Capturing the temporal evolution of choice across prefrontal cortex

Laurence T Hunt,Steven W Kennerley,Jonathan D Wallis,Takayuki Hosokawa,Timothy Ej Behrens

doi:10.7554/elife.11945

Abstract

Activity in prefrontal cortex (PFC) has been richly described using economic models of choice. Yet such descriptions fail to capture the dynamics of decision formation. Describing dynamic neural processes has proven challenging due to the problem of indexing the internal state of PFC and its trial-by-trial variation. Using primate neurophysiology and human magnetoencephalography, we here recover a single-trial index of PFC internal states from multiple simultaneously recorded PFC subregions. This index can explain the origins of neural representations of economic variables in PFC. It describes the relationship between neural dynamics and behaviour in both human and monkey PFC, directly bridging between human neuroimaging data and underlying neuronal activity. Moreover, it reveals a functionally dissociable interaction between orbitofrontal cortex, anterior cingulate cortex and dorsolateral PFC in guiding cost-benefit decisions. We cast our observations in terms of a recurrent neural network model of choice, providing formal links to mechanistic dynamical accounts of decision-making.

Highlights

Correlates of decision variables are routinely found in prefrontal cortex (PFC) during value-guided decision making (Clithero and Rangel, 2014; Kennerley and Walton, 2011)
We find that orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC) dynamics selectively influence dorsolateral dorsolateral prefrontal cortex (DLPFC) activity on delay- and effort-based decisions respectively
We examined a study of cost-benefit decision making in which single neuron firing and local field potentials (LFPs) were recorded simultaneously from three PFC subregions fundamental to valueguided choice in four macaque monkeys: orbitofrontal cortex (OFC), anterior cingulate cortex (ACC) and dorsolateral prefrontal cortex (DLPFC)

Summary

Introduction

Correlates of decision variables are routinely found in prefrontal cortex (PFC) during value-guided decision making (Clithero and Rangel, 2014; Kennerley and Walton, 2011). They have been richly described using static, economic models of choice (Glimcher and Fehr, 2014). Neuroeconomic accounts explain firing rates of single neurons or human neuroimaging data in terms of experimental variables that motivate choice behaviour. These include the magnitude or likelihood of available reward, and the costs involved in obtaining those rewards. Our present understanding of economic decision formation has been founded upon careful study of neural representations of value and how they differ across PFC subregions (Glimcher and Fehr, 2014; Rushworth et al, 2012; Rangel and Hare, 2010)

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