Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models

Author:

Adams Rick A1234,Moutoussis Michael56,Nour Matthew M347,Dahoun Tarik348,Lewis Declan1,Illingworth Benjamin1,Veronese Mattia9,Mathys Christoph61011,de Boer Lieke12,Guitart-Masip Marc612,Friston Karl J5,Howes Oliver D347,Roiser Jonathan P1

Affiliation:

1. Institute of Cognitive Neuroscience, University College London, London WC1N 3AZ, UK

2. Division of Psychiatry, University College London, London W1T 7NF, UK

3. Psychiatric Imaging Group, Robert Steiner MRI Unit, MRC London Institute of Medical Sciences, Hammersmith Hospital, London W12 0NN, UK

4. Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, Hammersmith Hospital, London W12 0NN, UK

5. Wellcome Centre for Human Neuroimaging, University College London, London WC1N 3BG, UK

6. Max Planck-UCL Centre for Computational Psychiatry and Ageing Research, London WC1B 5EH, UK

7. Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience (IoPPN), King’s College London, London SE5 8AF, UK

8. Department of Psychiatry, University of Oxford, Warneford Hospital, Oxford OX3 7JX, UK

9. Centre for Neuroimaging Sciences, Institute of Psychiatry, Psychology & Neuroscience (IoPPN), King's College London, London SE5 8AF, UK

10. Scuola Internazionale Superiore di Studi Avanzati (SISSA), 34136 Trieste, Italy

11. Translational Neuromodeling Unit (TNU), Institute for Biomedical Engineering, University of Zurich and ETH Zurich, 8032 Zurich, Switzerland

12. Aging Research Center, Karolinska Institute, 171 65 Stockholm, Sweden

Abstract

Abstract Choosing actions that result in advantageous outcomes is a fundamental function of nervous systems. All computational decision-making models contain a mechanism that controls the variability of (or confidence in) action selection, but its neural implementation is unclear—especially in humans. We investigated this mechanism using two influential decision-making frameworks: active inference (AI) and reinforcement learning (RL). In AI, the precision (inverse variance) of beliefs about policies controls action selection variability—similar to decision ‘noise’ parameters in RL—and is thought to be encoded by striatal dopamine signaling. We tested this hypothesis by administering a ‘go/no-go’ task to 75 healthy participants, and measuring striatal dopamine 2/3 receptor (D2/3R) availability in a subset (n = 25) using [11C]-(+)-PHNO positron emission tomography. In behavioral model comparison, RL performed best across the whole group but AI performed best in participants performing above chance levels. Limbic striatal D2/3R availability had linear relationships with AI policy precision (P = 0.029) as well as with RL irreducible decision ‘noise’ (P = 0.020), and this relationship with D2/3R availability was confirmed with a ‘decision stochasticity’ factor that aggregated across both models (P = 0.0006). These findings are consistent with occupancy of inhibitory striatal D2/3Rs decreasing the variability of action selection in humans.

Funder

Academy of Medical Sciences

National Institute of Health Research

Wellcome Strategic Award

National Institute for Health Research

EU-FP7 MC6 ITN IN-SENS

Swedish Research Council

NIHR UCLH Biomedical Research Centre pump priming award to JPR

Medical Research Council

Wellcome Trust

National Institute for Health Research Biomedical Research Centre

South London and Maudsley NHS Foundation Trust

Kings College London

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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