Incorporation of a cost of deliberation time in perceptual decision making.

Many decisions benefit from the accumulation of evidence obtained sequentially over time. In such circumstances, the decision maker must balance speed against accuracy, and the nature of this tradeoff mediates competing desiderata and costs, especially those associated with the passage of time. A neural mechanism to achieve this balance is to accumulate evidence in suitable units and to terminate the deliberation when enough evidence has accrued. To accommodate time costs, it has been hypothesized that the criterion to terminate a decision may become lax as a function of time. Here we tested this hypothesis by manipulating the cost of time in a perceptual choice-reaction time task. Participants discriminated the direction of motion in a dynamic random-dot display, which varied in difficulty across trials. After each trial, they received feedback in the form of points based on whether they made a correct or erroneous choice. They were instructed to maximize their points per unit of time. Unbeknownst to the participants, halfway through the experiment, we increased the time pressure by canceling a small fraction of trials if they had not made a decision by a provisional deadline. Although the manipulation canceled less than 5% of trials, it induced the participants to make faster decisions while lowering their decision accuracy. The pattern of choices and reaction times were explained by bounded drift-diffusion. In all phases of the experiment, stopping bounds were found to decline as a function of time, consistent with the optimal solution, and this decline was exaggerated in response to the time-cost manipulation.

DREDge: robust motion correction for high-density extracellular recordings across species.

High-density microelectrode arrays (MEAs) have opened new possibilities for systems neuroscience in human and non-human animals, but brain tissue motion relative to the array poses a challenge for downstream analyses, particularly in human recordings. We introduce DREDge (Decentralized Registration of Electrophysiology Data), a robust algorithm which is well suited for the registration of noisy, nonstationary extracellular electrophysiology recordings. In addition to estimating motion from spikes in the action potential (AP) frequency band, DREDge enables automated tracking of motion at high temporal resolution in the local field potential (LFP) frequency band. In human intraoperative recordings, which often feature fast (period <1s) motion, DREDge correction in the LFP band enabled reliable recovery of evoked potentials, and significantly reduced single-unit spike shape variability and spike sorting error. Applying DREDge to recordings made during deep probe insertions in nonhuman primates demonstrated the possibility of tracking probe motion of centimeters across several brain regions while simultaneously mapping single unit electrophysiological features. DREDge reliably delivered improved motion correction in acute mouse recordings, especially in those made with an recent ultra-high density probe. We also implemented a procedure for applying DREDge to recordings made across tens of days in chronic implantations in mice, reliably yielding stable motion tracking despite changes in neural activity across experimental sessions. Together, these advances enable automated, scalable registration of electrophysiological data across multiple species, probe types, and drift cases, providing a stable foundation for downstream scientific analyses of these rich datasets.

Judging the difficulty of perceptual decisions.

Deciding how difficult it is going to be to perform a task allows us to choose between tasks, allocate appropriate resources, and predict future performance. To be useful for planning, difficulty judgments should not require completion of the task. Here, we examine the processes underlying difficulty judgments in a perceptual decision-making task. Participants viewed two patches of dynamic random dots, which were colored blue or yellow stochastically on each appearance. Stimulus coherence (the probability, pblue, of a dot being blue) varied across trials and patches thus establishing difficulty, |pblue -0.5|. Participants were asked to indicate for which patch it would be easier to decide the dominant color. Accuracy in difficulty decisions improved with the difference in the stimulus difficulties, whereas the reaction times were not determined solely by this quantity. For example, when the patches shared the same difficulty, reaction times were shorter for easier stimuli. A comparison of several models of difficulty judgment suggested that participants compare the absolute accumulated evidence from each stimulus and terminate their decision when they differed by a set amount. The model predicts that when the dominant color of each stimulus is known, reaction times should depend only on the difference in difficulty, which we confirm empirically. We also show that this model is preferred to one that compares the confidence one would have in making each decision. The results extend evidence accumulation models, used to explain choice, reaction time, and confidence to prospective judgments of difficulty.

Transient Oscillations of Neural Firing Rate Associated With Routing of Evidence in a Perceptual Decision.

To form a perceptual decision, the brain must acquire samples of evidence from the environment and incorporate them in computations that mediate choice behavior. While much is known about the neural circuits that process sensory information and those that form decisions, less is known about the mechanisms that establish the functional linkage between them. We trained monkeys of both sexes to make difficult decisions about the net direction of visual motion under conditions that required trial-by-trial control of functional connectivity. In one condition, the motion appeared at different locations on different trials. In the other, two motion patches appeared, only one of which was informative. Neurons in the parietal cortex produced brief oscillations in their firing rate at the time routing was established: upon onset of the motion display when its location was unpredictable across trials, and upon onset of an attention cue that indicated in which of two locations an informative patch of dots would appear. The oscillation was absent when the stimulus location was fixed across trials. We interpret the oscillation as a manifestation of the mechanism that establishes the source and destination of flexibly routed information, but not the transmission of the information per se Significance Statement It has often been suggested that oscillations in neural activity might serve a role in routing information appropriately. We observe an oscillation in neural firing rate in the lateral intraparietal area consistent with such a role. The oscillations are transient. They coincide with the establishment of routing, but they do not appear to play a role in the transmission (or conveyance) of the routed information itself.

A neural mechanism for terminating decisions.

The brain makes decisions by accumulating evidence until there is enough to stop and choose. Neural mechanisms of evidence accumulation are established in association cortex, but the site and mechanism of termination are unknown. Here, we show that the superior colliculus (SC) plays a causal role in terminating decisions, and we provide evidence for a mechanism by which this occurs. We recorded simultaneously from neurons in the lateral intraparietal area (LIP) and SC while monkeys made perceptual decisions. Despite similar trial-averaged activity, we found distinct single-trial dynamics in the two areas: LIP displayed drift-diffusion dynamics and SC displayed bursting dynamics. We hypothesized that the bursts manifest a threshold mechanism applied to signals represented in LIP to terminate the decision. Consistent with this hypothesis, SC inactivation produced behavioral effects diagnostic of an impaired threshold sensor and prolonged the buildup of activity in LIP. The results reveal the transformation from deliberation to commitment.

Judging the difficulty of perceptual decisions.

Deciding how difficult it is going to be to perform a task allows us to choose between tasks, allocate appropriate resources, and predict future performance. To be useful for planning, difficulty judgments should not require completion of the task. Here we examine the processes underlying difficulty judgments in a perceptual decision making task. Participants viewed two patches of dynamic random dots, which were colored blue or yellow stochastically on each appearance. Stimulus coherence (the probability, pblue, of a dot being blue) varied across trials and patches thus establishing difficulty, pblue-0.5. Participants were asked to indicate for which patch it would be easier to decide the dominant color. Accuracy in difficulty decisions improved with the difference in the stimulus difficulties, whereas the reaction times were not determined solely by this quantity. For example, when the patches shared the same difficulty, reaction times were shorter for easier stimuli. A comparison of several models of difficulty judgment suggested that participants compare the absolute accumulated evidence from each stimulus and terminate their decision when they differed by a set amount. The model predicts that when the dominant color of each stimulus is known, reaction times should depend only on the difference in difficulty, which we confirm empirically. We also show that this model is preferred to one that compares the confidence one would have in making each decision. The results extend evidence accumulation models, used to explain choice, reaction time and confidence to prospective judgments of difficulty.

Flexible neural control of motor units.

Voluntary movement requires communication from cortex to the spinal cord, where a dedicated pool of motor units (MUs) activates each muscle. The canonical description of MU function rests upon two foundational tenets. First, cortex cannot control MUs independently but supplies each pool with a common drive. Second, MUs are recruited in a rigid fashion that largely accords with Henneman's size principle. Although this paradigm has considerable empirical support, a direct test requires simultaneous observations of many MUs across diverse force profiles. In this study, we developed an isometric task that allowed stable MU recordings, in a rhesus macaque, even during rapidly changing forces. Patterns of MU activity were surprisingly behavior-dependent and could be accurately described only by assuming multiple drives. Consistent with flexible descending control, microstimulation of neighboring cortical sites recruited different MUs. Furthermore, the cortical population response displayed sufficient degrees of freedom to potentially exert fine-grained control. Thus, MU activity is flexibly controlled to meet task demands, and cortex may contribute to this ability.

Decision formation in parietal cortex transcends a fixed frame of reference.

Neurons in the lateral intraparietal cortex represent the formation of a decision when it is linked to a specific action, such as an eye movement to a choice target. However, these neurons should be unable to represent a decision that transpires across actions that would disrupt this linkage. We investigated this limitation by simultaneously recording many neurons from two rhesus monkeys. Although intervening actions disrupt the representation by single neurons, the ensemble achieves continuity of the decision process by passing information from currently active neurons to neurons that will become active after the action. In this way, the representation of an evolving decision can be generalized across actions and transcends the frame of reference that specifies the neural response fields. The finding extends previous observations of receptive field remapping, thought to support the stability of perception across eye movements, to the continuity of a thought process, such as a decision.

Deficits in decision-making induced by parietal cortex inactivation are compensated at two timescales.

Perceptual decisions arise through the transformation of samples of evidence into a commitment to a proposition or plan of action. Such transformation is thought to involve cortical circuits capable of computation over timescales associated with working memory, attention, and planning. Neurons in the lateral intraparietal area (LIP) play a role in these functions, and much of what is known about the neurobiology of decision-making has been influenced by studies of LIP and its network of connections. However, the causal role of LIP remains controversial. In this study, we used pharmacological and chemogenetic methods to inactivate LIP in one brain hemisphere of four rhesus monkeys. This inactivation produced biases in decisions, but the effects dissipated despite persistent neural inactivation, implying compensation by unaffected areas. Compensation occurred rapidly within an experimental session and more gradually across sessions. These findings resolve disparate studies and inform the interpretation of focal perturbations of brain function.

Sequential sampling from memory underlies action selection during abstract decision-making.

The study of perceptual decision-making in monkeys has provided insights into the process by which sensory evidence is integrated toward a decision. When monkeys make decisions with the knowledge of the motor actions the decisions bear upon, the process of evidence integration is instantiated by neurons involved in the selection of said actions. It is less clear how monkeys make decisions when unaware of the actions required to communicate their choice-what we refer to as "abstract" decisions. We investigated this by training monkeys to associate the direction of motion of a noisy random-dot display with the color of two targets. Crucially, the targets were displayed at unpredictable locations after the motion stimulus was extinguished. We found that the monkeys postponed decision formation until the targets were revealed. Neurons in the parietal association area LIP represented the integration of evidence leading to a choice, but as the stimulus was no longer visible, the samples of evidence must have been retrieved from short-term memory. Our results imply that when decisions are temporally unyoked from the motor actions they bear upon, decision formation is protracted until they can be framed in terms of motor actions.

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.

Low-dimensional dynamics for working memory and time encoding.

Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding, we analyze neural activity recorded during delays in four experiments on nonhuman primates. To disambiguate potential mechanisms, we propose two analyses, namely, decoding the passage of time from neural data and computing the cumulative dimensionality of the neural trajectory over time. Time can be decoded with high precision in tasks where timing information is relevant and with lower precision when irrelevant for performing the task. Neural trajectories are always observed to be low-dimensional. In addition, our results further constrain the mechanisms underlying time encoding as we find that the linear "ramping" component of each neuron's firing rate strongly contributes to the slow timescale variations that make decoding time possible. These constraints rule out working memory models that rely on constant, sustained activity and neural networks with high-dimensional trajectories, like reservoir networks. Instead, recurrent networks trained with backpropagation capture the time-encoding properties and the dimensionality observed in the data.

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.

Context-Dependent Decision Making in a Premotor Circuit.

Cognitive capacities afford contingent associations between sensory information and behavioral responses. We studied this problem using an olfactory delayed match to sample task whereby a sample odor specifies the association between a subsequent test odor and rewarding action. Multi-neuron recordings revealed representations of the sample and test odors in olfactory sensory and association cortex, which were sufficient to identify the test odor as match or non-match. Yet, inactivation of a downstream premotor area (ALM), but not orbitofrontal cortex, confined to the epoch preceding the test odor led to gross impairment. Olfactory decisions that were not context-dependent were unimpaired. Therefore, ALM does not receive the outcome of a match/non-match decision from upstream areas. It receives contextual information-the identity of the sample-to establish the mapping between test odor and action. A novel population of pyramidal neurons in ALM layer 2 may mediate this process.

The hippocampus supports deliberation during value-based decisions.

Choosing between two items involves deliberation and comparison of the features of each item and its value. Such decisions take more time when choosing between options of similar value, possibly because these decisions require more evidence, but the mechanisms involved are not clear. We propose that the hippocampus supports deliberation about value, given its well-known role in prospection and relational cognition. We assessed the role of the hippocampus in deliberation in two experiments. First, using fMRI in healthy participants, we found that BOLD activity in the hippocampus increased as a function of deliberation time. Second, we found that patients with hippocampal damage exhibited more stochastic choices and longer reaction times than controls, possibly due to their failure to construct value-based or internal evidence during deliberation. Both sets of results were stronger in value-based decisions compared to perceptual decisions.

Counterfactual Reasoning Underlies the Learning of Priors in Decision Making.

Accurate decisions require knowledge of prior probabilities (e.g., prevalence or base rate), but it is unclear how prior probabilities are learned in the absence of a teacher. We hypothesized that humans could learn base rates from experience making decisions, even without feedback. Participants made difficult decisions about the direction of dynamic random dot motion. Across blocks of 15-42 trials, the base rate favoring left or right varied. Participants were not informed of the base rate or choice accuracy, yet they gradually biased their choices and thereby increased accuracy and confidence in their decisions. They achieved this by updating knowledge of base rate after each decision, using a counterfactual representation of confidence that simulates a neutral prior. The strategy is consistent with Bayesian updating of belief and suggests that humans represent both true confidence, which incorporates the evolving belief of the prior, and counterfactual confidence, which discounts the prior.

Bridging Neural and Computational Viewpoints on Perceptual Decision-Making.

Sequential sampling models have provided a dominant theoretical framework guiding computational and neurophysiological investigations of perceptual decision-making. While these models share the basic principle that decisions are formed by accumulating sensory evidence to a bound, they come in many forms that can make similar predictions of choice behaviour despite invoking fundamentally different mechanisms. The identification of neural signals that reflect some of the core computations underpinning decision formation offers new avenues for empirically testing and refining key model assumptions. Here, we highlight recent efforts to explore these avenues and, in so doing, consider the conceptual and methodological challenges that arise when seeking to infer decision computations from complex neural data.

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.

Comparison of Decision-Related Signals in Sensory and Motor Preparatory Responses of Neurons in Area LIP.

Neurons in the lateral intraparietal (LIP) area of Macaques exhibit both sensory and oculomotor preparatory responses. During perceptual decision making, the preparatory responses have been shown to track the state of the evolving evidence leading to the decision. The sensory responses are known to reflect categorical properties of visual stimuli, but it is not known whether these responses also track evolving evidence. We recorded neural responses from lateral intraparietal area of 2 female rhesus monkeys during a direction discrimination task. We compared sensory and oculomotor-preparatory responses in the same neurons when either the discriminandum (random dot motion) or an eye movement choice-target was in the neuron's response field. The neural responses in both configurations reflected the strength and direction of motion and were correlated with the animal's choice, albeit more prominently when the choice-target was in the response field. However, the variance and autocorrelation pattern of only the motor preparatory responses reflected the process of evidence accumulation. Simulations suggest that the task related activity of sensory responses could be inherited through lateral interactions with neurons that are carrying evidence accumulation signals in their motor-preparatory responses. The results are consistent with the proposal that evolving decision processes are supported by persistent neural activity in the service of actions or intentions, as opposed to high-order representations of stimulus properties.SIGNIFICANCE STATEMENT Perceptual decision making is the process of choosing an appropriate motor action based on perceived sensory information. Association areas of the cortex play an important role in this sensory-motor transformation. The neurons in these areas show both sensory- and motor-related activity. We show here that, in the macaque parietal association area LIP, signatures of the process of evidence accumulation that underlies the decisions are predominantly reflected in the motor-related activity. This finding supports the proposal that perceptual decision making is implemented in the brain as a process of choosing between available motor actions rather than as a process of representing the properties of the sensory stimulus.

Piercing of Consciousness as a Threshold-Crossing Operation.

Many decisions arise through an accumulation of evidence to a terminating threshold. The process, termed bounded evidence accumulation (or drift diffusion), provides a unified account of decision speed and accuracy, and it is supported by neurophysiology in human and animal models. In many situations, a decision maker may not communicate a decision immediately and yet feel that at some point she had made up her mind. We hypothesized that this occurs when an accumulation of evidence reaches a termination threshold, registered, subjectively, as an "aha" moment. We asked human participants to make perceptual decisions about the net direction of dynamic random dot motion. The difficulty and viewing duration were controlled by the experimenter. After indicating their choice, participants adjusted the setting of a clock to the moment they felt they had reached a decision. The subjective decision times (tSDs) were faster on trials with stronger (easier) motion, and they were well fit by a bounded drift-diffusion model. The fits to the tSDs alone furnished parameters that fully predicted the choices (accuracy) of four of the five participants. The quality of the prediction provides compelling evidence that these subjective reports correspond to the terminating process of a decision rather than a post hoc inference or arbitrary report. Thus, conscious awareness of having reached a decision appears to arise when the brain's representation of accumulated evidence reaches a threshold or bound. We propose that such a mechanism might play a more widespread role in the "piercing of consciousness" by non-conscious thought processes.