A disinhibitory circuit mechanism explains a general principle of peak performance during mid-level arousal.

Perceptual decision-making is highly dependent on the momentary arousal state of the brain, which fluctuates over time on a scale of hours, minutes, and even seconds. The textbook relationship between momentary arousal and task performance is captured by an inverted U-shape, as put forward in the Yerkes-Dodson law. This law suggests optimal performance at moderate levels of arousal and impaired performance at low or high arousal levels. However, despite its popularity, the evidence for this relationship in humans is mixed at best. Here, we use pupil-indexed arousal and performance data from various perceptual decision-making tasks to provide converging evidence for the inverted U-shaped relationship between spontaneous arousal fluctuations and performance across different decision types (discrimination, detection) and sensory modalities (visual, auditory). To further understand this relationship, we built a neurobiologically plausible mechanistic model and show that it is possible to reproduce our findings by incorporating two types of interneurons that are both modulated by an arousal signal. The model architecture produces two dynamical regimes under the influence of arousal: one regime in which performance increases with arousal and another regime in which performance decreases with arousal, together forming an inverted U-shaped arousal-performance relationship. We conclude that the inverted U-shaped arousal-performance relationship is a general and robust property of sensory processing. It might be brought about by the influence of arousal on two types of interneurons that together act as a disinhibitory pathway for the neural populations that encode the available sensory evidence used for the decision.

Predictions and rewards affect decision-making but not subjective experience.

To survive, organisms constantly make decisions to avoid danger and maximize rewards in information-rich environments. As a result, decisions about sensory input are not only driven by sensory information but also by other factors, such as the expected rewards of a decision (known as the payoff matrix) or by information about temporal regularities in the environment (known as cognitive priors or predictions). However, it is unknown to what extent these different types of information affect subjective experience or whether they merely result in nonperceptual response criterion shifts. To investigate this question, we used three carefully matched manipulations that typically result in behavioral shifts in decision criteria: a visual illusion (Müller-Lyer condition), a punishment scheme (payoff condition), and a change in the ratio of relevant stimuli (base rate condition). To gauge shifts in subjective experience, we introduce a task in which participants not only make decisions about what they have just seen but are also asked to reproduce their experience of a target stimulus. Using Bayesian ordinal modeling, we show that each of these three manipulations affects the decision criterion as intended but that the visual illusion uniquely affects sensory experience as measured by reproduction. In a series of follow-up experiments, we use computational modeling to show that although the visual illusion results in a distinct drift-diffusion (DDM) parameter profile relative to nonsensory manipulations, reliance on DDM parameter estimates alone is not sufficient to ascertain whether a given manipulation is perceptual or nonperceptual.

The human visual system differentially represents subjectively and objectively invisible stimuli.

The study of unconscious processing requires a measure of conscious awareness. Awareness measures can be either subjective (based on participant's report) or objective (based on perceptual performance). The preferred awareness measure depends on the theoretical position about consciousness and may influence conclusions about the extent of unconscious processing and about the neural correlates of consciousness. We obtained functional magnetic resonance imaging (fMRI) measurements from 43 subjects while they viewed masked faces and houses that were either subjectively or objectively invisible. Even for objectively invisible (perceptually indiscriminable) stimuli, we found significant category information in both early, lower-level visual areas and in higher-level visual cortex, although representations in anterior, category-selective ventrotemporal areas were less robust. For subjectively invisible stimuli, similar to visible stimuli, there was a clear posterior-to-anterior gradient in visual cortex, with stronger category information in ventrotemporal cortex than in early visual cortex. For objectively invisible stimuli, however, category information remained virtually unchanged from early visual cortex to object- and category-selective visual areas. These results demonstrate that although both objectively and subjectively invisible stimuli are represented in visual cortex, the extent of unconscious information processing is influenced by the measurement approach. Furthermore, our data show that subjective and objective approaches are associated with different neural correlates of consciousness and thus have implications for neural theories of consciousness.

How (not) to demonstrate unconscious priming: Overcoming issues with post-hoc data selection, low power, and frequentist statistics.

One widely used scientific approach to studying consciousness involves contrasting conscious operations with unconscious ones. However, challenges in establishing the absence of conscious awareness have led to debates about the extent and existence of unconscious processes. We collected experimental data on unconscious semantic priming, manipulating prime presentation duration to highlight the critical role of the analysis approach in attributing priming effects to unconscious processing. We demonstrate that common practices like post-hoc data selection, low statistical power, and frequentist statistical testing can erroneously support claims of unconscious priming. Conversely, adopting best practices like direct performance-awareness contrasts, Bayesian tests, and increased statistical power can prevent such erroneous conclusions. Many past experiments, including our own, fail to meet these standards, casting doubt on previous claims about unconscious processing. Implementing these robust practices will enhance our understanding of unconscious processing and shed light on the functions and neural mechanisms of consciousness.

A Silent Disco: Differential Effects of Beat-based and Pattern-based Temporal Expectations on Persistent Entrainment of Low-frequency Neural Oscillations.

The brain uses temporal structure in the environment, like rhythm in music and speech, to predict the timing of events, thereby optimizing their processing and perception. Temporal expectations can be grounded in different aspects of the input structure, such as a regular beat or a predictable pattern. One influential account posits that a generic mechanism underlies beat-based and pattern-based expectations, namely, entrainment of low-frequency neural oscillations to rhythmic input, whereas other accounts assume different underlying neural mechanisms. Here, we addressed this outstanding issue by examining EEG activity and behavioral responses during silent periods following rhythmic auditory sequences. We measured responses outlasting the rhythms both to avoid confounding the EEG analyses with evoked responses, and to directly test whether beat-based and pattern-based expectations persist beyond stimulation, as predicted by entrainment theories. To properly disentangle beat-based and pattern-based expectations, which often occur simultaneously, we used non-isochronous rhythms with a beat, a predictable pattern, or random timing. In Experiment 1 (n = 32), beat-based expectations affected behavioral ratings of probe events for two beat-cycles after the end of the rhythm. The effects of pattern-based expectations reflected expectations for one interval. In Experiment 2 (n = 27), using EEG, we found enhanced spectral power at the beat frequency for beat-based sequences both during listening and silence. For pattern-based sequences, enhanced power at a pattern-specific frequency was present during listening, but not silence. Moreover, we found a difference in the evoked signal following pattern-based and beat-based sequences. Finally, we show how multivariate pattern decoding and multiscale entropy-measures sensitive to non-oscillatory components of the signal-can be used to probe temporal expectations. Together, our results suggest that the input structure used to form temporal expectations may affect the associated neural mechanisms. We suggest climbing activity and low-frequency oscillations may be differentially associated with pattern-based and beat-based expectations.

Broadband Dynamics Rather than Frequency-Specific Rhythms Underlie Prediction Error in the Primate Auditory Cortex.

Detection of statistical irregularities, measured as a prediction error response, is fundamental to the perceptual monitoring of the environment. We studied whether prediction error response is associated with neural oscillations or asynchronous broadband activity. Electrocorticography was conducted in three male monkeys, who passively listened to the auditory roving oddball stimuli. Local field potentials (LFPs) recorded over the auditory cortex underwent spectral principal component analysis, which decoupled broadband and rhythmic components of the LFP signal. We found that the broadband component captured the prediction error response, whereas none of the rhythmic components were associated with statistical irregularities of sounds. The broadband component displayed more stochastic, asymmetrical multifractal properties than the rhythmic components, which revealed more self-similar dynamics. We thus conclude that the prediction error response is captured by neuronal populations generating asynchronous broadband activity, defined by irregular dynamic states, which, unlike oscillatory rhythms, appear to enable the neural representation of auditory prediction error response.SIGNIFICANCE STATEMENT This study aimed to examine the contribution of oscillatory and asynchronous components of auditory local field potentials in the generation of prediction error responses to sensory irregularities, as this has not been directly addressed in the previous studies. Here, we show that mismatch negativity-an auditory prediction error response-is driven by the asynchronous broadband component of potentials recorded in the auditory cortex. This finding highlights the importance of nonoscillatory neural processes in the predictive monitoring of the environment. At a more general level, the study demonstrates that stochastic neural processes, which are often disregarded as neural noise, do have a functional role in the processing of sensory information.

Beta and Theta Oscillations Differentially Support Free Versus Forced Control over Multiple-Target Search.

Many important situations require human observers to simultaneously search for more than one object. Despite a long history of research into visual search, the behavioral and neural mechanisms associated with multiple-target search are poorly understood. Here we test the novel theory that the efficiency of looking for multiple targets critically depends on the mode of cognitive control the environment affords to the observer. We used an innovative combination of electroencephalogram (EEG) and eye tracking while participants searched for two targets, within two different contexts: either both targets were present in the search display and observers were free to prioritize either one of them, thus enabling proactive control over selection; or only one of the two targets would be present in each search display, which requires reactive control to reconfigure selection when the wrong target has been prioritized. During proactive control, both univariate and multivariate signals of beta-band (15-35 Hz) power suppression before display onset predicted switches between target selections. This signal originated over midfrontal and sensorimotor regions and has previously been associated with endogenous state changes. In contrast, imposed target selections requiring reactive control elicited prefrontal power enhancements in the delta/theta band (2-8 Hz), but only after display onset. This signal predicted individual differences in associated oculomotor switch costs, reflecting reactive reconfiguration of target selection. The results provide compelling evidence that multiple target representations are differentially prioritized during visual search, and for the first time reveal distinct neural mechanisms underlying proactive and reactive control over multiple-target search.SIGNIFICANCE STATEMENT Searching for more than one object in complex visual scenes can be detrimental for search performance. Although perhaps annoying in daily life, this can have severe consequences in professional settings such as medical and security screening. Previous research has not yet resolved whether multiple-target search involves changing priorities in what people attend to, and how such changes are controlled. We approached these questions by concurrently measuring cortical activity and eye movements using EEG and eye tracking while observers searched for multiple possible targets. Our findings provide the first unequivocal support for the existence of two modes of control during multiple-target search, which are expressed in qualitatively distinct time-frequency signatures of the EEG both before and after visual selection.

Perceptual integration without conscious access.

The visual system has the remarkable ability to integrate fragmentary visual input into a perceptually organized collection of surfaces and objects, a process we refer to as perceptual integration. Despite a long tradition of perception research, it is not known whether access to consciousness is required to complete perceptual integration. To investigate this question, we manipulated access to consciousness using the attentional blink. We show that, behaviorally, the attentional blink impairs conscious decisions about the presence of integrated surface structure from fragmented input. However, despite conscious access being impaired, the ability to decode the presence of integrated percepts remains intact, as shown through multivariate classification analyses of electroencephalogram (EEG) data. In contrast, when disrupting perception through masking, decisions about integrated percepts and decoding of integrated percepts are impaired in tandem, while leaving feedforward representations intact. Together, these data show that access consciousness and perceptual integration can be dissociated.

Frontal cortex differentiates between free and imposed target selection in multiple-target search.

Cognitive control can involve proactive (preparatory) and reactive (corrective) mechanisms. Using a gaze-contingent eye tracking paradigm combined with fMRI, we investigated the involvement of these different modes of control and their underlying neural networks, when switching between different targets in multiple-target search. Participants simultaneously searched for two possible targets presented among distractors, and selected one of them. In one condition, only one of the targets was available in each display, so that the choice was imposed, and reactive control would be required. In the other condition, both targets were present, giving observers free choice over target selection, and allowing for proactive control. Switch costs emerged only when targets were imposed and not when target selection was free. We found differential levels of activity in the frontoparietal control network depending on whether target switches were free or imposed. Furthermore, we observed core regions of the default mode network to be active during target repetitions, indicating reduced control on these trials. Free and imposed switches jointly activated parietal and posterior frontal cortices, while free switches additionally activated anterior frontal cortices. These findings highlight unique contributions of proactive and reactive control during visual search.

Lack of Free Choice Reveals the Cost of Having to Search for More Than One Object.

It is debated whether people can actively search for more than one object or whether this results in switch costs. Using a gaze-contingent eye-tracking paradigm, we revealed a crucial role for cognitive control in multiple-target search. We instructed participants to simultaneously search for two target objects presented among distractors. In one condition, both targets were available, which gave the observer free choice of what to search for and allowed for proactive control. In the other condition, only one of the two targets was available, so that the choice was imposed, and a reactive mechanism would be required. No switch costs emerged when target choice was free, but switch costs emerged reliably when targets were imposed. Bridging contradictory findings, the results are consistent with models of visual selection in which only one attentional template actively drives selection and in which the efficiency of switching targets depends on the type of cognitive control allowed for by the environment.

NMDA Receptor Antagonist Ketamine Distorts Object Recognition by Reducing Feedback to Early Visual Cortex.

It is a well-established fact that top-down processes influence neural representations in lower-level visual areas. Electrophysiological recordings in monkeys as well as theoretical models suggest that these top-down processes depend on NMDA receptor functioning. However, this underlying neural mechanism has not been tested in humans. We used fMRI multivoxel pattern analysis to compare the neural representations of ambiguous Mooney images before and after they were recognized with their unambiguous grayscale version. Additionally, we administered ketamine, an NMDA receptor antagonist, to interfere with this process. Our results demonstrate that after recognition, the pattern of brain activation elicited by a Mooney image is more similar to that of its easily recognizable grayscale version than to the pattern evoked by the identical Mooney image before recognition. Moreover, recognition of Mooney images decreased mean response; however, neural representations of separate images became more dissimilar. So from the neural perspective, unrecognizable Mooney images all "look the same", whereas recognized Mooneys look different. We observed these effects in posterior fusiform part of lateral occipital cortex and in early visual cortex. Ketamine distorted these effects of recognition, but in early visual cortex only. This suggests that top-down processes from higher- to lower-level visual areas might operate via an NMDA pathway.

Neuronal integration in visual cortex elevates face category tuning to conscious face perception.

The human brain has the extraordinary capability to transform cluttered sensory input into distinct object representations. For example, it is able to rapidly and seemingly without effort detect object categories in complex natural scenes. Surprisingly, category tuning is not sufficient to achieve conscious recognition of objects. What neural process beyond category extraction might elevate neural representations to the level where objects are consciously perceived? Here we show that visible and invisible faces produce similar category-selective responses in the ventral visual cortex. The pattern of neural activity evoked by visible faces could be used to decode the presence of invisible faces and vice versa. However, only visible faces caused extensive response enhancements and changes in neural oscillatory synchronization, as well as increased functional connectivity between higher and lower visual areas. We conclude that conscious face perception is more tightly linked to neural processes of sustained information integration and binding than to processes accommodating face category tuning.

Seeing without knowing: neural signatures of perceptual inference in the absence of report.

Every day, we experience a rich and complex visual world. Our brain constantly translates meaningless fragmented input into coherent objects and scenes. However, our attentional capabilities are limited, and we can only report the few items that we happen to attend to. So what happens to items that are not cognitively accessed? Do these remain fragmentary and meaningless? Or are they processed up to a level where perceptual inferences take place about image composition? To investigate this, we recorded brain activity using fMRI while participants viewed images containing a Kanizsa figure, an illusion in which an object is perceived by means of perceptual inference. Participants were presented with the Kanizsa figure and three matched nonillusory control figures while they were engaged in an attentionally demanding distractor task. After the task, one group of participants was unable to identify the Kanizsa figure in a forced-choice decision task; hence, they were "inattentionally blind." A second group had no trouble identifying the Kanizsa figure. Interestingly, the neural signature that was unique to the processing of the Kanizsa figure was present in both groups. Moreover, within-subject multivoxel pattern analysis showed that the neural signature of unreported Kanizsa figures could be used to classify reported Kanizsa figures and that this cross-report classification worked better for the Kanizsa condition than for the control conditions. Together, these results suggest that stimuli that are not cognitively accessed are processed up to levels of perceptual interpretation.

Accurate metacognition for visual sensory memory representations.

The capacity to attend to multiple objects in the visual field is limited. However, introspectively, people feel that they see the whole visual world at once. Some scholars suggest that this introspective feeling is based on short-lived sensory memory representations, whereas others argue that the feeling of seeing more than can be attended to is illusory. Here, we investigated this phenomenon by combining objective memory performance with subjective confidence ratings during a change-detection task. This allowed us to compute a measure of metacognition--the degree of knowledge that subjects have about the correctness of their decisions--for different stages of memory. We show that subjects store more objects in sensory memory than they can attend to but, at the same time, have similar metacognition for sensory memory and working memory representations. This suggests that these subjective impressions are not an illusion but accurate reflections of the richness of visual perception.

Catecholaminergic neuromodulation and selective attention jointly shape perceptual decision-making.

Perceptual decisions about sensory input are influenced by fluctuations in ongoing neural activity, most prominently driven by attention and neuromodulator systems. It is currently unknown if neuromodulator activity and attention differentially modulate perceptual decision-making and/or whether neuromodulatory systems in fact control attentional processes. To investigate the effects of two distinct neuromodulatory systems and spatial attention on perceptual decisions, we pharmacologically elevated cholinergic (through donepezil) and catecholaminergic (through atomoxetine) levels in humans performing a visuo-spatial attention task, while we measured electroencephalography (EEG). Both attention and catecholaminergic enhancement improved decision-making at the behavioral and algorithmic level, as reflected in increased perceptual sensitivity and the modulation of the drift rate parameter derived from drift diffusion modeling. Univariate analyses of EEG data time-locked to the attentional cue, the target stimulus, and the motor response further revealed that attention and catecholaminergic enhancement both modulated pre-stimulus cortical excitability, cue- and stimulus-evoked sensory activity, as well as parietal evidence accumulation signals. Interestingly, we observed both similar, unique, and interactive effects of attention and catecholaminergic neuromodulation on these behavioral, algorithmic, and neural markers of the decision-making process. Thereby, this study reveals an intricate relationship between attentional and catecholaminergic systems and advances our understanding about how these systems jointly shape various stages of perceptual decision-making.

An academic survey on theoretical foundations, common assumptions and the current state of consciousness science.

We report the results of an academic survey into the theoretical and methodological foundations, common assumptions, and the current state of the field of consciousness research. The survey consisted of 22 questions and was distributed on two different occasions of the annual meeting of the Association of the Scientific Study of Consciousness (2018 and 2019). We examined responses from 166 consciousness researchers with different backgrounds (e.g. philosophy, neuroscience, psychology, and computer science) and at various stages of their careers (e.g. junior/senior faculty and graduate/undergraduate students). The results reveal that there remains considerable discussion and debate between the surveyed researchers about the definition of consciousness and the way it should be studied. To highlight a few observations, a majority of respondents believe that machines could have consciousness, that consciousness is a gradual phenomenon in the animal kingdom, and that unconscious processing is extensive, encompassing both low-level and high-level cognitive functions. Further, we show which theories of consciousness are currently considered most promising by respondents and how supposedly different theories cluster together, which dependent measures are considered best to index the presence or absence of consciousness, and which neural measures are thought to be the most likely signatures of consciousness. These findings provide us with a snapshot of the current views of researchers in the field and may therefore help prioritize research and theoretical approaches to foster progress.

Dissociable brain mechanisms underlying the conscious and unconscious control of behavior.

Cognitive control allows humans to overrule and inhibit habitual responses to optimize performance in challenging situations. Contradicting traditional views, recent studies suggest that cognitive control processes can be initiated unconsciously. To further capture the relation between consciousness and cognitive control, we studied the dynamics of inhibitory control processes when triggered consciously versus unconsciously in a modified version of the stop task. Attempts to inhibit an imminent response were often successful after unmasked (visible) stop signals. Masked (invisible) stop signals rarely succeeded in instigating overt inhibition but did trigger slowing down of response times. Masked stop signals elicited a sequence of distinct ERP components that were also observed on unmasked stop signals. The N2 component correlated with the efficiency of inhibitory control when elicited by unmasked stop signals and with the magnitude of slowdown when elicited by masked stop signals. Thus, the N2 likely reflects the initiation of inhibitory control, irrespective of conscious awareness. The P3 component was much reduced in amplitude and duration on masked versus unmasked stop trials. These patterns of differences and similarities between conscious and unconscious cognitive control processes are discussed in a framework that differentiates between feedforward and feedback connections in yielding conscious experience.

Pre-SMA graymatter density predicts individual differences in action selection in the face of conscious and unconscious response conflict.

The presupplementary motor area (pre-SMA) is considered key in contributing to voluntary action selection during response conflict. Here we test whether individual differences in the ability to select appropriate actions in the face of strong (conscious) and weak (virtually unconscious) distracting alternatives are related to individual variability in pre-SMA anatomy. To this end, we scanned 58 participants, who performed a masked priming task in which conflicting response tendencies were elicited either consciously (through primes that were weakly masked) or virtually unconsciously (strongly masked primes), with structural magnetic resonance imaging. Voxel-based morphometry revealed that individual differences in pre-SMA gray-matter density are related to subjects' ability to voluntary select the correct action in the face of conflict, irrespective of the awareness level of conflict-inducing stimuli. These results link structural anatomy to individual differences in cognitive control ability, and provide support for the role of the pre-SMA in the selection of appropriate actions in situations of response conflict. Furthermore, these results suggest that flexible and voluntary behavior requires efficiently dealing with competing response tendencies, even those that are activated automatically and unconsciously.

Criteria for empirical theories of consciousness should focus on the explanatory power of mechanisms, not on functional equivalence.

Doerig and colleagues put forward the notion that we need hard and theory-neutral criteria by which to arbitrate between empirical (mechanistic) theories of consciousness. However, most of the criteria that they propose are not theory neutral because they focus on functional equivalence between systems. Because empirical theories of consciousness are mechanistic rather than functionalist, we think these criteria are not helpful when arbitrating between them.

High-pass filtering artifacts in multivariate classification of neural time series data.

BACKGROUND: Traditionally, EEG/MEG data are high-pass filtered and baseline-corrected to remove slow drifts. Minor deleterious effects of high-pass filtering in traditional time-series analysis have been well-documented, including temporal displacements. However, its effects on time-resolved multivariate pattern classification analyses (MVPA) are largely unknown. NEW METHOD: To prevent potential displacement effects, we extend an alternative method of removing slow drift noise - robust detrending - with a procedure in which we mask out all cortical events from each trial. We refer to this method as trial-masked robust detrending. RESULTS: In both real and simulated EEG data of a working memory experiment, we show that both high-pass filtering and standard robust detrending create artifacts that result in the displacement of multivariate patterns into activity silent periods, particularly apparent in temporal generalization analyses, and especially in combination with baseline correction. We show that trial-masked robust detrending is free from such displacements. COMPARISON WITH EXISTING METHOD(S): Temporal displacement may emerge even with modest filter cut-off settings such as 0.05 Hz, and even in regular robust detrending. However, trial-masked robust detrending results in artifact-free decoding without displacements. Baseline correction may unwittingly obfuscate spurious decoding effects and displace them to the rest of the trial. CONCLUSIONS: Decoding analyses benefit from trial-masked robust detrending, without the unwanted side effects introduced by filtering or regular robust detrending. However, for sufficiently clean data sets and sufficiently strong signals, no filtering or detrending at all may work adequately. Implications for other types of data are discussed, followed by a number of recommendations.