Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network

Bahareh Taghizadeh,Nicholas C Foley,Michael Cohanpour,Sameer A Sheth,Reza Lashgari,Jacqueline Gottlieb,Mulugeta Semework,Saeed Karimimehr

doi:10.1038/s42003-020-01320-6

Abstract

A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings. However, while computational theories predict that the benefits of new information depend on prior uncertainty, the cellular effects of uncertainty on the executive network are incompletely understood. Using simultaneous recordings in monkeys, we describe several mechanisms by which the fronto-parietal network reacts to uncertainty. We show that the variance of expected rewards, independently of the value of the rewards, was encoded in single neuron and population spiking activity and local field potential (LFP) oscillations, and, importantly, asymmetrically affected fronto-parietal information transmission (measured through the coherence between spikes and LFPs). Higher uncertainty selectively enhanced information transmission from the parietal to the frontal lobe and suppressed it in the opposite direction, consistent with Bayesian principles that prioritize sensory information according to a decision maker’s prior uncertainty.

Highlights

A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings
We show that the uncertainty of an expected reward, independently of the value of the reward, affects multiple aspects of microscopic and mesoscopic fronto-parietal activity, including single-neuron responses, local field potential (LFP) oscillations, and spike-field coherence (SFC)
Low-frequencyα/low-β-LFP power homogenously decreased in 7A and the dorsolateral prefrontal cortex (dlPFC) as a function of EV and uncertainty

Summary

Introduction

A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings. Because the decision-theoretic (Bayesian) definition of information is in terms of a reduction of uncertainty, an important implication of this view is that control should be optimally allocated to tasks that not merely have reward value but, have uncertainty It is in conditions of higher ex ante uncertainty that animals can expect to obtain the greatest benefits from processing new information and improving prediction accuracy[4,5,6,7]. Consistent with this view, a growing literature shows that attention is recruited by uncertainty independently of reward gains. In instrumental conditions, when animals make reward-maximizing decisions, reductions of decision uncertainty are closely related with increases in long-term reward gains[5,18]

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Conclusion