It is often suggested that decisions are made when accumulated sensory information reaches a fixed accuracy criterion. This is supported by many studies showing a gradual build up of neural activity to a threshold. However, the proposal that this build up is caused by sensory accumulation is challenged by findings that decisions are based on information from a time window much shorter than the build-up process. Here, we propose that in natural conditions where the environment can suddenly change, the policy that maximizes reward rate is to estimate evidence by accumulating only novel information and then compare the result to a decreasing accuracy criterion. We suggest that the brain approximates this policy by multiplying an estimate of sensory evidence with a motor-related urgency signal and that the latter is primarily responsible for neural activity build up. We support this hypothesis using human behavioral data from a modified random-dot motion task in which motion coherence changes during each trial.

Neurophysiological studies of decision making have primarily focused on decisions about information that is stable over time. However, during natural behavior, animals make decisions in a constantly changing environment. To investigate the neural mechanisms of such dynamic choices, we recorded activity in dorsal premotor (PMd) and primary motor cortex (M1) while monkeys performed a two-choice reaching task in which sensory information about the correct choice was changing within each trial and the decision could be made at any time. During deliberation, activity in both areas did not integrate sensory information but instead tracked it and combined it with a growing urgency signal. Approximately 280 ms before movement onset, PMd activity tuned to the selected target reached a consistent peak while M1 activity tuned to the unselected target was suppressed. We propose that this reflects the resolution of a competition between the potential responses and constitutes the volitional commitment to an action choice.

Recent work suggests that while animals decide between reaching actions, neurons in dorsal premotor (PMd) and primary motor (M1) cortex reflect a dynamic competition between motor plans and determine when commitment to a choice is made. This competition is biased by at least two sources of information: the changing sensory evidence for one choice versus another, and an urgency signal that grows over time. Here, we test the hypothesis that the urgency signal adjusts the trade-off between speed and accuracy during both decision-making and movement execution. Two monkeys performed a reaching decision task in which sensory evidence continuously evolves over the course of each trial. In different blocks, task timing parameters encouraged monkeys to voluntarily adapt their behavior to be either hasty or conservative. Consistent with our hypothesis, during the deliberation process the baseline and gain of neural activity in decision-related PMd (29%) and M1 cells (45%) was higher when monkeys applied a hasty policy than when they behaved conservatively, but at the time of commitment the population activity was similar across blocks. Other cells (30% in PMd, 30% in M1) showed activity that increased or decreased with elapsing time until the moment of commitment. Movement-related neurons were also more active after longer decisions, as if they were influenced by the same urgency signal controlling the gain of decision-related activity. Together, these results suggest that the arm motor system receives an urgency/vigor signal that adjusts the speed-accuracy trade-off for decision-making and movement execution. Key words: decision-making; monkey; speed-accuracy trade-off; urgency IntroductionDuring natural behavior, animals are motivated to optimize their reward rate. To do so, they must find the best speed-accuracy trade-off (SAT) for both their decisions and their movements, and to adjust it to the current context. Recent studies examined how the SAT is adjusted during a variety of perceptual discrimination tasks. For example, several fMRI studies reported that time pressure leads to an increased BOLD response during baseline periods (Forstmann et al., 2008;Ivanoff et al., 2008;van Veen et al., 2008). Additional mechanisms for SAT adjustment have been identified at the level of single neurons. In the frontal eye fields (FEFs), Heitz and Schall (2012) found baseline changes as well as changes in neural gain and the onset time of perceptual Received June 9, 2015; revised Nov. 26, 2015; accepted Dec. 9, 2015. Author Significance StatementThis work addresses the neural mechanisms that control the speed-accuracy trade-off in both decisions and movements, in the kinds of dynamic situations that are typical of natural animal behavior. We found that many "decision-related" premotor and motor neurons are modulated in a time-dependent manner compatible with an "urgency" signal that changes between hasty and conservative decision policies. We also found that such modulation influenced cells related to the speed of the reaching ...

Prominent theories of decision making suggest that the basal ganglia (BG) play a causal role in deliberation between action choices. An alternative hypothesis is that deliberation occurs in cortical regions, while the BG control the speed-accuracy trade-off (SAT) between committing to a choice versus continuing to deliberate. Here, we test these hypotheses by recording activity in the internal and external segments of the globus pallidus (GPi/GPe) while monkeys perform a task dissociating the process of deliberation, the moment of commitment, and adjustment of the SAT. Our data suggest that unlike premotor and motor cortical regions, pallidal output does not contribute to the process of deliberation but instead provides a time-varying signal that controls the SAT and reflects the growing urgency to commit to a choice. Once a target is selected by cortical regions, GP activity confirms commitment to the decision and invigorates the subsequent movement.

Speed-accuracy tradeoffs (SATs) exist in both decision-making and movement control, and are generally studied separately. However, in natural behavior animals are free to adjust the time invested in deciding and moving so as to maximize their reward rate. Here, we investigate whether shared mechanisms exist for SAT adjustment in both decisions and actions. Two monkeys performed a reach decision task in which they watched 15 tokens jump, one every 200 ms, from a central circle to one of two peripheral targets, and had to guess which target would ultimately receive the majority of tokens. The monkeys could decide at any time, and once a target was reached, the remaining token movements accelerated to either 50 ms ("fast" block) or 150 ms ("slow" block). Decisions were generally earlier and less accurate in fast than slow blocks, and in both blocks, the criterion of accuracy decreased over time within each trial. This could be explained by a simple model in which sensory information is combined with a linearly growing urgency signal. Remarkably, the duration of the reaching movements produced after the decision decreased over time in a similar block-dependent manner as the criterion of accuracy estimated by the model. This suggests that SATs for deciding and acting are influenced by a shared urgency/vigor signal. Consistent with this, we observed that the vigor of saccades performed during the decision process was higher in fast than in slow blocks, suggesting the influence of a context-dependent global arousal.