Microscopic and mesoscopic effects of reward uncertainty in monkey fronto-parietal areas

Abstract

Theories of executive function propose that controlled information processing is costly and is allocated according to the behavioral benefits it brings. Computational theories predict that the benefits of new information depend on prior uncertainty, but the cellular effects of uncertainty on the executive network are incompletely understood. Using simultaneous recordings in monkeys, we reveal several mechanisms by which the fronto-parietal network reacts to uncertainty independently of average reward gains. We show that the variance of expected rewards, independently of the value of the rewards, was represented in single neuron and population spiking activity and local field potential (LFP) oscillations. Moreover, uncertainty asymmetrically affected the coherence between spikes and LFPs, selectively suppressing information transmission from the frontal to the parietal lobe but enhancing transmission from the parietal to the frontal lobe, consistent with Bayesian principles of optimal inference under uncertainty.