Similar Dynamic Frontal Cortex Representations of Auditory Stimuli Cueing Opposite Actions and Rewards

Frontal Cortex (FC) plays a pivotal role in controlling actions and their dynamics in response to incoming sensory stimuli. We explored FC representations of the same stimuli when signifying diametrically opposite behavioral meanings depending on task context. Two groups of ferrets performed Go-NoGo auditory categorization tasks with opposite contingencies and rewards, and varied stimuli. Remarkably, despite the 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. Three major dynamic response profiles were extracted from the overall responses, and their combination defined separate neuronal clusters that exhibited different roles in relation to task events. Decoding based on the temporal structure of the population responses revealed distinct decoders that were aligned to different task events. Furthermore, the β-band power, extracted from the FC local field potentials, was similarly and strongly modulated during Target stimuli in all tasks despite opposite behavioral actions. Based on these findings, we propose a model of pathway-specific functional projections from the tripartite FC neuronal clusters to the basal ganglia that is consistent with previous evidence for the conjoint roles of the FC and striatum in adaptive motor control.