Timothy D. Hanks

Probabilistic Population Codes for Bayesian Decision Making

When making a decision, one must first accumulate evidence, often over time, and then select the appropriate action. Here, we present a neural model of decision making that can perform both evidence accumulation and action selection optimally. More specifically, we show that, given a Poisson-like distribution of spike counts, biological neural networks can accumulate evidence without loss of information through linear integration of neural activity and can select the most likely action through attractor dynamics. This holds for arbitrary correlations, any tuning curves, continuous and discrete variables, and sensory evidence whose reliability varies over time. Our model predicts that the neurons in the lateral intraparietal cortex involved in evidence accumulation encode, on every trial, a probability distribution which predicts the animals performance. We present experimental evidence consistent with this prediction and discuss other predictions applicable to more general settings.

Bounded Integration in Parietal Cortex Underlies Decisions Even When Viewing Duration Is Dictated by the Environment

Decisions about sensory stimuli are often based on an accumulation of evidence in time. When subjects control stimulus duration, the decision terminates when the accumulated evidence reaches a criterion level. Under many natural circumstances and in many laboratory settings, the environment, rather than the subject, controls the stimulus duration. In these settings, it is generally assumed that subjects commit to a choice at the end of the stimulus stream. Indeed, failure to benefit from the full stream of information is interpreted as a sign of imperfect accumulation or memory leak. Contrary to these assumptions, we show that monkeys performing a direction discrimination task commit to a choice when the accumulated evidence reaches a threshold level (or bound), sometimes long before the end of stimulus. This bounded accumulation of evidence is reflected in the activity of neurons in the lateral intraparietal cortex. Thus, the readout of visual cortex embraces a termination rule to limit processing even when potentially useful information is available.

Microstimulation of macaque area LIP affects decision-making in a motion discrimination task

A central goal of cognitive neuroscience is to elucidate the neural mechanisms underlying decision-making. Recent physiological studies suggest that neurons in association areas may be involved in this process. To test this, we measured the effects of electrical microstimulation in the lateral intraparietal area (LIP) while monkeys performed a reaction-time motion discrimination task with a saccadic response. In each experiment, we identified a cluster of LIP cells with overlapping response fields (RFs) and sustained activity during memory-guided saccades. Microstimulation of this cluster caused an increase in the proportion of choices toward the RF of the stimulated neurons. Choices toward the stimulated RF were faster with microstimulation, while choices in the opposite direction were slower. Microstimulation never directly evoked saccades, nor did it change reaction times in a simple saccade task. These results demonstrate that the discharge of LIP neurons is causally related to decision formation in the discrimination task.

Elapsed Decision Time Affects the Weighting of Prior Probability in a Perceptual Decision Task

Decisions are often based on a combination of new evidence with prior knowledge of the probable best choice. Optimal combination requires knowledge about the reliability of evidence, but in many realistic situations, this is unknown. Here we propose and test a novel theory: the brain exploits elapsed time during decision formation to combine sensory evidence with prior probability. Elapsed time is useful because (1) decisions that linger tend to arise from less reliable evidence, and (2) the expected accuracy at a given decision time depends on the reliability of the evidence gathered up to that point. These regularities allow the brain to combine prior information with sensory evidence by weighting the latter in accordance with reliability. To test this theory, we manipulated the prior probability of the rewarded choice while subjects performed a reaction-time discrimination of motion direction using a range of stimulus reliabilities that varied from trial to trial. The theory explains the effect of prior probability on choice and reaction time over a wide range of stimulus strengths. We found that prior probability was incorporated into the decision process as a dynamic bias signal that increases as a function of decision time. This bias signal depends on the speed–accuracy setting of human subjects, and it is reflected in the firing rates of neurons in the lateral intraparietal area (LIP) of rhesus monkeys performing this task.

Distinct relationships of parietal and prefrontal cortices to evidence accumulation

Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions. 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 and prefrontal cortex (frontal orienting fields, FOF). We recorded the firing rates of neurons in posterior parietal cortex 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 posterior parietal cortex encodes a graded value of the accumulating evidence, the FOF has a more categorical encoding that indicates, throughout the trial, the decision provisionally favoured by the evidence accumulated so far. Contrary to current views, this suggests that premotor activity in the frontal cortex does not have a role in the accumulation process, but instead has a more categorical function, such as transforming accumulated evidence into a discrete choice. To probe causally the role of FOF activity, we optogenetically silenced it during different time points 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 behavioural 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.

A neural mechanism of speed-accuracy tradeoff in macaque area LIP

Decision making often involves a tradeoff between speed and accuracy. Previous studies indicate that neural activity in the lateral intraparietal area (LIP) represents the gradual accumulation of evidence toward a threshold level, or evidence bound, which terminates the decision process. The level of this bound is hypothesized to mediate the speed-accuracy tradeoff. To test this, we recorded from LIP while monkeys performed a motion discrimination task in two speed-accuracy regimes. Surprisingly, the terminating threshold levels of neural activity were similar in both regimes. However, neurons recorded in the faster regime exhibited stronger evidence-independent activation from the beginning of decision formation, effectively reducing the evidence-dependent neural modulation needed for choice commitment. Our results suggest that control of speed vs accuracy may be exerted through changes in decision-related neural activity itself rather than through changes in the threshold applied to such neural activity to terminate a decision. DOI: http://dx.doi.org/10.7554/eLife.02260.001

Distinct effects of prefrontal and parietal cortex inactivations on an accumulation of evidence task in the rat

Numerous brain regions have been shown to have neural correlates of gradually accumulating evidence for decision-making, but the causal roles of these regions in decisions driven by accumulation of evidence have yet to be determined. Here, in rats performing an auditory evidence accumulation task, we inactivated the frontal orienting fields (FOF) and posterior parietal cortex (PPC), two rat cortical regions that have neural correlates of accumulating evidence and that have been proposed as central to decision-making. We used a detailed model of the decision process to analyze the effect of inactivations. Inactivation of the FOF induced substantial performance impairments that were quantitatively best described as an impairment in the output pathway of an evidence accumulator with a long integration time constant (>240 ms). In contrast, we found a minimal role for PPC in decisions guided by accumulating auditory evidence, even while finding a strong role for PPC in internally-guided decisions. DOI: http://dx.doi.org/10.7554/eLife.05457.001

Perceptual Decision Making in Rodents, Monkeys, and Humans

Perceptual decision making is the process by which animals detect, discriminate, and categorize information from the senses. Over the past two decades, understanding how perceptual decisions are made has become a central theme in the neurosciences. Exceptional progress has been made by recording from single neurons in the cortex of the macaque monkey and using computational models from mathematical psychology to relate these neural data to behavior. More recently, however, the range of available techniques and paradigms has dramatically broadened, and researchers have begun to harness new approaches to explore how rodents and humans make perceptual decisions. The results have illustrated some striking convergences with findings from the monkey, but also raised new questions and provided new theoretical insights. In this review, we summarize key findings, and highlight open challenges, for understanding perceptual decision making in rodents, monkeys, and humans.

Neural underpinnings of the evidence accumulator.

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.

When is enough enough

How does the decision-making process stop? Lo and Wang propose that a large-scale interconnected network encompassing parietal cortex, basal ganglia and motor structures controls the balance between speed and accuracy.