Abstract

The external globus pallidus (GPe) is a key nucleus within basal ganglia circuits that are thought to be involved in action selection. A class of computational models assumes that, during action selection, the basal ganglia compute for all actions available in a given context the probabilities that they should be selected. These models suggest that a network of GPe and subthalamic nucleus (STN) neurons computes the normalization term in Bayes’ equation. In order to perform such computation, the GPe needs to send feedback to the STN equal to a particular function of the activity of STN neurons. However, the complex form of this function makes it unlikely that individual GPe neurons, or even a single GPe cell type, could compute it. Here, we demonstrate how this function could be computed within a network containing two types of GABAergic GPe projection neuron, so-called ‘prototypic’ and ‘arkypallidal’ neurons, that have different response properties in vivo and distinct connections. We compare our model predictions with the experimentally-reported connectivity and input-output functions (f-I curves) of the two populations of GPe neurons. We show that, together, these dichotomous cell types fulfil the requirements necessary to compute the function needed for optimal action selection. We conclude that, by virtue of their distinct response properties and connectivities, a network of arkypallidal and prototypic GPe neurons comprises a neural substrate capable of supporting the computation of the posterior probabilities of actions.

Highlights

  • A set of subcortical brain nuclei known as the basal ganglia are thought to be involved in action selection [1]

  • One of the brain regions involved in action selection is a set of subcortical nuclei known as the basal ganglia

  • The optimal action selection models have predicted that, in order to compute the normalization, the GPe needs to send feedback to the subthalamic nucleus (STN) that is proportional to a particular function of STN activity

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Summary

Introduction

A set of subcortical brain nuclei known as the basal ganglia are thought to be involved in action selection [1]. A class of models [9,10,11,12] suggests that, during selection of the most appropriate action, corticobasal ganglia circuits approximate a statistical procedure known as the Multihypothesis Sequential Probability Ratio Test (MSPRT) [13]. These models assume the basal ganglia continuously update the probabilities of different actions being appropriate given sensory signals, and that an action is initiated whenever its corresponding probability exceeds a threshold of confidence. We will refer to this property as the ‘optimal action selection’

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