Neural dynamics underlying self-control in the primate subthalamic nucleus

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Abstract

The subthalamic nucleus (STN) is hypothesized to play a central role in neural processes that regulate self-control. Still uncertain, however, is how that brain structure participates in the dynamically evolving estimation of value that underlies the ability to delay gratification and wait patiently for a gain. To address that gap in knowledge, we studied the spiking activity of neurons in the STN of monkeys during a task in which animals were required to remain motionless for varying periods of time in order to obtain food reward. At the single-neuron and population levels, we found a cost-benefit integration between the desirability of the expected reward and the imposed delay to reward delivery, with STN signals that dynamically combined both attributes of the reward to form a single integrated estimate of value. This neural encoding of subjective value evolved dynamically across the waiting period that intervened after instruction cue. Moreover, this encoding was distributed inhomogeneously along the antero-posterior axis of the STN such that the most dorso-posterior-placed neurons represented the temporal discounted value most strongly. These findings highlight the selective involvement of the dorso-posterior STN in the representation of temporally discounted rewards. The combination of rewards and time delays into an integrated representation is essential for self-control, the promotion of goal pursuit and the willingness to bear the costs of time delays.

Data availability

Data analysed during this study are available at https://github.com/benjaminpasquereau/Neural-dynamics-underlying-self-control-in-the-primate-subthalamic-nucleus

Article and author information

Author details

Benjamin Pasquereau

Department of Neurobiology, Institut des Sciences Cognitives Marc Jeannerod, CNRS UMR 5229, Bron, France

For correspondence
benjamin.pasquereau@isc.cnrs.fr

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2855-0672
Robert S Turner

Department of Neurobiology, University of Pittsburgh, Pittsburgh, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6074-4365

Funding

NIH (NIH R01 NS113817-01)

Robert S Turner

NIH (NIH R01 NS091853-01)

Robert S Turner

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Two rhesus monkeys (monkey C, 8 kg, male; and monkey H, 6 kg, female) were used in this study. Procedures were approved by the Institutional Animal Care and Use Committee of the University of Pittsburgh (protocol number: 12111162) and complied with the Public Health Service Policy on thehumane care and use of laboratory animals (amended 2002). When animals were not in active use, they were housed in individual primate cages in an air-conditioned room where water was always available. The monkeys' access to food was regulated to increase their motivation to perform the task. Throughout the study, the animals were monitored daily by an animal research technician or veterinary technician for evidence of disease or injury and body weight was documented weekly. If a body weight <90% of baseline was observed, the food regulation was stopped.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.