Brain Regions Involved in Decision-Making
Nature 520, 220–223 (09 April 2015)
Distinct relationships of parietal and prefrontal cortices to evidence accumulation
Timothy D. Hanks, et.al.
Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA
Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA
Departments of Biology and Applied Mathematics, University of Washington, Seattle, Washington 98105, USA
NYU-ECNU Institute of Brain and Cognitive Science, NYU-Shanghai, Shanghai 200122, China
Howard Hughes Medical Institute, Princeton University, Princeton, New Jersey 08544, USA
Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions. 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 views, 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.
We trained rats on a previously developed decision task in which subjects accumulate sensory evidence over many hundreds of milliseconds to inform a binary left–right choice (‘Poisson clicks’ task). On each trial, rats kept their nose in a central port during the presentation of two simultaneous trains of randomly timed auditory clicks, one played from a speaker to their left and the other from a speaker to their right. At the end of the variable-duration stimulus, the rat’s task was to decide which side had played the greater total number of clicks. Easy trials had a large mean rate difference between the two click trains (for example, 39:1 clicks per second), while difficult trials had a small mean rate difference (for example, 21:19 clicks per second). Accumulation of evidence models predict that averaging within a given difficulty class will produce a mean trajectory for the accumulated evidence that gradually ramps over time with a slope proportional to the mean strength of the sensory evidence. This type of correlate of evidence accumulation has been reported in several interconnected primate brain regions, including the posterior parietal cortex (PPC) and frontal eye fields (FEF). To examine whether signatures of evidence accumulation are present in the rodent brain, we recorded from 394 neurons in the PPC of 4 rats, and 397 neurons in the FOF of 6 rats while they performed the Poisson clicks task. These two areas (the PPC and FOF) have been suggested as potential rat homologues of the primate PPC and FEF, respectively. We recorded all isolatable neurons encountered regardless of response properties. A total of 93 neurons in the PPC (23%) and 128 neurons in the FOF (32%) exhibited firing rates during the pre-movement period (from stimulus onset to centre port withdrawal) that were significantly different (P < 0.05) for trials that subsequently ended with a right versus left choice. This pre-movement side selectivity is consistent with previous findings in both rat PPC and FOF. We focus on these pre-movement side-selective neurons because they are most likely to have a role in decision formation.
Our results indicate that rather than participating in a single, distributed process during decision-making, neurons in parietal and prefrontal areas have distinct relationships to accumulating evidence. PPC neurons veridically encode a graded value of the accumulated evidence, even though separate work from our laboratory suggests that PPC activity is not necessary for choice behaviour in this task. By contrast, perhaps in readiness for the ‘go’ signal that comes at a variable duration after stimulus onset, neural activity in the FOF can be approximately described as representing, throughout the stimulus, the categorical answer to the question ‘if the go signal came now, which choice should I make?’. Unilateral FOF perturbations affect choice behaviour only at the end of the evidence accumulation period, when the provisional choice must be converted into a motor act. These results suggest that accumulation occurs upstream to FOF and challenge the prevailing view that the prefrontal cortex is part of the neural circuit for accumulation of evidence. The FOF may instead be necessary for the final step in the decision process: the conversion of the graded accumulation signal into a categorical choice.
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