Joshua I. Gold

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.

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.

Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area.

This study aimed to identify neural mechanisms that underlie perceptual learning in a visual-discrimination task. We trained two monkeys (Macaca mulatta) to determine the direction of visual motion while we recorded from their middle temporal area (MT), which in trained monkeys represents motion information that is used to solve the task, and lateral intraparietal area (LIP), which represents the transformation of motion information into a saccadic choice. During training, improved behavioral sensitivity to weak motion signals was accompanied by changes in motion-driven responses of neurons in LIP, but not in MT. The time course and magnitude of the changes in LIP correlated with the changes in behavioral sensitivity throughout training. Thus, for this task, perceptual learning does not appear to involve improvements in how sensory information is represented in the brain, but rather how the sensory representation is interpreted to form the decision that guides behavior.

Rational regulation of learning dynamics by pupil-linked arousal systems

The ability to make inferences about the current state of a dynamic process requires ongoing assessments of the stability and reliability of data generated by that process. We found that these assessments, as defined by a normative model, were reflected in nonluminance-mediated changes in pupil diameter of human subjects performing a predictive-inference task. Brief changes in pupil diameter reflected assessed instabilities in a process that generated noisy data. Baseline pupil diameter reflected the reliability with which recent data indicate the current state of the data-generating process and individual differences in expectations about the rate of instabilities. Together these pupil metrics predicted the influence of new data on subsequent inferences. Moreover, a task- and luminance-independent manipulation of pupil diameter predictably altered the influence of new data. Thus, pupil-linked arousal systems can help to regulate the influence of incoming data on existing beliefs in a dynamic environment.

Relationships between Pupil Diameter and Neuronal Activity in the Locus Coeruleus, Colliculi, and Cingulate Cortex

Changes in pupil diameter that reflect effort and other cognitive factors are often interpreted in terms of the activity of norepinephrine-containing neurons in the brainstem nucleus locus coeruleus (LC), but there is little direct evidence for such a relationship. Here, we show that LC activation reliably anticipates changes in pupil diameter that either fluctuate naturally or are driven by external events during near fixation, as in many psychophysical tasks. This relationship occurs on as fine a temporal and spatial scale as single spikes from single units. However, this relationship is not specific to the LC. Similar relationships, albeit with delayed timing and different reliabilities across sites, are evident in the inferior and superior colliculus and anterior and posterior cingulate cortex. Because these regions are interconnected with the LC, the results suggest that non-luminance-mediated changes in pupil diameter might reflect LC-mediated coordination of neuronal activity throughout some parts of the brain.

Reinforcement learning can account for associative and perceptual learning on a visual decision task

We recently showed that improved perceptual performance on a visual motion direction–discrimination task corresponds to changes in how an unmodified sensory representation in the brain is interpreted to form a decision that guides behavior. Here we found that these changes can be accounted for using a reinforcement-learning rule to shape functional connectivity between the sensory and decision neurons. We modeled performance on the basis of the readout of simulated responses of direction-selective sensory neurons in the middle temporal area (MT) of monkey cortex. A reward prediction error guided changes in connections between these sensory neurons and the decision process, first establishing the association between motion direction and response direction, and then gradually improving perceptual sensitivity by selectively strengthening the connections from the most sensitive neurons in the sensory population. The results suggest a common, feedback-driven mechanism for some forms of associative and perceptual learning.

An approximately Bayesian delta-rule model explains the dynamics of belief updating in a changing environment.

Maintaining appropriate beliefs about variables needed for effective decision making can be difficult in a dynamic environment. One key issue is the amount of influence that unexpected outcomes should have on existing beliefs. In general, outcomes that are unexpected because of a fundamental change in the environment should carry more influence than outcomes that are unexpected because of persistent environmental stochasticity. Here we use a novel task to characterize how well human subjects follow these principles under a range of conditions. We show that the influence of an outcome depends on both the error made in predicting that outcome and the number of similar outcomes experienced previously. We also show that the exact nature of these tendencies varies considerably across subjects. Finally, we show that these patterns of behavior are consistent with a computationally simple reduction of an ideal-observer model. The model adjusts the influence of newly experienced outcomes according to ongoing estimates of uncertainty and the probability of a fundamental change in the process by which outcomes are generated. A prior that quantifies the expected frequency of such environmental changes accounts for individual variability, including a positive relationship between subjective certainty and the degree to which new information influences existing beliefs. The results suggest that the brain adaptively regulates the influence of decision outcomes on existing beliefs using straightforward updating rules that take into account both recent outcomes and prior expectations about higher-order environmental structure.

Caudate Encodes Multiple Computations for Perceptual Decisions

Perceptual decision making is a complex process that requires multiple computations, including the accumulation of sensory evidence and an ongoing evaluation of the accumulation process to use for prediction and adjustment. Implementing these computations likely involves interactions among many brain regions. For perceptual decisions linked to oculomotor actions, neural correlates of sensory evidence accumulation have been identified in several cortical areas, including the frontal eye field and lateral intraparietal area, and one of their direct, subcortical targets, the superior colliculus. These structures are also connected indirectly, via the basal ganglia. The basal ganglia pathway has been theorized to contribute to perceptual decision making, but the nature of this contribution has yet to be examined directly. Here we show that in monkeys performing a reaction-time visual motion direction-discrimination task, neurons in a primary input structure of the basal ganglia, the caudate nucleus, encode three aspects of decision making: evidence accumulation, evaluation, and choice biases. These results indicate that the basal ganglia pathway can provide important signals to influence and assess perceptual decisions that guide oculomotor behavior.

Distinct Representations of a Perceptual Decision and the Associated Oculomotor Plan in the Monkey Lateral Intraparietal Area

Perceptual decisions that are used to select particular actions can appear to be formed in an intentional framework, in which sensory evidence is converted directly into a plan to act. However, because the relationship between perceptual decision-making and action selection has been tested primarily under conditions in which the two could not be dissociated, it is not known whether this intentional framework plays a general role in forming perceptual decisions or only reflects certain task conditions. To dissociate decision and motor processing in the brain, we recorded from individual neurons in the lateral intraparietal area of monkeys performing a task that included a flexible association between a decision about the direction of random-dot motion and the direction of the appropriate eye-movement response. We targeted neurons that responded selectively in anticipation of a particular eye-movement response. We found that these neurons encoded the perceptual decision in a manner that was distinct from how they encoded the associated response. These decision-related signals were evident regardless of whether the appropriate decision–response association was indicated before, during, or after decision formation. The results suggest that perceptual decision-making and action selection are different brain processes that only appear to be inseparable under particular behavioral contexts.