Michael N. Shadlen

Noise, neural codes and cortical organization

Cortical circuitry must facilitate information transfer in accordance with a neural code. In this article we examine two candidate neural codes: information is represented in the spike rate of neurons, or information is represented in the precise timing of individual spikes. These codes can be distinguished by examining the physiological basis of the highly irregular interspike intervals typically observed in cerebral cortex. Recent advances in our understanding of cortical microcircuitry suggest that the timing of neuronal spikes conveys little, if any, information. The cortex is likely to propagate a noisy rate code through redundant, patchy interconnections.

Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task

Decisions about the visual world can take time to form, especially when information is unreliable. We studied the neural correlate of gradual decision formation by recording activity from the lateral intraparietal cortex (area LIP) of rhesus monkeys during a combined motion-discrimination reaction-time task. Monkeys reported the direction of random-dot motion by making an eye movement to one of two peripheral choice targets, one of which was within the response field of the neuron. We varied the difficulty of the task and measured both the accuracy of direction discrimination and the time required to reach a decision. Both the accuracy and speed of decisions increased as a function of motion strength. During the period of decision formation, the epoch between onset of visual motion and the initiation of the eye movement response, LIP neurons underwent ramp-like changes in their discharge rate that predicted the monkeys decision. A steeper rise in spike rate was associated with stronger stimulus motion and shorter reaction times. The observations suggest that neurons in LIP integrate time-varying signals that originate in the extrastriate visual cortex, accumulating evidence for or against a specific behavioral response. A threshold level of LIP activity appears to mark the completion of the decision process and to govern the tradeoff between accuracy and speed of perception.

A relationship between behavioral choice and the visual responses of neurons in macaque MT

We have previously documented the exquisite motion sensitivity of neurons in extrastriate area MT by studying the relationship between their responses and the direction and strength of visual motion signals delivered to their receptive fields. These results suggested that MT neurons might provide the signals supporting behavioral choice in visual discrimination tasks. To approach this question from another direction, we have now studied the relationship between the discharge of MT neurons and behavioral choice, independently of the effects of visual stimulation. We found that trial-to-trial variability in neuronal signals was correlated with the choices the monkey made. Therefore, when a directionally selective neuron in area MT fires more vigorously, the monkey is more likely to make a decision in favor of the preferred direction of the cell. The magnitude of the relationship was modest, on average, but was highly significant across a sample of 299 cells from four monkeys. The relationship was present for all stimuli (including those without a net motion signal), and for all but the weakest responses. The relationship was reduced or eliminated when the demands of the task were changed so that the directional signal carried by the cell was less informative. The relationship was evident within 50 ms of response onset, and persisted throughout the stimulus presentation. On average, neurons that were more sensitive to weak motion signals had a stronger relationship to behavior than those that were less sensitive. These observations are consistent with the idea that neuronal signals in MT are used by the monkey to determine the direction of stimulus motion. The modest relationship between behavioral choice and the discharge of any one neuron, and the prevalence of the relationship across the population, make it likely that signals from many neurons are pooled to form the data on which behavioral choices are based.

Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque

To make a visual discrimination, the brain must extract relevant information from the retina, represent appropriate variables in the visual cortex and read out this representation to decide which of two or more alternatives is more likely. We recorded from neurons in the dorsolateral prefrontal cortex (areas 8 and 46) of the rhesus monkey while it performed a motion discrimination task. The monkey indicated its judgment of direction by making appropriate eye movements. As the monkey viewed the motion stimulus, the neural response predicted the monkeys subsequent gaze shift, hence its judgment of direction. The response comprised a mixture of high–level oculomotor signals and weaker visual sensory signals that reflected the strength and direction of motion. This combination of sensory integration and motor planning could reflect the conversion of visual motion information into a categorical decision about direction and thus give insight into the neural computations behind a simple cognitive act.

Neural computations that underlie decisions about sensory stimuli

Decision-making behavior has been studied extensively, but the neurophysiological mechanisms responsible for this remarkable cognitive ability are just beginning to be understood. Here we propose neural computations that can account for the formation of categorical decisions about sensory stimuli by accumulating information over time into a single quantity: the logarithm of the likelihood ratio favoring one alternative over another. We also review electrophysio-logical studies that have identified brain structures that may be involved in computing this sort of decision variable. The ideas presented constitute a framework for understanding how and where perceptual decisions are formed in the brain.

Representation of a perceptual decision in developing oculomotor commands.

Behaviour often depends on the ability to make categorical judgements about sensory information acquired over time. Such judgements require a comparison of the evidence favouring the alternatives, but how the brain forms these comparisons is unknown. Here we show that in a visual discrimination task, the accumulating balance of sensory evidence favouring one interpretation over another is evident in the neural circuits that generate the behavioural response. We trained monkeys to make a direction judgement about dynamic random-dot motion and to indicate their judgement with an eye movement to a visual target. We interrupted motion viewing with electrical microstimulation of the frontal eye field and analysed the resulting, evoked eye movements for evidence of ongoing activity associated with the oculomotor response. Evoked eye movements deviated in the direction of the monkeys judgement. The magnitude of the deviation depended on motion strength and viewing time. The oculomotor signals responsible for these deviations reflected the accumulated motion information that informed the monkeys choices on the discrimination task. Thus, for this task, decision formation and motor preparation appear to share a common level of neural organization.

Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex

Decisive Monkeys Decision-making is a central theme in current research in cognitive neuroscience. Behavioral protocols have provided an entry into explorations of the neural processes that underlie decision-making. Empirical studies have provided support for a diffusion model in which information accumulates over time until a threshold is reached, with noisiness in the inputs related to decision errors. Kiani and Shadlen (p. 759) developed a behavioral task to study choice certainty and identified the corresponding neuronal representations in monkeys. The monkeys were allowed to choose to opt out of an uncertain, higher reward choice in favor of a certain, lower payoff. The same neurons that encoded the information used to make a choice also encoded the extent of certainty, which in humans would be described as the degree of confidence in ones decision. Neurons in the primate parietal cortex encode information required to make a decision and also the certainty of that choice. The degree of confidence in a decision provides a graded and probabilistic assessment of expected outcome. Although neural mechanisms of perceptual decisions have been studied extensively in primates, little is known about the mechanisms underlying choice certainty. We have shown that the same neurons that represent formation of a decision encode certainty about the decision. Rhesus monkeys made decisions about the direction of moving random dots, spanning a range of difficulties. They were rewarded for correct decisions. On some trials, after viewing the stimulus, the monkeys could opt out of the direction decision for a small but certain reward. Monkeys exercised this option in a manner that revealed their degree of certainty. Neurons in parietal cortex represented formation of the direction decision and the degree of certainty underlying the decision to opt out.

Banburismus and the brain: decoding the relationship between sensory stimuli, decisions, and reward.

This article relates a theoretical framework developed by British codebreakers in World War II to the neural computations thought to be responsible for forming categorical decisions about sensory stimuli. In both, a weight of evidence is computed and accumulated to support or oppose the alternative interpretations. A decision is reached when the evidence reaches a threshold value. In the codebreaking scheme, the threshold determined the speed and accuracy of the decision process. Here we propose that in the brain, the threshold may be controlled by neural circuits that calculate the rate of reward.

Effect of expected reward magnitude on the response of neurons in the dorsolateral prefrontal cortex of the macaque.

The dorsolateral prefrontal cortex plays a critical role in guiding actions that ensue seconds after an instruction. We recorded from neurons in area 46 and the frontal eye field (FEF) while monkeys performed a memory-guided eye movement task. A visual cue signaled whether a small or large liquid reward would accompany a correct response. Many neurons in area 46 responded more when the monkey expected a larger reward. Reward-related enhancement was evident throughout the memory period and was most pronounced when the remembered target appeared in the neurons response field. Enhancement was not present in the FEF. The mixture of neural signals representing spatial working memory and reward expectation appears to be a distinct feature of area 46.

The effect of stimulus strength on the speed and accuracy of a perceptual decision

Both the speed and the accuracy of a perceptual judgment depend on the strength of the sensory stimulation. When stimulus strength is high, accuracy is high and response time is fast; when stimulus strength is low, accuracy is low and response time is slow. Although the psychometric function is well established as a tool for analyzing the relationship between accuracy and stimulus strength, the corresponding chronometric function for the relationship between response time and stimulus strength has not received as much consideration. In this article, we describe a theory of perceptual decision making based on a diffusion model. In it, a decision is based on the additive accumulation of sensory evidence over time to a bound. Combined with simple scaling assumptions, the proportional-rate and power-rate diffusion models predict simple analytic expressions for both the chronometric and psychometric functions. In a series of psychophysical experiments, we show that this theory accounts for response time and accuracy as a function of both stimulus strength and speed-accuracy instructions. In particular, the results demonstrate a close coupling between response time and accuracy. The theory is also shown to subsume the predictions of Piérons Law, a power function dependence of response time on stimulus strength. The theorys analytic chronometric function allows one to extend theories of accuracy to response time.