Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions1,2,3,4,5,6,7,8. 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 and prefrontal cortex (frontal orienting fields, FOF). We recorded the firing rates of neurons in posterior parietal cortex 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 posterior parietal cortex encodes a graded value of the accumulating evidence, the FOF has a more categorical encoding that indicates, throughout the trial, the decision provisionally favoured by the evidence accumulated so far. Contrary to current views3,5,7,8,9, this suggests that premotor activity in the frontal cortex does not have a role in the accumulation process, but instead has a more categorical function, such as transforming accumulated evidence into a discrete choice. To probe causally the role of FOF activity, we optogenetically silenced it during different time points 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 behavioural 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.
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We thank K. Deisseroth for support with optogenetics. We thank A. Akrami, T. Buschman, J. Gold, B. Pesaran, B. Scott, D. Tank and M. Yartsev for comments on the manuscript. We thank A. Begelfer, K. Osorio and J. Teran for animal and laboratory support. T.D.H. was supported by National Institutes of Health (NIH) Award Number F32MH098572. C.A.D. was supported by a Howard Hughes Medical Institute predoctoral fellowship. C.D.K. was supported in part by the NIH Award Number T32MH065214.
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Nature Communications (2018)