The role of basal ganglia in motivational processes has been under scrutiny in recent decades, with increasing evidence from clinical studies of cognitive and motivational deficits in patients with basal ganglia lesions. Tonically active neurons (TANs), the presumed striatal cholinergic interneurons, could be important actors in integrating and relaying motivational information arising from various modalities. Their multiphasic responses to rewards and to conditioned stimuli associated with reward conferred them a role in limbic processes. They are also modulated by a task's motor aspect. Recent studies suggest they are influenced by the context in which behavioral responses are expressed. To investigate the role of TANs in motor-limbic interaction processes, we recorded 169 TANs in the striatum of two monkeys performing a motivational task, in which they had to develop a variable force to receive different amounts of reward in response to visual stimuli. Our results reveal new features of TANs response properties. First, TANs usually responded either by a pause or an elevation of discharge rate to the visual cues and the reward, with few neurons combining both pause and rebound. Second, the elevations of discharge rate after the cues were most sensitive to the least valuable (high force or small reward) task conditions. Finally, the responses of TANs to the visual cues were time locked on the onset of the animal's movement. TANs' population and responses could thus play a role in signaling less attractive situations, those with either a high motor demand and/or small reward.

Humans and animals must evaluate the costs and expected benefits of their actions to make adaptive choices. Prior studies have demonstrated the involvement of the basal ganglia in this evaluation. However, little is known about the role of the external part of the globus pallidus (GPe), which is well positioned to integrate motor and reward-related information, in this process. To investigate this role, the activity of 126 neurons was recorded in the associative and limbic parts of the GPe of two monkeys performing a behavioral task in which different levels of force were required to obtain different amounts of liquid reward. The results first revealed that the activity of associative and limbic GPe neurons could be modulated not only by cognitive and limbic but also motor information at the same time, both during a single period or during different periods throughout the trial, mainly in an independent way. Moreover, as a population, GPe neurons encoded these types of information dynamically throughout the trial, when each piece of information was the most relevant for the achievement of the action. Taken together, these results suggest that GPe neurons could be dedicated to the parallel monitoring of task parameters essential to adjusting and maintaining goal-directed behavior.

Recent studies have shown that neuronal stability over time can be estimated by the structure of the spike-count autocorrelation of neuronal populations. This estimation, called the intrinsic timescale, has been computed for several cortical areas and can be used to propose a cortical hierarchy reflecting a scale of temporal receptive windows between areas. In this study, we performed an autocorrelation analysis on neuronal populations of three basal ganglia (BG) nuclei, including the striatum and the subthalamic nucleus (STN), the input structures of the BG, and the external globus pallidus (GPe). The analysis was performed during the baseline period of a motivational visuomotor task in which monkeys had to apply different amounts of force to receive a different amount of reward. We found that the striatum and the STN have longer intrinsic timescales than the GPe. Moreover, our results allow for the placement of these subcortical structures within the already-defined scale of cortical temporal receptive windows. Estimates of intrinsic timescales are important in adding further constraints in the development of computational models of the complex dynamics among these nuclei and throughout cortico-BG-thalamo-cortical loops.

The understanding of the electrophysiological properties of the subthalamic nucleus (STN) neurons is crucial since it represents the main target of deep brain stimulation for the treatment of Parkinson's Disease and obsessive compulsive disorders. The study of its nonmotor properties could shed light on the cognitive and motivational alterations possibly encountered after stimulation. In this study, we recorded the activity of STN neurons in two male behaving monkeys (Macaca mulatta) while they performed a visuomotor motivational task in which visual cues indicated which amount of force was required to obtain which amount of reward. Our results evidenced force-and reward-modulated neurons. After the occurrence of the visual stimuli, the force-modulated neurons mainly fired when a high effort was required. Differently, the activity of the population of reward-modulated neurons encoded the motivational value of the stimuli. This population consisted of neurons increasing or decreasing their activity according to the motivational ranking of the task conditions. Both populations could play complementary roles, one in the implementation of the difficulty of the action and the other in enhancing or slowing its execution based on the subjective value of each conditions. SIGNIFICANT STATEMENTAn increasing number of studies confers a role to the subthalamic nucleus (STN) in motivational and reward-related processes. However, the electrophysiological bases of such properties at the neuronal level remains unclear. The present study investigated the modulation of STN neuronal activity in monkeys performing a motivational task in which the force to produce and the reward obtained were manipulated. We found two main populations of neurons, one modulated by the effort required and the other integrating the motivational subjective value of the stimuli. This last population could help at improving decision-making to act or not, depending on the subjective value set by the motivational context. This highlights the pivotal role of STN in valuation of cost/benefit for decision-making processes.

Observational learning has been investigated in monkeys mainly using conspecifics or humans as models to observe. Some studies attempted to clarify the social agent’s role and to test whether non-human primates could learn from observation of a non-social agent, usually mentioned as a ‘ghost display’ condition, but they reported conflicting results. To address this question, we trained three rhesus monkeys in an object-in-place task consisting of the presentation of five subsequent problems composed of two objects, one rewarded and one unrewarded, for six times, or runs. Three types of learning conditions were tested. In the individual learning condition, the monkeys performed the first run, learned from it and improved their performance in the following runs. In the social and non-social learning conditions, they observed respectively a human model and a computer performing the first run and learned by the observation of their successes or errors. In all three conditions, the monkeys themselves received the reward after correct choices only. One-trial learning occurred in all three conditions. The monkeys performed over chance in the second run in all conditions, providing evidence of non-social observational learning with differential reward in macaque monkeys using a “ghost display” condition in a cognitive task.

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Recent studies have shown that temporal stability of the neuronal activity over time can be estimated by the structure of the spike-count autocorrelation of neuronal populations. This estimation, called the intrinsic timescale, has been computed for several cortical areas and can be used to propose a cortical hierarchy reflecting a scale of temporal receptive windows between areas. In this study, we performed an autocorrelation analysis on neuronal populations of three basal ganglia (BG) nuclei, including the striatum and the subthalamic nucleus (STN), the input structures of the BG, and the external globus pallidus (GPe). The analysis was performed during the baseline period of a motivational visuomotor task in which monkeys had to apply different amounts of force to receive different amounts of reward. We found that the striatum and the STN have longer intrinsic timescales than the GPe. Moreover, our results allow for the placement of these subcortical structures within the already-defined scale of cortical temporal receptive windows. Estimates of intrinsic timescales are important in adding further constraints in the development of computational models of the complex dynamics among these nuclei and throughout cortico-BG-thalamo-cortical loops.