Frontopolar cortex stimulation induces prolonged disruption to counterfactual processing: insights from altered local field potentials

Abstract

Frontopolar cortex (FPC) is a large, anterior sub-region of prefrontal cortex found in both humans and non-human primates (NHPs) and is thought to support monitoring the value of switching between alternative goals. However, the neuronal mechanisms underlying this function are unclear. Here we used multielectrode arrays to record the local field potentials (LFPs) in the FPC of two macaques performing a Wisconsin Card Sorting Test analogue and found that bursts of gamma and beta in FPC tracked counterfactual not current rule value. Moreover, we show that brief high-frequency microstimulation to a single trial causally affects both LFP activity in FPC, as well as rule-guided decision-making across successive trials. Following stimulation of FPC we observed reduced exploration of the counterfactual rule pre-rule-change, as well as a delayed adaptation to the newly relevant following post-rule-change. A similar, multi-trial time-course disturbance to beta and gamma activity within FPC was also induced following single-trial microstimulation. These findings conclusively link neuronal activity in FPC with behavioural monitoring of the value of counterfactual rules and provide neural mechanistic insights into how FPC supports rule-based decision-making. Significance statementIncreasing evidence from human and non-human primates has prompted theories linking FPC with the control of exploration during decision-making. However, it is current unclear how the neuronal activity within frontal pole supports exploratory decision-making processes. Here we show that rhythmic activity, in the beta and gamma bands, recorded from FPC is correlated both with outcome of the previous choice, and the value of switching to an alternative choice. Furthermore, we show that disrupting beta and gamma activity within FPC causally influences exploratory decision-making: initially decreasing exploration before impairing adaptation to abstract rule changes. Together these findings provide the first mechanistic insight into how the neuronal activity within FPC can support exploratory behaviour.