communication and technology. Imaging and lesion studies have indicated that same brain areas are involved during the processing of both magnitudes and have suggested that rather than coding the specific magnitude itself the brain represents them as abstract concepts. Recent neurophysiological studies in prefrontal cortex, however, have shown that the coding of absolute and relative space and time in this area is realized by independent groups of neurons. Interestingly, instead, a high overlap was observed in this same area in the coding of goal choices across tasks. These results suggest that rather than during perception or estimation of space and time the interference between the two magnitudes might occur, at least in the prefrontal cortex, in a subsequent phase in which the goal has to be chosen or the response provided

Learning the meaning of new stimuli increases the cross-correlated activity of prefrontal neurons

The prefrontal cortex (PF) has a key role in learning rules and generating associations between stimuli and responses also called conditional motor learning. Previous studies in PF have examined conditional motor learning at the single cell level but not the correlation of discharges between neurons at the ensemble level. In the present study, we recorded from two rhesus monkeys in the dorsolateral and the mediolateral parts of the prefrontal cortex to address the role of correlated firing of simultaneously recorded pairs during conditional motor learning. We trained two rhesus monkeys to associate three stimuli with three response targets, such that each stimulus was mapped to only one response. We recorded the neuronal activity of the same neuron pairs during learning of new associations and with already learned associations. In these tasks after a period of fixation, a visual instruction stimulus appeared centrally and three potential response targets appeared in three positions: right, left, and up from center. We found a higher number of neuron pairs significantly correlated and higher cross-correlation coefficients during stimulus presentation in the new than in the familiar mapping task. These results demonstrate that learning affects the PF neural correlation structure

Independent coding of absolute duration and distance magnitudes in the prefrontal cortex

The estimation of space and time can interfere with each other, and neuroimaging studies have shown overlapping activation in the parietal and prefrontal cortical areas. We used duration and distance discrimination tasks to determine whether space and time share resources in prefrontal cortex (PF) neurons. Monkeys were required to report which of two stimuli, a red circle or blue square, presented sequentially, were longer and farther, respectively, in the duration and distance tasks. In a previous study, we showed that relative duration and distance are coded by different populations of neurons and that the only common representation is related to goal coding. Here, we examined the coding of absolute duration and distance. Our results support a model of independent coding of absolute duration and distance metrics by demonstrating that not only relative magnitude but also absolute magnitude are independently coded in the PF

Neural Intrinsic timescales in the macaque dorsal premotor cortex predict the strength of spatial response coding

Our 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

Coding of self and other's future choices in dorsal premotor cortex during social interaction

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. Understanding others’ intentions is essential to successful primate social life. Cirillo et al. explore the role of dorsal premotor cortex (PMd) in discriminating between self and others’ behavior while macaques interacted with humans. They show that the majority of neurons encoding the future choice did so selectively for the monkey or the human agent. PMd thus differentiates self from others’ behavior, leading to independent representations of future actions

role of the social actor during social interaction and learning in human monkey paradigms

Abstract The social interactions between primates is drawn by their ability to predict others' behaviours, to learn from others' actions and to represent others' intentions. It allows them to extract information by observation to understand which action is leading to which outcome and to maximize the efficiency of their own future behaviours. These processes have mainly been investigated studying non-human primates observing conspecifics, but more recently an increasing body of work has adopted a human-monkey paradigm, and some have now convincingly shown that macaque monkeys understand human choices, consider them and can act accordingly. Two main hypotheses have been developed to explain macaque monkeys' ability to learn from humans: 1) the similarity between the behaviours of both species 2) the presence of a non-ambiguous link between the observed action and its outcome. Based on the literature examined the recent evidence appears to supports the second. The non-social observational learning, meaning the learning by observation of an inanimate agent, can be a powerful tool to understand the mechanisms underlying the social interactions

Neuronal modulation in the prefrontal cortex in a transitive inference task: evidence of neuronal correlates of mental schema management

When informed that A > B and B > C, humans and other animals can easily conclude that A > C. This remarkable trait of advanced animals, which allows them to manipulate knowledge flexibly to infer logical relations, has only recently garnered interest in mainstream neuroscience. How the brain controls these logical processes remains an unanswered question that has been merely superficially addressed in neuroimaging and lesion studies, which are unable to identify the underlying neuronal computations. We observed that the activation pattern of neurons in the prefrontal cortex (PFC) during pair comparisons in a highly demanding transitive inference task fully supports the behavioral performance of the two monkeys that we tested. Our results indicate that the PFC contributes to the construction and use of a mental schema to represent premises. This evidence provides a novel framework for understanding the function of various areas of brain in logic processes and impairments to them in degenerative, traumatic, and psychiatric pathologies. SIGNIFICANCE STATEMENT: In cognitive neuroscience, it is unknown how information that leads to inferential deductions are encoded and manipulated at the neuronal level. We addressed this question by recording single-unit activity from the dorsolateral prefrontal cortex of monkeys that were performing a transitive inference (TI) task. The TI required one to choose the higher ranked of two items, based on previous, indirect experience. Our results demonstrated that single-neuron activity supports the construction of an abstract, mental schema of ordered items in solving the task and that this representation is independent of the reward value that is experienced for the single items. These findings identify the neural substrates of abstract mental representations that support inferential thinking

Monkeys Monitor Human Goals in a Nonmatch-to-Goal Interactive Task

We designed a new task, called nonmatch-to-goal, to study the ability of macaque monkeys to interact with humans in a rule-guided paradigm. In this task the monkeys were required to choose one of two targets, from a list of three. For each choice, they were required to switch from their choice on the previous trial to a different one. In a subset of trials the monkeys observed a human partner performing the task. When the human concluded his turn, the monkeys were required to switch to a new goal discarding the human's previous goal. We found that monkeys were very skillful in monitoring goals, not only of their own choice by also those of their human partner. They showed also a surprising ability to coordinate their actions, taking turns with the human partner, starting and stopping their own turn following the decision of the human partner in the task