Distinct relationships of parietal and prefrontal cortices to evidence accumulation

Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in multiple brain regions(1–8). Here we develop a generalizable method to measure tuning curves that specify the relationship between neural responses and mentally-accumulated evidence, and apply it to distinguish the encoding of decision variables in posterior parietal cortex (PPC) and prefrontal cortex (frontal orienting fields, FOF). We recorded the firing rates of neurons in PPC and FOF from rats performing a perceptual decision-making task. Classical analyses uncovered correlates of accumulating evidence, similar to previous observations in primates and also similar across the two regions. However, tuning curve assays revealed that while the PPC encodes a graded value of the accumulating evidence, the FOF has a more categorical encoding that indicates, throughout the trial, the decision provisionally favored by the evidence accumulated so far. Contrary to current views(3,5,7–9), this suggests that premotor activity in frontal cortex does not play a role in the accumulation process, but instead has a more categorical function, such as transforming accumulated evidence into a discrete choice. To causally probe the role of FOF activity, we optogenetically silenced it during different timepoints of the trial. Consistent with a role in committing to a categorical choice at the end of the evidence accumulation process, but not consistent with a role during the accumulation itself, a behavioral effect was observed only when FOF silencing occurred at the end of the perceptual stimulus. Our results place important constraints on the circuit logic of brain regions involved in decision-making.