Assessing Selectivity in the Basal Ganglia: The “Gearbox” Hypothesis

Abstract 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. Author summary Our brains are continuously called to select the most appropriate action between alternative competing choices. A plethora of evidence and theoretical work indicates that a fundamental brain region called the basal ganglia might be the locus where this competition occurs. But how is the winning choice determined each time? Using a detailed computational model, based on neurophysiological properties of this region, we suggest that, whereas the basal ganglia might indeed contain the circuitry of action selection, the cerebral cortex is, in fact, the brain region that dictates this process. Similarly to a gearbox in a car, the basal ganglia provide modes for the exploitation of the safest option (forward gears), exploration of alternative options (reverse gear) and a neutral state, in case that the selection process needs to be halted. Our results further indicate that the instructions for mode-switching are relayed to the basal ganglia through specific low frequencies of oscillations within cortical areas. Finally, we provide estimations for the frequency ranges that can be used to activate each selectivity mode, as well as the duration of the selection process under various conditions.