Neural underpinnings of the evidence accumulator

Abstract

Gradual accumulation of evidence favoring one or another choice is considered a core component of many different types of decisions, and has been the subject of many neurophysiological studies in non-human primates. But its neural circuit mechanisms remain mysterious. Investigating it in rodents has recently become possible, facilitating perturbation experiments to delineate the relevant causal circuit, as well as the application of other tools more readily available in rodents. In addition, advances in stimulus design and analysis have aided studying the relevant neural encoding. In complement to ongoing non-human primate studies, these newly available model systems and tools place the field at an exciting time that suggests that the dynamical circuit mechanisms underlying accumulation of evidence could soon be revealed.

Figure 1

Evidence accumulator models and associated circuits. a, Schematic of evidence accumulation process, here illustrated for a case when the subject must decide between orienting Left or Right. As the decision process unfolds, noisy evidence favoring one choice (RIGHT) adds to the accumulator while evidence favoring the other choice (LEFT) subtracts from the accumulator. The sign of the accumulated evidence when the subject is asked to report their decision dictates the resulting decision choice. Trials with strong evidence that more consistently favors one choice over the other result in steeper slopes on average, and the accumulator will soon be far away from the decision boundary, so easy decisions can be made quickly. Weaker, less consistent evidence will result in meandering trajectories with shallower slopes on average, and even after lengthy accumulation periods, the accumulator may not be far from the decision boundary, leading to slow, more error-prone decisions. In tasks in which the subject determines the duration of the decision process, known as “reaction time tasks,” the subject commits to a decision when the evidence reaches a bound (+C or −C in the figure); the reaction time is determined by when the bound is reached, and the decision choice is given by which bound was reached. b, Average neural responses from monkey PPC (area LIP) during the period of decision formation in the random dot motion discrimination task [27]. After a delay, responses exhibit ramping response profiles with slopes that depend on stimulus strength. Stronger motion leads to sharper slopes and weaker motion to shallower slopes. This corresponds to the average trends predicted by the evidence accumulator model. c, Diagram of interconnected brain regions that have been demonstrated to exhibit responses profiles correlated with accumulating evidence. These areas thus serve as candidates to be involved in the evidence accumulation process.

Figure 2

Characteristics of rat PPC and FOF during accumulation of evidence based decision making, from [45]. a, Average neural responses in rat PPC during the Poisson Clicks task. Trials are grouped by average stimulus strength. Similar to monkey PPC, responses exhibit ramping profiles that depend on stimulus strength. b, Same as a for FOF. c, Click-triggered average responses for rat PPC during the Poisson clicks task. Individual clicks have a measurable and sustained influence on responses in PPC. d, Same as c for FOF. Individual clicks also produced a sustained response, with a magnitude that slowly but significantly decayed over hundreds of milliseconds. e, Time-average population comparison of tuning curves for accumulating evidence in PPC and FOF. PPC shows a smoothly graded relationship, while FOF shows a sharper dependence on the sign of the accumulator value. f, Bias caused by 500-ms unilateral inactivation of FOF with halorhodopsin during one of four epochs of the task: before the stimulus (red), during the first half of the stimulus (yellow), during the second half of the stimulus (green), or during the movement period (blue). Only peri-choice perturbation of FOF has a significant effect on decision making. A further experiment using half the inactivation time period (250 ms) reached the same conclusion [45].