Neurons in the Monkey's Subthalamic Nucleus Differentially Encode Motivation and Effort

Abstract

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.

Neural underpinnings of action adaptation in the subthalamic nucleus

“…As detailed above, all patients were studied ON medication and immediately after DBS surgery to mitigate this effect. Furthermore, there is a vast literature beyond STN LFP recordings in PD patients demonstrating neural correlates of force production in the basal ganglia including non-invasive recordings with functional magnetic resonance imaging in healthy people 46, 47 , invasive electrophysiological recordings in healthy non-human primates 48, 49 and invasive electrophysiological recordings in humans with neurological disorders other than PD 50 . In addition, cortical beta oscillations have been shown to reflect action adaptation in healthy humans using electroencephalography 51, 52 .…”

Psychological Resilience in Adolescence as a function of Genetic Risk for Major Depressive Disorder and Alzheimer’s Disease

“…The first index gauged fine-tuning of task-specific functional brain architecture. The second index reflected context-specificity in neural coding (i.e., inhibitory control-incentive processing differentiation), a cross-species marker of adaptive functioning and resilience (54)(55)(56). Partial least squares analysis (PLS) was subsequently applied to parcel-specific "flexibility" indices to identify connectomic features linked to resilience and/or genetic risk for AD/MDD.…”

Neural dynamics underlying self-control in the primate subthalamic nucleus

“…Electrophysiological recordings collected from the STN of these patients have shown low-frequency oscillations (<12Hz) and spiking activities related to various aspects of reward processing, with neural signals modulated by the magnitude of monetary reward and cost-benefit value attribution (Fumagalli et al, 2015; Justin Rossi et al, 2017; Zénon et al, 2016). In non-human animals, the ability of the STN to represent the subjective desirability of actions has also been evidenced by studies that show neurons firing as a function of the expected reward and the associated effort cost (Breysse et al, 2015; Espinosa-Parrilla et al, 2013; Nougaret et al, 2022). Although substantial effort has been directed to elucidate the role of the STN in valuation-related processes at the time of decision-making (Cavanagh et al, 2011; Coulthard et al, 2012; Frank et al, 2007) and in movement incentive (Nougaret et al, 2022; Tan et al, 2015; Zénon et al, 2016), much less attention has been paid to STN involvement in the computation of temporally discounted value during the post-instruction delay period, when behavioral inhibition must be sustained patiently over time.…”

“…Electrophysiological recordings collected from the STN of these patients have shown low-frequency oscillations (<12Hz) and spiking activities related to various aspects of reward processing, with neural signals modulated by the magnitude of monetary reward and cost-benefit value attribution (Fumagalli et al, 2015;Justin Rossi et al, 2017;Zénon et al, 2016). In non-human animals, the ability of the STN to represent the subjective desirability of actions has also been evidenced by studies that show neurons firing as a function of the expected reward and the associated effort cost (Breysse et al, 2015;Espinosa-Parrilla et al, 2013;Nougaret et al, 2022).…”

“…Although substantial effort has been directed to elucidate the role of the STN in valuation-related processes at the time of decision-making (Cavanagh et al, 2011;Coulthard et al, 2012;Frank et al, 2007) and in movement incentive (Nougaret et al, 2022;Tan et al, 2015;Zénon et al, 2016), much less attention has been paid to STN involvement in the computation of temporally discounted value during the post-instruction delay period, when behavioral inhibition must be sustained patiently over time. In addition, it is still unclear how these roles for STN in cost-benefit valuation and motivational processing relate to the known organization of this nucleus into anatomically and functionally distinct territories (Alexander et al, 1990;Nambu et al, 2002;Parent and Hazrati, 1995).…”