Distinct relationships of parietal and prefrontal cortices to evidence accumulation

• Published in: Nature (London) Vol. 520; no. 7546; pp. 220 - 223
• Main Authors: Hanks, Timothy D., Kopec, Charles D., Brunton, Bingni W., Duan, Chunyu A., Erlich, Jeffrey C., Brody, Carlos D.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 09.04.2015; Nature Publishing Group
• Subjects: 631/378; 631/378/2649; 631/378/2649/1409; Accumulation; Animals; Bias; Brain; Brain research; Decision making; Decision Making - physiology; Halorhodopsins - metabolism; Humanities and Social Sciences; letter; Male; multidisciplinary; Neural circuitry; Neural Pathways; Neurons; Neurons - physiology; Parietal Lobe - cytology; Parietal Lobe - physiology; Physiological aspects; Prefrontal cortex; Prefrontal Cortex - cytology; Prefrontal Cortex - physiology; Psychological aspects; Rats; Rats, Long-Evans; Rodents; Science
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature14066

A method to measure the precise relationship between neuronal firing rates and the representation of accumulated evidence is described; results in the parietal and prefrontal cortex of rats, together with transient optogenetic inactivation of the prefrontal cortex, challenge the prevailing view that the prefrontal cortex is part of the neural circuit for accumulating evidence, and suggest that neurons in parietal and prefrontal areas have distinct relationships to evidence accumulation in decision-making. Neuronal correlates of decision making Previous work in nonhuman primates has documented neural correlates of accumulating evidence for decision-making in a variety of brain regions, primarily in the posterior parietal cortex and the frontal eye fields in the prefrontal cortex. Carlos Brody and colleagues test these observations in rats trained to perform an auditory evidence-accumulation decision task, and develop a method to measure the precise relationship between neuronal firing rates and representation of evidence. Their results challenge the prevailing view that the prefrontal cortex is part of the neural circuit for accumulating evidence and suggest that neurons in parietal and prefrontal areas have distinct relationships during decision-making. Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions 1 , 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 views 3 , 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.