Biased competition in the absence of input bias revealed through corticostriatal computation

Significance The canonical model of the basal ganglia is based on competing direct (GO) vs. indirect (NO-GO) pathways. However, how is either of the two pathways activated if they receive the same corticostriatal inputs as experimental evidence suggests? Also, in the context of rule-based decisions, how is a specific action selected among competing GO pathways? We introduce a neural circuit model that identifies three alternative mechanisms flexibly supporting preferential processing between GO and NO-GO alternatives under balanced input. Only one of these mechanisms, however, is capable of enabling action selection by reinforcing, in the striatum, the rule-based rhythmic biases reported in prefrontal cortex. Classical accounts of biased competition require an input bias to resolve the competition between neuronal ensembles driving downstream processing. However, flexible and reliable selection of behaviorally relevant ensembles can occur with unbiased stimulation: striatal D1 and D2 spiny projection neurons (SPNs) receive balanced cortical input, yet their activity determines the choice between GO and NO-GO pathways in the basal ganglia. We here present a corticostriatal model identifying three mechanisms that rely on physiological asymmetries to effect rate- and time-coded biased competition in the presence of balanced inputs. First, tonic input strength determines which one of the two SPN phenotypes exhibits a higher mean firing rate. Second, low-strength oscillatory inputs induce higher firing rate in D2 SPNs but higher coherence between D1 SPNs. Third, high-strength inputs oscillating at distinct frequencies can preferentially activate D1 or D2 SPN populations. Of these mechanisms, only the latter accommodates observed rhythmic activity supporting rule-based decision making in prefrontal cortex.