Neural dynamics underlying self-control in the primate subthalamic nucleus

  1. Benjamin Pasquereau  Is a corresponding author
  2. Robert S Turner
  1. Institut des Sciences Cognitives Marc Jeannerod, CNRS UMR 5229, France
  2. University of Pittsburgh, United States

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

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2855-0672
  2. Robert S Turner

    Department of Neurobiology, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "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

© 2023, Pasquereau & Turner

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.

Metrics

  • 724
    views
  • 137
    downloads
  • 3
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Benjamin Pasquereau
  2. Robert S Turner
(2023)
Neural dynamics underlying self-control in the primate subthalamic nucleus
eLife 12:e83971.
https://doi.org/10.7554/eLife.83971

Share this article

https://doi.org/10.7554/eLife.83971

Further reading

    1. Neuroscience
    Lenia Amaral, Xiaosha Wang ... Ella Striem-Amit
    Research Article

    Research on brain plasticity, particularly in the context of deafness, consistently emphasizes the reorganization of the auditory cortex. But to what extent do all individuals with deafness show the same level of reorganization? To address this question, we examined the individual differences in functional connectivity (FC) from the deprived auditory cortex. Our findings demonstrate remarkable differentiation between individuals deriving from the absence of shared auditory experiences, resulting in heightened FC variability among deaf individuals, compared to more consistent FC in the hearing group. Notably, connectivity to language regions becomes more diverse across individuals with deafness. This does not stem from delayed language acquisition; it is found in deaf native signers, who are exposed to natural language since birth. However, comparing FC diversity between deaf native signers and deaf delayed signers, who were deprived of language in early development, we show that language experience also impacts individual differences, although to a more moderate extent. Overall, our research points out the intricate interplay between brain plasticity and individual differences, shedding light on the diverse ways reorganization manifests among individuals. It joins findings of increased connectivity diversity in blindness and highlights the importance of considering individual differences in personalized rehabilitation for sensory loss.

    1. Computational and Systems Biology
    2. Neuroscience
    Gabriel Loewinger, Erjia Cui ... Francisco Pereira
    Tools and Resources

    Fiber photometry has become a popular technique to measure neural activity in vivo, but common analysis strategies can reduce the detection of effects because they condense within-trial signals into summary measures, and discard trial-level information by averaging across-trials. We propose a novel photometry statistical framework based on functional linear mixed modeling, which enables hypothesis testing of variable effects at every trial time-point, and uses trial-level signals without averaging. This makes it possible to compare the timing and magnitude of signals across conditions while accounting for between-animal differences. Our framework produces a series of plots that illustrate covariate effect estimates and statistical significance at each trial time-point. By exploiting signal autocorrelation, our methodology yields joint 95% confidence intervals that account for inspecting effects across the entire trial and improve the detection of event-related signal changes over common multiple comparisons correction strategies. We reanalyze data from a recent study proposing a theory for the role of mesolimbic dopamine in reward learning, and show the capability of our framework to reveal significant effects obscured by standard analysis approaches. For example, our method identifies two dopamine components with distinct temporal dynamics in response to reward delivery. In simulation experiments, our methodology yields improved statistical power over common analysis approaches. Finally, we provide an open-source package and analysis guide for applying our framework.