Ariel Zylberberg

The brain's router: a cortical network model of serial processing in the primate brain.

The human brain efficiently solves certain operations such as object recognition and categorization through a massively parallel network of dedicated processors. However, human cognition also relies on the ability to perform an arbitrarily large set of tasks by flexibly recombining different processors into a novel chain. This flexibility comes at the cost of a severe slowing down and a seriality of operations (100–500 ms per step). A limit on parallel processing is demonstrated in experimental setups such as the psychological refractory period (PRP) and the attentional blink (AB) in which the processing of an element either significantly delays (PRP) or impedes conscious access (AB) of a second, rapidly presented element. Here we present a spiking-neuron implementation of a cognitive architecture where a large number of local parallel processors assemble together to produce goal-driven behavior. The precise mapping of incoming sensory stimuli onto motor representations relies on a “router” network capable of flexibly interconnecting processors and rapidly changing its configuration from one task to another. Simulations show that, when presented with dual-task stimuli, the network exhibits parallel processing at peripheral sensory levels, a memory buffer capable of keeping the result of sensory processing on hold, and a slow serial performance at the router stage, resulting in a performance bottleneck. The network captures the detailed dynamics of human behavior during dual-task-performance, including both mean RTs and RT distributions, and establishes concrete predictions on neuronal dynamics during dual-task experiments in humans and non-human primates.

The human Turing machine: a neural framework for mental programs.

In recent years much has been learned about how a single computational processing step is implemented in the brain. By contrast, we still have surprisingly little knowledge of the neuronal mechanisms by which multiple such operations are sequentially assembled into mental algorithms. We outline a theory of how individual neural processing steps might be combined into serial programs. We propose a hybrid neuronal device: each step involves massively parallel computation that feeds a slow and serial production system. Production selection is mediated by a system of competing accumulator neurons that extends the role of these neurons beyond the selection of a motor action. Productions change the state of sensory and mnemonic neurons and iteration of such cycles provides a basis for mental programs.

The construction of confidence in a perceptual decision

Decision-making involves the selection of one out of many possible courses of action. A decision may bear on other decisions, as when humans seek a second medical opinion before undergoing a risky surgical intervention. These “meta-decisions” are mediated by confidence judgments—the degree to which decision-makers consider that a choice is likely to be correct. We studied how subjective confidence is constructed from noisy sensory evidence. The psychophysical kernels used to convert sensory information into choice and confidence decisions were precisely reconstructed measuring the impact of small fluctuations in sensory input. This is shown in two independent experiments in which human participants made a decision about the direction of motion of a set of randomly moving dots, or compared the brightness of a group of fluctuating bars, followed by a confidence report. The results of both experiments converged to show that: (1) confidence was influenced by evidence during a short window of time at the initial moments of the decision, and (2) confidence was influenced by evidence for the selected choice but was virtually blind to evidence for the non-selected choice. Our findings challenge classical models of subjective confidence—which posit that the difference of evidence in favor of each choice is the seed of the confidence signal.

A common mechanism underlies changes of mind about decisions and confidence

Decisions are accompanied by a degree of confidence that a selected option is correct. A sequential sampling framework explains the speed and accuracy of decisions and extends naturally to the confidence that the decision rendered is likely to be correct. However, discrepancies between confidence and accuracy suggest that confidence might be supported by mechanisms dissociated from the decision process. Here we show that this discrepancy can arise naturally because of simple processing delays. When participants were asked to report choice and confidence simultaneously, their confidence, reaction time and a perceptual decision about motion were explained by bounded evidence accumulation. However, we also observed revisions of the initial choice and/or confidence. These changes of mind were explained by a continuation of the mechanism that led to the initial choice. Our findings extend the sequential sampling framework to vacillation about confidence and invites caution in interpreting dissociations between confidence and accuracy. DOI: http://dx.doi.org/10.7554/eLife.12192.001

Neurophysiological bases of exponential sensory decay and top-down memory retrieval: a model

Behavioral observations suggest that multiple sensory elements can be maintained for a short time, forming a perceptual buffer which fades after a few hundred milliseconds. Only a subset of this perceptual buffer can be accessed under top-down control and broadcasted to working memory and consciousness. In turn, single-cell studies in awake-behaving monkeys have identified two distinct waves of response to a sensory stimulus: a first transient response largely determined by stimulus properties and a second wave dependent on behavioral relevance, context and learning. Here we propose a simple biophysical scheme which bridges these observations and establishes concrete predictions for neurophsyiological experiments in which the temporal interval between stimulus presentation and top-down allocation is controlled experimentally. Inspired in single-cell observations, the model involves a first transient response and a second stage of amplification and retrieval, which are implemented biophysically by distinct operational modes of the same circuit, regulated by external currents. We explicitly investigated the neuronal dynamics, the memory trace of a presented stimulus and the probability of correct retrieval, when these two stages were bracketed by a temporal gap. The model predicts correctly the dependence of performance with response times in interference experiments suggesting that sensory buffering does not require a specific dedicated mechanism and establishing a direct link between biophysical manipulations and behavioral observations leading to concrete predictions.

Pupil dilation : a fingerprint of temporal selection during the “attentional blink"

Pupil dilation indexes cognitive events of behavioral relevance, like the storage of information to memory and the deployment of attention. Yet, given the slow temporal response of the pupil dilation, it is not known from previous studies whether the pupil can index cognitive events in the short time scale of ∼100 ms. Here we measured the size of the pupil in the Attentional Blink (AB) experiment, a classic demonstration of attentional limitations in processing rapidly presented stimuli. In the AB, two targets embedded in a sequence have to be reported and the second stimulus is often missed if presented between 200 and 500 ms after the first. We show that pupil dilation can be used as a marker of cognitive processing in AB, revealing both the timing and amount of cognitive processing. Specifically, we found that in the time range where the AB is known to occur: (i) the pupil dilation was delayed, mimicking the pattern of response times in the Psychological Refractory Period (PRP) paradigm, (ii) the amplitude of the pupil was reduced relative to that of larger lags, even for correctly identified targets, and (iii) the amplitude of the pupil was smaller for missed than for correctly reported targets. These results support two-stage theories of the Attentional Blink where a second processing stage is delayed inside the interference regime, and indicate that the pupil dilation can be used as a marker of cognitive processing in the time scale of ∼100 ms. Furthermore, given the known relation between the pupil dilation and the activity of the locus coeruleus, our results also support theories that link the serial stage to the action of a specific neuromodulator, norepinephrine.

Individual consistency in the accuracy and distribution of confidence judgments

We examine which aspects of the confidence distributions - its shape, its bias toward higher or lower values, and its ability to distinguish correct from erred trials - are idiosyncratic of the who (individual specificity), the when (variability across days) and the what (task specificity). Measuring confidence across different sessions of four different perceptual tasks we show that: (1) Confidence distributions are virtually identical when measured in different days for the same subject and the same task, constituting a subjective fingerprint, (2) The capacity of confidence reports to distinguish correct from incorrect responses is only modestly (but significantly) correlated when compared across tasks, (3) Confidence distributions are very similar for tasks that involve different sensory modalities but have similar structure, (4) Confidence accuracy is independent of the mean and width of the confidence distribution, (5) The mean of the confidence distribution (an individuals confidence bias) constitutes the most efficient indicator to infer a subjects identity from confidence reports and (6) Confidence bias measured in simple perceptual decisions correlates with an individuals optimism bias measured with standard questionnaire.

Decision Making during the Psychological Refractory Period

In spite of its massively parallel architecture [1], the human brain is fundamentally limited if required to perform two tasks at the same time [2, 3]. This limitation can be studied with the psychological refractory period (PRP) paradigm, where two stimuli that require speeded responses occur in close succession [4]. Interference generally takes the form of a delay in the time to respond to the second stimulus [5]. Previous studies suggested that sensory decisions require the accumulation of sensory evidence [6, 7] and that the PRP reflects the inability to form more than one decision at a time [4, 8]. In the present study, we used a psychophysical reverse-correlation technique [9, 10] to measure the time-course of evidence accumulation during the PRP. We found that the accumulation of evidence could occur during the PRP albeit with a reduced efficiency, which implies that multiple decision processes can occur in parallel in the human brain. In addition to the reduced efficiency of evidence accumulation, our results uncover an additional delay in the routing of the decision to motor structures during the PRP, which implies that the process of sensory decision making is separable from the preparation of a motor response [11-13].

Confidence Is the Bridge between Multi-stage Decisions

Summary Demanding tasks often require a series of decisions to reach a goal. Recent progress in perceptual decision-making has served to unite decision accuracy, speed, and confidence in a common framework of bounded evidence accumulation, furnishing a platform for the study of such multi-stage decisions. In many instances, the strategy applied to each decision, such as the speed-accuracy trade-off, ought to depend on the accuracy of the previous decisions. However, as the accuracy of each decision is often unknown to the decision maker, we hypothesized that subjects may carry forward a level of confidence in previous decisions to affect subsequent decisions. Subjects made two perceptual decisions sequentially and were rewarded only if they made both correctly. The speed and accuracy of individual decisions were explained by noisy evidence accumulation to a terminating bound. We found that subjects adjusted their speed-accuracy setting by elevating the termination bound on the second decision in proportion to their confidence in the first. The findings reveal a novel role for confidence and a degree of flexibility, hitherto unknown, in the brain’s ability to rapidly and precisely modify the mechanisms that control the termination of a decision.

Comment on "Single-trial spike trains in parietal cortex reveal discrete steps during decision-making".

Latimer et al. (Reports, 10 July 2015, p. 184) claim that during perceptual decision formation, parietal neurons undergo one-time, discrete steps in firing rate instead of gradual changes that represent the accumulation of evidence. However, that conclusion rests on unsubstantiated assumptions about the time window of evidence accumulation, and their stepping model cannot explain existing data as effectively as evidence-accumulation models.