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Zylberberg, A.

Publications and source records attributed to Zylberberg, A..

14 recordsLinked to original sources

Behavioral demands organize a decision process into distinct yet coordinated neural representations in parietal cortex

Perceptual decisions are widely modeled as the accumulation of evidence to a bound. In the lateral intraparietal area (LIP), this computation is thought to be implemented in a low-dimensional population representation organized around the single action used to report the choice, consistent with an intentional framework. The intentional framework, however, implies that changing the behavioral demands on the report should change the representation itself, raising a question about the generality of the low-dimensional decision representation described in LIP: is it a special case of decisions reported through a single action, or does it reflect a more general computational architecture that can support multiple behavioral outputs? We tested this by training monkeys to report the \textit{termination} of a motion-discrimination decision with a saccade to a choice-neutral target, and its \textit{content} only later, with a saccade to one of two choice targets. Even though the two reports were behaviorally separable, the timing of termination remained systematically linked to the accumulation of sensory evidence supporting the eventual choice in both monkeys, indicating that both reports continued to draw on a common underlying computation. Using high-density Neuropixels recordings from LIP, however, we found that decision termination and decision content were represented along orthogonal population coding directions supported by largely non-overlapping groups of neurons. Yet the two representations were not independent: trial-by-trial fluctuations in the population encoding content predicted subsequent fluctuations in the population encoding termination, with their coupling strengthening as the decision evolved. These results suggest that a single decision computation can be flexibly reformatted into distinct, action-specific representations, coordinated by selective transfer of information between neural populations.

neuroscience↗

The Metacognitive Sensitivity of Verbal and Numerical Confidence Reports

We study how confidence in perceptual decisions depends on whether it is communicated verbally (e.g., "very likely") or numerically (e.g., "80% certainty"). We find that verbal expressions more reliably distinguish correct from incorrect choices than numerical reports, challenging the common assumption that numerical probabilities provide more precise representations of uncertainty. Additionally, in a dyadic decision-making task in which participants can revise their initial reports based on a partners choice and expressed confidence, verbal and numerical reports are equally effective in supporting accurate revisions of initial judgments. Together, these results underscore the effectiveness of verbal expressions as a means of conveying decision confidence.

animal behavior and cognition↗

Contrasting Probabilistic and Intentional Accounts of Confidence in Perceptual Decisions

The ability to evaluate ones own knowledge states is often studied using paradigms in which participants make a decision and subsequently report their confidence. This structure has motivated hierarchical models in which confidence arises from a metacognitive process, distinct from the decision process itself, that estimates the probability that the choice is correct (Meyniel et al., 2015; Pouget et al., 2016; Fleming and Daw, 2017). Here, we contrast this framework with an alternative based on an intentional architecture (Shadlen et al., 2008). In this account, choice and confidence are determined simultaneously through a multidimensional drift-diffusion process, where each dimension represents one choice-confidence combination (Ratcliff and Starns, 2009, 2013). Choice, response time, and confidence jointly emerge when one of these accumulators reaches a decision bound. To adjudicate between these accounts, we fit both models to behavioral data from two perceptual tasks: a random-dots motion discrimination task with incentivized confidence reports, and a luminance discrimination task without feedback or incentives. The integrated model provided a superior fit for the incentivized motion task, whereas the hierarchical model more accurately captured behavior in the un-incentivized luminance task. These results suggest that confidence does not rely on a single computational mechanism, but rather its implementation may adapt to the specific demands and structure of the task.

animal behavior and cognition↗

Behavioral Signatures of Post-Decisional Attention in Preferential Choice

Attention plays a key role in decision-making by directing limited cognitive resources to relevant information. It has been proposed that attention also biases the decision process, due to a multiplicative interaction between attention and subjective value (e.g., Krajbich et al., 2010). We tested two predictions of models that posit a causal multiplicative effect of attention on decision formation: (i) the last fixation should be more informative about the choice when the overall value of the alternatives is high, and (ii) more attention should be directed to the chosen option when choices conflict with stated preferences than when they do not. Reanalyzing several datasets from a food-choice task, we found no evidence supporting these predictions. An alternative model where attention reflects choices after the decision has completed, explains key observations, including the last-fixation bias, the gaze-cascade effect and the effect of the overall value of the alternatives on response times. However, this model does not fully account for the association between dwell time and choice. We conclude that gaze behavior prior to the choice report likely reflects both decisional and post-decisional processes.

animal behavior and cognition↗

Population Representation of the Confidence in a Decision in the Lateral Intraparietal Area of the Macaque

Confidence in a decision is the belief, prior to feedback, that ones choice is correct. In the brain, many decisions are implemented as a race between competing evidence-accumulation processes. We ask whether the neurons that represent evidence accumulation also carry information about whether the choice is correct (i.e., confidence). Monkeys performed a reaction time version of the random dot motion task. Neuropixels probes were used to record from neurons in the lateral intraparietal (LIP) area. LIP neurons with response fields that overlap the choice-target contralateral to the recording site (Tin neurons) represent the accumulation of evidence in favor of contralateral target selection. We demonstrate that shortly before a contralateral choice is reported, the population of Tin neurons contains information about the accuracy of the choice (i.e., whether the choice is correct or incorrect). This finding is unexpected because, on average, Tin neurons exhibit a level of activity before the report that is independent of reaction time and evidence strength--both strong predictors of accuracy. This apparent contradiction is resolved by examining the variability in neuronal responses across the population of Tin neurons. While on average, Tin neurons exhibit a stereotyped level of activity before a contralateral choice, many neurons depart from this average in a consistent manner. From these neurons, the accuracy of the choice can be predicted using a simple logistic decoder. The accuracy of the choice predicted from neural activity reproduces the hallmarks of confidence identified in human behavioral experiments. Therefore, neurons that represent evidence accumulation can also inform the monkeys confidence.

neuroscience↗

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.

neuroscience↗

Value construction through sequential sampling explains serial dependencies in decision making

Many decisions are expressed as a preference for one item over another. When these items are familiar, it is often assumed that the decision maker assigns a value to each of the items and chooses the item with the highest value. These values may be imperfectly recalled, but are assumed to be stable over the course of an interview or psychological experiment. Choices that are inconsistent with a stated valuation are thought to occur because of unspecified noise that corrupts the neural representation of value. Assuming that the noise is uncorrelated over time, the pattern of choices and response times in value-based decisions are modeled within the framework of Bounded Evidence Accumulation (BEA), similar to that used in perceptual decision-making. In BEA, noisy evidence samples accumulate over time until the accumulated evidence for one of the options reaches a threshold. Here, we argue that the assumption of temporally uncorrelated noise, while reasonable for perceptual decisions, is not reasonable for value-based decisions. Subjective values depend on the internal state of the decision maker, including their desires, needs, priorities, attentional state, and goals. These internal states may change over time, or undergo revaluation, as will the subjective values. We reasoned that these hypothetical value changes should be detectable in the pattern of choices made over a sequence of decisions. We reanalyzed data from a well-studied task in which participants were presented with pairs of snacks and asked to choose the one they preferred. Using a novel algorithm (Reval), we show that the subjective value of the items changes significantly during a short experimental session (about 1 hour). Values derived with Reval explain choice and response time better than explicitly stated values. They also better explain the BOLD signal in the ventromedial prefrontal cortex, known to represent the value of decision alternatives. Revaluation is also observed in a BEA model in which successive evidence samples are not assumed to be independent. We argue that revaluation is a consequence of the process by which values are constructed during deliberation to resolve preference choices.

neuroscience↗

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.

neuroscience↗

Direct observation of the neural computations underlying a single decision

Neurobiological investigations of perceptual decision-making have furnished the first glimpse of a flexible cognitive process at the level of single neurons (Shadlen and Newsome, 1996; Shadlen and Kiani, 2013). Neurons in the parietal and prefrontal cortex (Kim and Shadlen, 1999; Romo et al., 2004; Hernandez et al., 2002; Ding and Gold, 2012) are thought to represent the accumulation of noisy evidence, acquired over time, leading to a decision. Neural recordings averaged over many decisions have provided support for the deterministic rise in activity to a termination bound (Roitman and Shadlen, 2002). Critically, it is the unobserved stochastic component that is thought to confer variability in both choice and decision time (Gold and Shadlen, 2007). Here, we elucidate this drift-diffusion signal on individual decisions. We recorded simultaneously from hundreds of neurons in the lateral intraparietal cortex (LIP) of monkeys while they made decisions about the direction of random dot motion. We show that a single scalar quantity, derived from the weighted sum of the population activity, represents a combination of deterministic drift and stochastic diffusion. Moreover, we provide direct support for the hypothesis that this drift-diffusion signal approximates the quantity responsible for the variability in choice and reaction times. The population-derived signals rely on a small subset of neurons with response fields that overlap the choice targets. These neurons represent the integral of noisy evidence. Another subset of direction-selective neurons with response fields that overlap the motion stimulus appear to represent the integrand. This parsimonious architecture would escape detection by state-space analyses, absent a clear hypothesis.

neuroscience↗

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.

neuroscience↗

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-makers strategy and support solutions to achieve this goal.

neuroscience↗

Value-based decisions involve sequential sampling from memory

Deciding between two equally appealing options can take considerable time. This observation has puzzled economists and philosophers, because more deliberation only delays the reward. Here we show that this seemingly irrational behavior is explained by the constructive use of memory. Using functional brain imaging in humans, we show that how long it takes to decide between two familiar food items is related to activity in the hippocampus, within specific regions shown to be associated with the retrieval of long-term memories. Moreover, we show that value is partially constructed during deliberation to resolve preference, and this constructive process changes behavior and brain responses. These results render memory as a supplier of evidence in value-based decisions, resolving a central paradox of choice.

animal behavior and cognition↗

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 probability is 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. For each block of 15-42 trials, the base rate favored left or right by a different amount. Participants were not informed of the base rate, 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, that incorporates the evolving belief of the prior, and counterfactual confidence that discounts the prior.

neuroscience↗

Cause for pause before leaping to conclusions about stepping

Many neurons in parietal and prefrontal association cortex undergo gradual changes in firing rate during the formation of some perceptual decisions. These dynamics are often ramp-like increases or decreases depending on the sign and strength of the sensory evidence and are thus hypothesized to represent the accumulation of noisy samples of evidence, analogous to biased diffusion. This idea was challenged recently. An analysis of sequences of action potentials recorded from neurons in the lateral intraparietal cortex (area LIP) suggests that the spikes on single trials are explained by rates that undergo a discrete step from an intermediate rate to either a low or high rate at a random time during deliberation. The average of such steps, like the average of biased diffusion, is consistent with the ramp-like firing rates observed in LIP, but a Bayesian model comparison deemed stepping superior. Here we show that a shortcoming in the mathematical depiction of drift-diffusion led to a severe bias in the model comparison. We conclude that at present there is no compelling evidence that favors the stepping account.

neuroscience↗