Metacognitive evaluation of postdecisional perceptual representations.

Perceptual confidence is thought to arise from metacognitive processes that evaluate the underlying perceptual decision evidence. We investigated whether metacognitive access to perceptual evidence is constrained by the hierarchical organization of visual cortex, where high-level representations tend to be more readily available for explicit scrutiny. We found that the ability of human observers to evaluate their confidence did depend on whether they performed a high-level or low-level task on the same stimuli, but was also affected by manipulations that occurred long after the perceptual decision. Confidence in low-level perceptual decisions degraded with more time between the decision and the response cue, especially when backward masking was present. Confidence in high-level tasks was immune to backward masking and benefitted from additional time. These results can be explained by a model assuming confidence heavily relies on postdecisional internal representations of visual stimuli that degrade over time, where high-level representations are more persistent.

The Human Brain Encodes a Chronicle of Visual Events at Each Instant of Time Through the Multiplexing of Traveling Waves.

The human brain continuously processes streams of visual input. Yet, a single image typically triggers neural responses that extend beyond 1s. To understand how the brain encodes and maintains successive images, we analyzed with electroencephalography the brain activity of human subjects while they watched ∼5000 visual stimuli presented in fast sequences. First, we confirm that each stimulus can be decoded from brain activity for ∼1s, and we demonstrate that the brain simultaneously represents multiple images at each time instant. Second, we source localize the corresponding brain responses in the expected visual hierarchy and show that distinct brain regions represent, at each time instant, different snapshots of past stimulations. Third, we propose a simple framework to further characterize the dynamical system of these traveling waves. Our results show that a chain of neural circuits, which each consist of (1) a hidden maintenance mechanism and (2) an observable update mechanism, accounts for the dynamics of macroscopic brain representations elicited by visual sequences. Together, these results detail a simple architecture explaining how successive visual events and their respective timings can be simultaneously represented in the brain.SIGNIFICANCE STATEMENT Our retinas are continuously bombarded with a rich flux of visual input. Yet, how our brain continuously processes such visual streams is a major challenge to neuroscience. Here, we developed techniques to decode and track, from human brain activity, multiple images flashed in rapid succession. Our results show that the brain simultaneously represents multiple successive images at each time instant by multiplexing them along a neural cascade. Dynamical modeling shows that these results can be explained by a hierarchy of neural assemblies that continuously propagate multiple visual contents. Overall, this study sheds new light on the biological basis of our visual experience.

Motor Coordination and Strategic Cooperation in Joint Action.

Naturalistic joint action between two agents typically requires both motor coordination and strategic cooperation. However, these two fundamental processes have systematically been studied independently. We presented 50 dyads of adult participants with a novel collaborative task that combined different levels of motor noise with different levels of strategic noise, to determine whether the sense of agency (the experience of control over an action) reflects the interplay between these low-level (motor) and high-level (strategic) dimensions. We also examined how dominance in motor control could influence prosocial behaviors. We found that self-agency was particularly dependent on motor cues, whereas joint agency was particularly dependent on strategic cues. We suggest that the prime importance of strategic cues to joint agency reflects the co-representation of coagents' interests during the task. Furthermore, we observed a reduction in prosocial strategies in agents who exerted dominant motor control over joint action, showing that the strategic dimension of human interactions is also susceptible to the influence of low-level motor characteristics.

Leveraging decision consistency to decompose suboptimality in terms of its ultimate predictability.

Although the suboptimality of perceptual decision making is indisputable in its strictest sense, characterizing the nature of suboptimalities constitutes a valuable drive for future research. I argue that decision consistency offers a rarely measured, yet important behavioral metric for decomposing suboptimality (or, more generally, deviations from any candidate model of decision making) into ultimately predictable and inherently unpredictable components.

Temporal Prediction in lieu of Periodic Stimulation.

Predicting not only what will happen, but also when it will happen is extremely helpful for optimizing perception and action. Temporal predictions driven by periodic stimulation increase perceptual sensitivity and reduce response latencies. At the neurophysiological level, a single mechanism has been proposed to mediate this twofold behavioral improvement: the rhythmic entrainment of slow cortical oscillations to the stimulation rate. However, temporal regularities can occur in aperiodic contexts, suggesting that temporal predictions per se may be dissociable from entrainment to periodic sensory streams. We investigated this possibility in two behavioral experiments, asking human participants to detect near-threshold auditory tones embedded in streams whose temporal and spectral properties were manipulated. While our findings confirm that periodic stimulation reduces response latencies, in agreement with the hypothesis of a stimulus-driven entrainment of neural excitability, they further reveal that this motor facilitation can be dissociated from the enhancement of auditory sensitivity. Perceptual sensitivity improvement is unaffected by the nature of temporal regularities (periodic vs aperiodic), but contingent on the co-occurrence of a fulfilled spectral prediction. Altogether, the dissociation between predictability and periodicity demonstrates that distinct mechanisms flexibly and synergistically operate to facilitate perception and action.

Conscious Vision Proceeds from Global to Local Content in Goal-Directed Tasks and Spontaneous Vision.

UNLABELLED: The reverse hierarchy theory (Hochstein and Ahissar, 2002) makes strong, but so far untested, predictions on conscious vision. In this theory, local details encoded in lower-order visual areas are unconsciously processed before being automatically and rapidly combined into global information in higher-order visual areas, where conscious percepts emerge. Contingent on current goals, local details can afterward be consciously retrieved. This model therefore predicts that (1) global information is perceived faster than local details, (2) global information is computed regardless of task demands during early visual processing, and (3) spontaneous vision is dominated by global percepts. We designed novel textured stimuli that are, as opposed to the classic Navon's letters, truly hierarchical (i.e., where global information is solely defined by local information but where local and global orientations can still be manipulated separately). In line with the predictions, observers were systematically faster reporting global than local properties of those stimuli. Second, global information could be decoded from magneto-encephalographic data during early visual processing regardless of task demands. Last, spontaneous subjective reports were dominated by global information and the frequency and speed of spontaneous global perception correlated with the accuracy and speed in the global task. No such correlation was observed for local information. We therefore show that information at different levels of the visual hierarchy is not equally likely to become conscious; rather, conscious percepts emerge preferentially at a global level. We further show that spontaneous reports can be reliable and are tightly linked to objective performance at the global level. SIGNIFICANCE STATEMENT: Is information encoded at different levels of the visual system (local details in low-level areas vs global shapes in high-level areas) equally likely to become conscious? We designed new hierarchical stimuli and provide the first empirical evidence based on behavioral and MEG data that global information encoded at high levels of the visual hierarchy dominates perception. This result held both in the presence and in the absence of task demands. The preferential emergence of percepts at high levels can account for two properties of conscious vision, namely, the dominance of global percepts and the feeling of visual richness reported independently of the perception of local details.

Neural mechanisms of human perceptual choice under focused and divided attention.

Perceptual decisions occur after the evaluation and integration of momentary sensory inputs, and dividing attention between spatially disparate sources of information impairs decision performance. However, it remains unknown whether dividing attention degrades the precision of sensory signals, precludes their conversion into decision signals, or dampens the integration of decision information toward an appropriate response. Here we recorded human electroencephalographic (EEG) activity while participants categorized one of two simultaneous and independent streams of visual gratings according to their average tilt. By analyzing trial-by-trial correlations between EEG activity and the information offered by each sample, we obtained converging behavioral and neural evidence that dividing attention between left and right visual fields does not dampen the encoding of sensory or decision information. Under divided attention, momentary decision information from both visual streams was encoded in slow parietal signals without interference but was lost downstream during their integration as reflected in motor mu- and beta-band (10-30 Hz) signals, resulting in a "leaky" accumulation process that conferred greater behavioral influence to more recent samples. By contrast, sensory inputs that were explicitly cued as irrelevant were not converted into decision signals. These findings reveal that a late cognitive bottleneck on information integration limits decision performance under divided attention, and places new capacity constraints on decision-theoretic models of information integration under cognitive load.

Dissociable prior influences of signal probability and relevance on visual contrast sensitivity.

According to signal detection theoretical analyses, visual signals occurring at a cued location are detected more accurately, whereas frequently occurring ones are reported more often but are not better distinguished from noise. However, conventional analyses that estimate sensitivity and bias by comparing true- and false-positive rates offer limited insights into the mechanisms responsible for these effects. Here, we reassessed the prior influences of signal probability and relevance on visual contrast detection using a reverse-correlation technique that quantifies how signal-like fluctuations in noise predict trial-to-trial variability in choice discarded by conventional analyses. This approach allowed us to estimate separately the sensitivity of true and false positives to parametric changes in signal energy. We found that signal probability and relevance both increased energy sensitivity, but in dissociable ways. Cues predicting the relevant location increased primarily the sensitivity of true positives by suppressing internal noise during signal processing, whereas cues predicting greater signal probability increased both the frequency and the sensitivity of false positives by biasing the baseline activity of signal-selective units. We interpret these findings in light of "predictive-coding" models of perception, which propose separable top-down influences of expectation (probability driven) and attention (relevance driven) on bottom-up sensory processing.

Feature expectation heightens visual sensitivity during fine orientation discrimination.

Attending to a stimulus enhances the sensitivity of perceptual decisions. However, it remains unclear how perceptual sensitivity varies according to whether a feature is expected or unexpected. Here, observers made fine discrimination judgments about the orientation of visual gratings embedded in low spatial-frequency noise, and psychophysical reverse correlation was used to estimate decision 'kernels' that revealed how visual features influenced choices. Orthogonal cues alerted subjects to which of two spatial locations was likely to be probed (spatial attention cue) and which of two oriented gratings was likely to occur (feature expectation cue). When an expected (relative to unexpected) feature occurred, decision kernels shifted away from the category boundary, allowing observers to capitalize on more informative, "off-channel" stimulus features. By contrast, the spatial attention cue had a multiplicative influence on decision kernels, consistent with an increase in response gain. Feature expectation thus heightens sensitivity to the most informative visual features, independent of selective attention.

Temporal expectation enhances contrast sensitivity by phase entrainment of low-frequency oscillations in visual cortex.

Although it is increasingly accepted that temporal expectation can modulate early perceptual processing, the underlying neural computations remain unknown. In the present study, we combined a psychophysical paradigm with electrophysiological recordings to investigate the putative contribution of low-frequency oscillatory activity in mediating the modulation of visual perception by temporal expectation. Human participants judged the orientation of brief targets (visual Gabor patterns tilted clockwise or counterclockwise) embedded within temporally regular or irregular streams of noise-patches used as temporal cues. Psychophysical results indicated that temporal expectation enhanced the contrast sensitivity of visual targets. A diffusion model indicated that rhythmic temporal expectation modulated the signal-to-noise gain of visual processing. The concurrent electrophysiological data revealed that the phase of delta oscillations overlying human visual cortex (1-4 Hz) was predictive of the quality of target processing only in regular streams of events. Moreover, in the regular condition, the optimum phase of these perception-predictive oscillations occurred in anticipation of the expected events. Together, these results show a strong correspondence between psychophysical and neurophysiological data, suggesting that the phase entrainment of low-frequency oscillations to external sensory cues can serve as an important and flexible mechanism for enhancing sensory processing.

Specifying the timescale of early life unpredictability helps explain the development of internalising and externalising behaviours.

Early life unpredictability is associated with both physical and mental health outcomes throughout the life course. Here, we classified adverse experiences based on the timescale on which they are likely to introduce variability in children's environments: variations unfolding over short time scales (e.g., hours, days, weeks) and labelled Stochasticity vs variations unfolding over longer time scales (e.g., months, years) and labelled Volatility and explored how they contribute to the development of problem behaviours. Results indicate that externalising behaviours at age 9 and 15 and internalising behaviours at age 15 were better accounted for by models that separated Stochasticity and Volatility measured at ages 3 to 5. Both externalising and internalising behaviours were specifically associated with Volatility, with larger effects for externalising behaviours. These findings are interpreted in light of evolutionary-developmental models of psychopathology and reinforcement learning models of learning under uncertainty.

Temporal expectation improves the quality of sensory information.

It is increasingly clear that we extract patterns of temporal regularity between events to optimize information processing. Whereas some of the mechanisms for facilitating action preparation and execution have been well documented, much less is understood about whether and how temporal expectations influence visual perception. We used a psychophysical paradigm and computational modeling to investigate the mechanisms by which temporal expectation can modulate visual perception. Visual targets appeared in a stream of noise-patches separated by a fixed (400 ms regular condition) or jittered (200/300/400/500/600 ms irregular condition) intervals. Targets were visual gratings tilted 45° clockwise or counter-clockwise, presented at one of seven contrast levels. Human observers were required to perform an orientation discrimination (i.e., left or right). Psychometric functions for contrast sensitivity fitted for the regular and irregular conditions indicated that temporal expectation modulates perceptual processing by enhancing the contrast sensitivity of visual targets. This increase in the signal strength was accompanied by a reduction in reaction times. A diffusion model indicated that rhythmic temporal expectation enhanced the signal-to-noise gain of the sensory evidence upon which decisions were made. These effects support the idea that temporal structure of external events can entrain the attentional focus and psychophysical data, optimizing the processing of relevant sensory information.

Effects of decision variables and intraparietal stimulation on sensorimotor oscillatory activity in the human brain.

To decide effectively, information must not only be integrated from multiple sources, but it must be distributed across the brain if it is to influence structures such as motor cortex that execute choices. Human participants integrated information from multiple, but only partially informative, cues in a probabilistic reasoning task in an optimal manner. We tested whether lateralization of alpha- and beta-band oscillatory brain activity over sensorimotor cortex reflected decision variables such as the sum of the evidence provided by observed cues, a key quantity for decision making, and whether this could be dissociated from an update signal reflecting processing of the most recent cue stimulus. Alpha- and beta-band activity in the electroencephalogram reflected the logarithm of the likelihood ratio associated with the each piece of information witnessed, and the same quantity associated with the previous cues. Only the beta-band, however, reflected the most recent cue in a manner that suggested it reflected updating processes associated with cue processing. In a second experiment, transcranial magnetic stimulation-induced disruption was used to demonstrate that the intraparietal sulcus played a causal role both in decision making and in the appearance of sensorimotor beta-band activity.

Adaptive tuning of human learning and choice variability to unexpected uncertainty.

Human value-based decisions are notably variable under uncertainty. This variability is known to arise from two distinct sources: variable choices aimed at exploring available options and imprecise learning of option values due to limited cognitive resources. However, whether these two sources of decision variability are tuned to their specific costs and benefits remains unclear. To address this question, we compared the effects of expected and unexpected uncertainty on decision-making in the same reinforcement learning task. Across two large behavioral datasets, we found that humans choose more variably between options but simultaneously learn less imprecisely their values in response to unexpected uncertainty. Using simulations of learning agents, we demonstrate that these opposite adjustments reflect adaptive tuning of exploration and learning precision to the structure of uncertainty. Together, these findings indicate that humans regulate not only how much they explore uncertain options but also how precisely they learn the values of these options.

A zero-cost attention-based approach to promote cleaner streets: A Signal Detection Theory approach in Parisian streets.

In an effort to inform interventions targeting littering behaviour, we estimate how much a change in trash-bag colour increases trash can visibility in Paris. To that end, we applied standard Signal Detection techniques to test how much changing trash-bag colour affects subjects' trash can detection rates. In three pre-registered studies, we found that changing trash bag colour from grey to either red, green or blue considerably increases the perception of bins in British (tourist) and Parisian (resident) samples. We found that changing the bag colour from grey to blue increased visibility the most.

Efficient stabilization of imprecise statistical inference through conditional belief updating.

Statistical inference is the optimal process for forming and maintaining accurate beliefs about uncertain environments. However, human inference comes with costs due to its associated biases and limited precision. Indeed, biased or imprecise inference can trigger variable beliefs and unwarranted changes in behaviour. Here, by studying decisions in a sequential categorization task based on noisy visual stimuli, we obtained converging evidence that humans reduce the variability of their beliefs by updating them only when the reliability of incoming sensory information is judged as sufficiently strong. Instead of integrating the evidence provided by all stimuli, participants actively discarded as much as a third of stimuli. This conditional belief updating strategy shows good test-retest reliability, correlates with perceptual confidence and explains human behaviour better than previously described strategies. This seemingly suboptimal strategy not only reduces the costs of imprecise computations but also, counterintuitively, increases the accuracy of resulting decisions.

Premature commitment to uncertain decisions during human NMDA receptor hypofunction.

Making accurate decisions based on unreliable sensory evidence requires cognitive inference. Dysfunction of n-methyl-d-aspartate (NMDA) receptors impairs the integration of noisy input in theoretical models of neural circuits, but whether and how this synaptic alteration impairs human inference and confidence during uncertain decisions remains unknown. Here we use placebo-controlled infusions of ketamine to characterize the causal effect of human NMDA receptor hypofunction on cognitive inference and its neural correlates. At the behavioral level, ketamine triggers inference errors and elevated decision uncertainty. At the neural level, ketamine is associated with imbalanced coding of evidence and premature response preparation in electroencephalographic (EEG) activity. Through computational modeling of inference and confidence, we propose that this specific pattern of behavioral and neural impairments reflects an early commitment to inaccurate decisions, which aims at resolving the abnormal uncertainty generated by NMDA receptor hypofunction.

Controllability boosts neural and cognitive signatures of changes-of-mind in uncertain environments.

In uncertain environments, seeking information about alternative choice options is essential for adaptive learning and decision-making. However, information seeking is usually confounded with changes-of-mind about the reliability of the preferred option. Here, we exploited the fact that information seeking requires control over which option to sample to isolate its behavioral and neurophysiological signatures. We found that changes-of-mind occurring with control require more evidence against the current option, are associated with reduced confidence, but are nevertheless more likely to be confirmed on the next decision. Multimodal neurophysiological recordings showed that these changes-of-mind are preceded by stronger activation of the dorsal attention network in magnetoencephalography, and followed by increased pupil-linked arousal during the presentation of decision outcomes. Together, these findings indicate that information seeking increases the saliency of evidence perceived as the direct consequence of one's own actions.

Endogenous modulation of low frequency oscillations by temporal expectations.

Recent studies have associated increasing temporal expectations with synchronization of higher frequency oscillations and suppression of lower frequencies. In this experiment, we explore a proposal that low-frequency oscillations provide a mechanism for regulating temporal expectations. We used a speeded Go/No-go task and manipulated temporal expectations by changing the probability of target presentation after certain intervals. Across two conditions, the temporal conditional probability of target events differed substantially at the first of three possible intervals. We found that reactions times differed significantly at this first interval across conditions, decreasing with higher temporal expectations. Interestingly, the power of theta activity (4-8 Hz), distributed over central midline sites, also differed significantly across conditions at this first interval. Furthermore, we found a transient coupling between theta phase and beta power after the first interval in the condition with high temporal expectation for targets at this time point. Our results suggest that the adjustments in theta power and the phase-power coupling between theta and beta contribute to a central mechanism for controlling neural excitability according to temporal expectations.

Separable neural signatures of confidence during perceptual decisions.

Perceptual confidence is an evaluation of the validity of perceptual decisions. While there is behavioural evidence that confidence evaluation differs from perceptual decision-making, disentangling these two processes remains a challenge at the neural level. Here, we examined the electrical brain activity of human participants in a protracted perceptual decision-making task where observers tend to commit to perceptual decisions early whilst continuing to monitor sensory evidence for evaluating confidence. Premature decision commitments were revealed by patterns of spectral power overlying motor cortex, followed by an attenuation of the neural representation of perceptual decision evidence. A distinct neural representation was associated with the computation of confidence, with sources localised in the superior parietal and orbitofrontal cortices. In agreement with a dissociation between perception and confidence, these neural resources were recruited even after observers committed to their perceptual decisions, and thus delineate an integral neural circuit for evaluating perceptual decision confidence.