Similar Response Dynamics Represent Opposite Behaviors and Rewards in the Frontal Cortex

Abstract

The frontal cortex (FC) plays a pivotal role in adaptively controlling actions and their dynamics in response to incoming sensory signals. We explored FC encoding of identical stimuli and their behavioral consequences when they signified diametrically opposite responses depending on task context. Two groups of female ferrets performed Go-NoGo auditory categorization tasks with opposite contingencies and rewards and diverse stimuli. Remarkably, despite opposite stimulus-action associations, single-unit responses were similar across all tasks, being more sustained and stronger to Target sounds (signaling a change in action) than to Reference sounds (indicating maintenance of ongoing actions) especially during task engagement. Overall activity was composed of three distinct dynamic response profiles. Each corresponded to a separate neuronal cluster and exhibited a different role in relation to the succession of task events. Decoding based on the temporal structure of population responses revealed distinct decoders that were aligned to different task events. Similar to single-unit findings, the β-band power extracted from the FC local field potentials (LFPs) was strongly and similarly modulated during Target stimuli across all tasks despite opposite behavioral actions. In contrast, power in all other LFP frequency bands varied significantly across task stimuli and actions. Based on these findings, we propose the FC encodes a common, highly abstract representation of all the different behavioral tasks. We further outline a hypothetical model of pathway-specific functional projections from the tripartite FC neuronal clusters to the basal ganglia, consistent with previous evidence for the conjoint roles of the FC and striatum in adaptive motor control.