Decision Making as a Window on Cognition

A decision is a commitment to a proposition or plan of action based on information and values associated with the possible outcomes. The process operates in a flexible timeframe that is free from the immediacy of evidence acquisition and the real time demands of action itself. Thus, it involves deliberation, planning, and strategizing. This Perspective focuses on perceptual decision making in nonhuman primates and the discovery of neural mechanisms that support accuracy, speed, and confidence in a decision. We suggest that these mechanisms expose principles of cognitive function in general, and we speculate about the challenges and directions before the field

A Neural Mechanism for Sensing and Reproducing a Time Interval

Timing plays a crucial role in sensorimotor function. However, the neural mechanisms that enable the brain to flexibly measure and reproduce time intervals are not known. We recorded neural activity in parietal cortex of monkeys in a time reproduction task. Monkeys were trained to measure and immediately afterward reproduce different sample intervals. While measuring an interval, neural responses had a nonlinear profile that increased with the duration of the sample interval. Activity was reset during the transition from measurement to production and was followed by a ramping activity whose slope encoded the previously measured sample interval. We found that firing rates at the end of the measurement epoch were correlated with both the slope of the ramp and the monkey's corresponding production interval on a trial-by-trial basis. Analysis of response dynamics further linked the rate of change of firing rates in the measurement epoch to the slope of the ramp in the production epoch. These observations suggest that, during time reproduction, an interval is measured prospectively in relation to the desired motor plan to reproduce that interval

A Neural Mechanism for Sensing and Reproducing a Time Interval

SummaryTiming plays a crucial role in sensorimotor function. However, the neural mechanisms that enable the brain to flexibly measure and reproduce time intervals are not known. We recorded neural activity in parietal cortex of monkeys in a time reproduction task. Monkeys were trained to measure and immediately afterward reproduce different sample intervals. While measuring an interval, neural responses had a nonlinear profile that increased with the duration of the sample interval. Activity was reset during the transition from measurement to production and was followed by a ramping activity whose slope encoded the previously measured sample interval. We found that firing rates at the end of the measurement epoch were correlated with both the slope of the ramp and the monkey’s corresponding production interval on a trial-by-trial basis. Analysis of response dynamics further linked the rate of change of firing rates in the measurement epoch to the slope of the ramp in the production epoch. These observations suggest that, during time reproduction, an interval is measured prospectively in relation to the desired motor plan to reproduce that interval

The Neurobiology of Decision-Making and Responsibility: Reconciling Mechanism and Mindedness

This essay reviews recent developments in neurobiology which are beginning to expose the mechanisms that underlie some elements of decision-making that bear on attributions of responsibility. These “elements” have been mainly studied in simple perceptual decision tasks, which are performed similarly by humans and non-human primates. Here we consider the role of neural noise, and suggest that thinking about the role of noise can shift the focus of discussions of randomness in decision-making away from its role in enabling alternate possibilities and toward a potential grounding role for responsibility

Representation of Accumulating Evidence for a Decision in Two Parietal Areas

Decisions are often made by accumulating evidence for and against the alternatives. The momentary evidence represented by sensory neurons is accumulated by downstream structures to form a decision variable, linking the evolving decision to the formation of a motor plan. When decisions are communicated by eye movements, neurons in the lateral intraparietal area (LIP) represent the accumulation of evidence bearing on the potential targets for saccades. We now show that reach-related neurons from the medial intraparietal area (MIP) exhibit a gradual modulation of their firing rates consistent with the representation of an evolving decision variable. When decisions were communicated by saccades instead of reaches, decision-related activity was attenuated in MIP, whereas LIP neurons were active while monkeys communicated decisions by saccades or reaches. Thus, for decisions communicated by a hand movement, a parallel flow of sensory information is directed to parietal areas MIP and LIP during decision formation

Differentiating between integration and non-integration strategies in perceptual decision making.

Many tasks used to study decision-making encourage subjects to integrate evidence over time. Such tasks are useful to understand how the brain operates on multiple samples of information over prolonged timescales, but only if subjects actually integrate evidence to form their decisions. We explored the behavioral observations that corroborate evidence-integration in a number of task-designs. Several commonly accepted signs of integration were also predicted by non-integration strategies. Furthermore, an integration model could fit data generated by non-integration models. We identified the features of non-integration models that allowed them to mimic integration and used these insights to design a motion discrimination task that disentangled the models. In human subjects performing the task, we falsified a non-integration strategy in each and confirmed prolonged integration in all but one subject. The findings illustrate the difficulty of identifying a decision-maker's strategy and support solutions to achieve this goal

Neural Circuit Dynamics Underlying Accumulation of Time-Varying Evidence During Perceptual Decision Making

How do neurons in a decision circuit integrate time-varying signals, in favor of or against alternative choice options? To address this question, we used a recurrent neural circuit model to simulate an experiment in which monkeys performed a direction-discrimination task on a visual motion stimulus. In a recent study, it was found that brief pulses of motion perturbed neural activity in the lateral intraparietal area (LIP), and exerted corresponding effects on the monkey's choices and response times. Our model reproduces the behavioral observations and replicates LIP activity which, depending on whether the direction of the pulse is the same or opposite to that of a preferred motion stimulus, increases or decreases persistently over a few hundred milliseconds. Furthermore, our model accounts for the observation that the pulse exerts a weaker influence on LIP neuronal responses when the pulse is late relative to motion stimulus onset. We show that this violation of time-shift invariance (TSI) is consistent with a recurrent circuit mechanism of time integration. We further examine time integration using two consecutive pulses of the same or opposite motion directions. The induced changes in the performance are not additive, and the second of the paired pulses is less effective than its standalone impact, a prediction that is experimentally testable. Taken together, these findings lend further support for an attractor network model of time integration in perceptual decision making

Multiple decisions about one object involve parallel sensory acquisition but time-multiplexed evidence incorporation.

The brain is capable of processing several streams of information that bear on different aspects of the same problem. Here, we address the problem of making two decisions about one object, by studying difficult perceptual decisions about the color and motion of a dynamic random dot display. We find that the accuracy of one decision is unaffected by the difficulty of the other decision. However, the response times reveal that the two decisions do not form simultaneously. We show that both stimulus dimensions are acquired in parallel for the initial ∼0.1 s but are then incorporated serially in time-multiplexed bouts. Thus, there is a bottleneck that precludes updating more than one decision at a time, and a buffer that stores samples of evidence while access to the decision is blocked. We suggest that this bottleneck is responsible for the long timescales of many cognitive operations framed as decisions

Focal optogenetic suppression in macaque area MT biases direction discrimination and decision confidence, but only transiently

Insights from causal manipulations of brain activity depend on targeting the spatial and temporal scales most relevant for behavior. Using a sensitive perceptual decision task in monkeys, we examined the effects of rapid, reversible inactivation on a spatial scale previously achieved only with electrical microstimulation. Inactivating groups of similarly tuned neurons in area MT produced systematic effects on choice and confidence. Behavioral effects were attenuated over the course of each session, suggesting compensatory adjustments in the downstream readout of MT over tens of minutes. Compensation also occurred on a sub-second time scale: behavior was largely unaffected when the visual stimulus (and concurrent suppression) lasted longer than 350 ms. These trends were similar for choice and confidence, consistent with the idea of a common mechanism underlying both measures. The findings demonstrate the utility of hyperpolarizing opsins for linking neural population activity at fine spatial and temporal scales to cognitive functions in primates