A major organizing principle of the brain proposes that the cortex, basal ganglia, and thalamus are interconnected in parallel recurrent loops. According to this model, the two principal basal ganglia pathways – termed direct and indirect – are thought to excite and inhibit cortical activity via their outputs to thalamus. Here, we test this model by simultaneously recording activity across cortex and striatum, while inhibiting the direct or indirect basal ganglia pathway as mice perform an evidence-accumulation task in which each manipulation produces opposing decision biases. Inconsistent with the classic model, we find that overall cortical activity exhibits equal amounts of excitation and inhibition following direct or indirect pathway inhibition. However, we find that the two pathways exert strong and opponent influence over cortical neurons that display graded tuning to varying levels of sensory evidence (“evidence-tuned”), depending on each neuron’s ipsilateral or contralateral tuning preference. In contrast, the two pathways have minimal influence over cortical neurons that display a binary tuning to the selected action (“choice-tuned”). Our results thus support an updated classic model, in which the opponent modulation of cortical activity by basal ganglia pathways depends on the functional tuning properties of their cortical partners.