Assessing Selectivity in the Basal Ganglia: The "Gearbox" Hypothesis

Despite experimental evidence, the literature so far contains no systematic attempt to address the impact of cortical oscillations on the ability of the basal ganglia (BG) to select. In this study, we employed a state-of-the-art spiking neural model of the BG circuitry and investigated the effectiveness of this circuitry as an action selection device. We found that cortical frequency, phase, dopamine and the examined time scale, all have a very important impact on this process. Our simulations resulted in a canonical profile of selectivity, termed selectivity portraits, which suggests that the cortex is the structure that determines whether selection will be performed in the BG and what strategy will be utilized. Some frequency ranges promote the exploitation of highly salient actions, others promote the exploration of alternative options, while the remaining frequencies halt the selection process. Based on this behaviour, we propose that the BG circuitry can be viewed as the gearbox of action selection. Coalitions of rhythmic cortical areas are able to switch between a repertoire of available BG modes which, in turn, change the course of information flow within the cortico-BG-thalamo-cortical loop. Dopamine, akin to control pedals, either stops or initiates a decision, while cortical frequencies, as a gear lever, determine whether a decision can be triggered and what type of decision this will be. Finally, we identified a selection cycle with a period of around 200ms, which was used to assess the biological plausibility of the popular cognitive architectures.