Visual salience of the stop signal affects the neuronal dynamics of controlled inhibition

The voluntary control of movement is often tested by using the countermanding, or stop-signal task that sporadically requires the suppression of a movement in response to an incoming stop-signal. Neurophysiological recordings in monkeys engaged in the countermanding task have shown that dorsal premotor cortex (PMd) is implicated in movement control. An open question is whether and how the perceptual demands inherent the stop-signal affects inhibitory performance and their underlying neuronal correlates. To this aim we recorded multi-unit activity (MUA) from the PMd of two male monkeys performing a countermanding task in which the salience of the stop-signals was modulated. Consistently to what has been observed in humans, we found that less salient stimuli worsened the inhibitory performance. At the neuronal level, these behavioral results were subtended by the following modulations: when the stop-signal was not noticeable compared to the salient condition the preparatory neuronal activity in PMd started to be affected later and with a less sharp dynamic. This neuronal pattern is probably the consequence of a less efficient inhibitory command useful to interrupt the neural dynamic that supports movement generation in PMd

Neuronal activity in posterior parietal cortex area LIP is not sufficient for saccadic eye movement production

It is widely recognized that the posterior parietal cortex (PPC) plays a role in active exploration with eye movements, arm reaching, and hand grasping. Whether this role is causal in nature is largely unresolved. One region of the PPC appears dedicated to the control of saccadic eye movement—lateral intraparietal (LIP) area. This area LIP possesses direct projections to well-established oculomotor centers and contains neurons with movement-related activity. In this study, we tested whether these neurons are implicated in saccade initiation and production. The movement-related activity of LIP neurons was tested by recording these neurons while monkeys performed a countermanding task. We found that LIP neuronal activity is not different before the execution or the cancelation of commanded saccades and thereby is not sufficient for the initiation and production of saccades. Consistent with the evolutionarily late emergence of the PPC, this finding relegates the role of this PPC area to processes that can regulate but not trigger eye movements

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

Effects of reward size and context on learning in macaque monkeys

Abstract The outcome of an action plays a crucial role in decision-making and reinforcement learning processes. Indeed, both human and animal behavioural studies have shown that different expected reward values, either quantitatively or qualitatively, modulate the motivation of subjects to perform an action and, as a consequence, affect their behavioural performance. Here, we investigated the effect of different amounts of reward on the learning of macaque monkeys using a modified version of the object-in-place task. This task offers the opportunity to shape rapid learning based on a set of external stimuli that enhance an animal's accuracy in terms of solving a problem. We compared the learning of three monkeys among three different reward conditions. Our results demonstrate that the larger the reward, the better the monkey's ability to learn the associations starting with the second presentation of the problem. Moreover, we compared the present results with those of our previous work using the same monkeys in the same task but with a unique reward condition, the intermediate one. Interestingly, the performance of our animals in our previous work matched with their performance in the largest and not intermediate reward condition of the present study These results suggest that learning is mostly influenced by the reward context and not by its absolute value

The small scale functional topology of movement control: Hierarchical organization of local activity anticipates movement generation in the premotor cortex of primates.

How neurons coordinate their collective activity for behavioural control is an open question in neuroscience. Several studies have progressively proven, on various scales, that the patterns of neural synchronization change accordingly with behavioural events. However, the topological features of the neural dynamics that underlie task-based cognitive decisions on the small scale level are not understood. We analysed the multiunit activity (MUA) from a multielectrode (96 channels) array of the dorsal premotor cortex (PMd) in rhesus monkeys during a countermanding reaching task. Within the framework of graph theory, we found that in the local PMd network motor execution is preceded by the emergence of hubs of anti-correlation that are organized in a hierarchical manner. Conversely, this organization is absent when monkeys correctly inhibit programmed movements. Thus, we interpret the presence of hubs as reflecting the readiness of the motor plan and the irrevocable signature of the onset of the incoming movement

Alpha- and beta-band oscillations subserve different processes in reactive control of limb movements

The capacity to rapidly suppress a behavioral act in response to sudden instruction to stop is a key cognitive function. This function, called reactive control, is tested in experimental settings using the stop signal task, which requires subjects to generate a movement in response to a go signal or suppress it when a stop signal appears. The ability to inhibit this movement fluctuates over time: sometimes, subjects can stop their response, and at other times, they can not. To determine the neural basis of this fluctuation, we recorded local field potentials (LFPs) in the alpha (6-12 Hz) and beta (13-35 Hz) bands from the dorsal premotor cortex of 2 nonhuman primates that were performing the task. The ability to countermand a movement after a stop signal was predicted by the activity of both bands, each purportedly representing a distinct neural process. The beta band represents the level of movement preparation; higher beta power corresponds to a lower level of movement preparation, whereas the alpha band supports a proper phasic, reactive inhibitory response: movements are inhibited when alpha band power increases immediately after a stop signal. Our findings support the function of LFP bands in generating the signatures of various neural computations that are multiplexed in the brain

Vicarious Learning from Human Models in Monkeys

We examined whether monkeys can learn by observing a human model, through vicarious learning. Two monkeys observed a human model demonstrating an object–reward association and consuming food found underneath an object. The monkeys observed human models as they solved more than 30 learning problems. For each problem, the human models made a choice between two objects, one of which concealed a piece of apple. In the test phase afterwards, the monkeys made a choice of their own. Learning was apparent from the first trial of the test phase, confirming the ability of monkeys to learn by vicarious observation of human models

CONTROLLED MOVEMENT PROCESSING: EVIDENCE FOR A COMMON INHIBITORY CONTROL OF FINGER, WRIST, AND ARM MOVEMENTS

We used the behavioral task and theoretical construct of the countermanding paradigm to test whether there is any difference between the inhibitory control of the finger, wrist, and arm. Participants were instructed (primary task) to respond to a directional go signal presented at the fovea by pressing a button with either their index or middle fingers, moving a joystick with their wrists, or reaching to a stimulus on a touch screen with their arms. They were also instructed (secondary task) to withhold their responses when a stop signal was presented on 25% of trials. The participants' ability to inhibit each of the commanded movements was captured by their inhibition probability function, which describes how withholding is increasingly difficult as the delay between the go and stop signals increased. By modeling each participant's inhibition function, we estimated that the time needed to inhibit a commanded movement was about 240 ms, a variable that did not differ significantly between the three limb segments. Moreover, we found that the best-fit model of each segment's inhibition function could fit equally well the inhibition functions obtained with the other two segments. These results provide evidence that the upper limb segments share a common inhibitory control, which may facilitate the regulation of neuronal activity within the distributed motor cortical representations and thus simplify the voluntary control of multi-segmental movements. (C) 2012 IBRO. Published by Elsevier Ltd. All rights reserved

Neural encoding of self and another agent's goal in the primate prefrontal cortex: human–monkey interactions

The primate prefrontal cortex represents both past and future goals. To investigate its role in representing the goals of other agents, we designed a nonmatch-to-goal task that involved a human-monkey (H-M) interaction. During each trial, 2 of 4 potential goal objects were presented randomly to the left or right part of a display screen, and the monkey's (or human's) task was to choose the one that did not match the object goal previously chosen. Human and monkey trials were intermixed, and each agent, when acting as observer, was required to monitor the other actor's choice to switch the object goal choice in case it became the actor on the subsequent trial. We found neurons encoding the actor, either the monkey itself or the human, neurons encoding the agent future goal position and neurons encoding the agent previous goal position. In the category of neurons encoding the human future goal, we differentiated between those encoding the future goal of both agents and those encoding only the human agent future goal. While the first one might represent a covert mental simulation in the human trials, the other one could represent a prediction signal of the other's agent choice