The gradual and noisy accumulation of evidence is a fundamental component of decision-making, with noise playing a key role as the source of variability and errors. However, the origins of this noise have never been determined. We developed decision-making tasks in which sensory evidence is delivered in randomly timed pulses, and analyzed the resulting data with models that use the richly detailed information of each trial's pulse timing to distinguish between different decision-making mechanisms. This analysis allowed measurement of the magnitude of noise in the accumulator's memory, separately from noise associated with incoming sensory evidence. In our tasks, the accumulator's memory was noiseless, for both rats and humans. In contrast, the addition of new sensory evidence was the primary source of variability. We suggest our task and modeling approach as a powerful method for revealing internal properties of decision-making processes.

Humans and monkeys have similar abilities to discriminate the difference in frequency between two mechanical vibrations applied sequentially to the fingertips. A key component of this sensory task is that the second stimulus is compared with the trace left by the first (base) stimulus, which must involve working memory. Where and how is this trace held in the brain? This question was investigated by recording from single neurons in the prefrontal cortex of monkeys while they performed the somatosensory discrimination task. Here we describe neurons in the inferior convexity of the prefrontal cortex whose discharge rates varied, during the delay period between the two stimuli, as a monotonic function of the base stimulus frequency. We describe this as 'monotonic stimulus encoding', and we suggest that the result may generalize: monotonic stimulus encoding may be the basic representation of one-dimensional sensory stimulus quantities in working memory. Thus we predict that other behavioural tasks that require ordinal comparisons between scalar analogue stimuli would give rise to monotonic responses similar to those reported here.

Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in multiple brain regions1–8. 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 views3,5,7–9, 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.