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.

Illusory object recognition is either perceptual or cognitive in origin depending on decision confidence.

We occasionally misinterpret ambiguous sensory input or report a stimulus when none is presented. It is unknown whether such errors have a sensory origin and reflect true perceptual illusions, or whether they have a more cognitive origin (e.g., are due to guessing), or both. When participants performed an error-prone and challenging face/house discrimination task, multivariate electroencephalography (EEG) analyses revealed that during decision errors (e.g., mistaking a face for a house), sensory stages of visual information processing initially represent the presented stimulus category. Crucially however, when participants were confident in their erroneous decision, so when the illusion was strongest, this neural representation flipped later in time and reflected the incorrectly reported percept. This flip in neural pattern was absent for decisions that were made with low confidence. This work demonstrates that decision confidence arbitrates between perceptual decision errors, which reflect true illusions of perception, and cognitive decision errors, which do not.

Feedback information transfer in the human brain reflects bistable perception in the absence of report.

In the search for the neural basis of conscious experience, perception and the cognitive processes associated with reporting perception are typically confounded as neural activity is recorded while participants explicitly report what they experience. Here, we present a novel way to disentangle perception from report using eye movement analysis techniques based on convolutional neural networks and neurodynamical analyses based on information theory. We use a bistable visual stimulus that instantiates two well-known properties of conscious perception: integration and differentiation. At any given moment, observers either perceive the stimulus as one integrated unitary object or as two differentiated objects that are clearly distinct from each other. Using electroencephalography, we show that measures of integration and differentiation based on information theory closely follow participants' perceptual experience of those contents when switches were reported. We observed increased information integration between anterior to posterior electrodes (front to back) prior to a switch to the integrated percept, and higher information differentiation of anterior signals leading up to reporting the differentiated percept. Crucially, information integration was closely linked to perception and even observed in a no-report condition when perceptual transitions were inferred from eye movements alone. In contrast, the link between neural differentiation and perception was observed solely in the active report condition. Our results, therefore, suggest that perception and the processes associated with report require distinct amounts of anterior-posterior network communication and anterior information differentiation. While front-to-back directed information is associated with changes in the content of perception when viewing bistable visual stimuli, regardless of report, frontal information differentiation was absent in the no-report condition and therefore is not directly linked to perception per se.

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.

On the necessity of recurrent processing during object recognition: it depends on the need for scene segmentation.

While feed-forward activity may suffice for recognizing objects in isolation, additional visual operations that aid object recognition might be needed for real-world scenes. One such additional operation is figure-ground segmentation; extracting the relevant features and locations of the target object while ignoring irrelevant features. In this study of 60 human participants (female and male), we show objects on backgrounds of increasing complexity to investigate whether recurrent computations are increasingly important for segmenting objects from more complex backgrounds. Three lines of evidence show that recurrent processing is critical for recognition of objects embedded in complex scenes. First, behavioral results indicated a greater reduction in performance after masking objects presented on more complex backgrounds; with the degree of impairment increasing with increasing background complexity. Second, electroencephalography (EEG) measurements showed clear differences in the evoked response potentials (ERPs) between conditions around time points beyond feed-forward activity and exploratory object decoding analyses based on the EEG signal indicated later decoding onsets for objects embedded in more complex backgrounds. Third, Deep Convolutional Neural Network performance confirmed this interpretation; feed-forward and less deep networks showed a higher degree of impairment in recognition for objects in complex backgrounds compared to recurrent and deeper networks. Together, these results support the notion that recurrent computations drive figure-ground segmentation of objects in complex scenes.SIGNIFICANCE STATEMENTThe incredible speed of object recognition suggests that it relies purely on a fast feed-forward build-up of perceptual activity. However, this view is contradicted by studies showing that disruption of recurrent processing leads to decreased object recognition performance. Here we resolve this issue by showing that how object recognition is resolved, and whether recurrent processing is crucial, depends on the context in which it is presented. For objects presented in isolation or in 'simple' environments, feed-forward activity could be sufficient for successful object recognition. However, when the environment is more complex, additional processing seems necessary to select the elements that belong to the object, and by that segregate them from the background.

Pupil Dilation and the Slow Wave ERP Reflect Surprise about Choice Outcome Resulting from Intrinsic Variability in Decision Confidence.

Central to human and animal cognition is the ability to learn from feedback in order to optimize future rewards. Such a learning signal might be encoded and broadcasted by the brain's arousal systems, including the noradrenergic locus coeruleus. Pupil responses and the positive slow wave component of event-related potentials reflect rapid changes in the arousal level of the brain. Here, we ask whether and how these variables may reflect surprise: the mismatch between one's expectation about being correct and the outcome of a decision, when expectations fluctuate due to internal factors (e.g., engagement). We show that during an elementary decision task in the face of uncertainty both physiological markers of phasic arousal reflect surprise. We further show that pupil responses and slow wave event-related potential are unrelated to each other and that prediction error computations depend on feedback awareness. These results further advance our understanding of the role of central arousal systems in decision-making under uncertainty.

Decreased Alertness Reconfigures Cognitive Control Networks.

Humans' remarkable capacity to flexibly adapt their behavior based on rapid situational changes is termed cognitive control. Intuitively, cognitive control is thought to be affected by the state of alertness; for example, when drowsy, we feel less capable of adequately implementing effortful cognitive tasks. Although scientific investigations have focused on the effects of sleep deprivation and circadian time, little is known about how natural daily fluctuations in alertness in the regular awake state affect cognitive control. Here we combined a conflict task in the auditory domain with EEG neurodynamics to test how neural and behavioral markers of conflict processing are affected by fluctuations in alertness. Using a novel computational method, we segregated alert and drowsy trials from two testing sessions and observed that, although participants (both sexes) were generally sluggish, the typical conflict effect reflected in slower responses to conflicting information compared with nonconflicting information, as well as the moderating effect of previous conflict (conflict adaptation), were still intact. However, the typical neural markers of cognitive control-local midfrontal theta-band power changes-that participants show during full alertness were no longer noticeable when alertness decreased. Instead, when drowsy, we found an increase in long-range information sharing (connectivity) between brain regions in the same frequency band. These results show the resilience of the human cognitive control system when affected by internal fluctuations of alertness and suggest that there are neural compensatory mechanisms at play in response to physiological pressure during diminished alertness.SIGNIFICANCE STATEMENT The normal variability in alertness we experience in daily tasks is rarely taken into account in cognitive neuroscience. Here we studied neurobehavioral dynamics of cognitive control with decreasing alertness. We used the classic Simon task where participants hear the word "left" or "right" in the right or left ear, eliciting slower responses when the word and the side are incongruent-the conflict effect. Participants performed the task both while fully awake and while getting drowsy, allowing for the characterization of alertness modulating cognitive control. The changes in the neural signatures of conflict from local theta oscillations to a long-distance distributed theta network suggest a reconfiguration of the underlying neural processes subserving cognitive control when affected by alertness fluctuations.

Representational dynamics preceding conscious access.

Our senses are continuously bombarded with more information than our brain can process up to the level of awareness. The present study aimed to enhance understanding on how attentional selection shapes conscious access under conditions of rapidly changing input. Using an attention task, EEG, and multivariate decoding of individual target- and distractor-defining features, we specifically examined dynamic changes in the representation of targets and distractors as a function of conscious access and the task-relevance (target or distractor) of the preceding item in the RSVP stream. At the behavioral level, replicating previous work and suggestive of a flexible gating mechanism, we found a significant impairment in conscious access to targets (T2) that were preceded by a target (T1) followed by one or two distractors (i.e., the attentional blink), but striking facilitation of conscious access to targets shown directly after another target (i.e., lag-1 sparing and blink reversal). At the neural level, conscious access to T2 was associated with enhanced early- and late-stage T1 representations and enhanced late-stage D1 representations, and interestingly, could be predicted based on the pattern of EEG activation well before T1 was presented. Yet, across task conditions, we did not find convincing evidence for the notion that conscious access is affected by rapid top-down selection-related modulations of the strength of early sensory representations induced by the preceding visual event. These results cannot easily be explained by existing accounts of how attentional selection shapes conscious access under rapidly changing input conditions, and have important implications for theories of the attentional blink and consciousness more generally.

Subjective visibility report is facilitated by conscious predictions only.

Predictions in the visual domain have been shown to modulate conscious access. Yet, little is known about how predictions may do so and to what extent they need to be consciously implemented to be effective. To address this, we administered an attentional blink (AB) task in which target 1 (T1) identity predicted target 2 (T2) identity, while participants rated their perceptual awareness of validly versus invalidly predicted T2s (Experiment 1 & 2) or reported T2 identity (Experiment 3). Critically, we tested the effects of conscious and non-conscious predictions, after seen and unseen T1s, on T2 visibility. We found that valid predictions increased subjective visibility reports and discrimination of T2s, but only when predictions were generated by a consciously accessed T1, irrespective of the timing at which the effects were measured (short vs. longs lags). These results further our understanding of the intricate relationship between predictive processing and consciousness.

Methylphenidate does not affect convergent and divergent creative processes in healthy adults.

An increasing number of healthy people use methylphenidate, a psychostimulant that increases dopamine and noradrenaline transmission in the brain, to help them focus over extended periods of time. While methylphenidate has been shown to facilitate some cognitive functions, like focus and distractor-resistance, the same drug might also contribute to cognitive impairment, for example, in creativity. In this study, we investigated whether acute administration of a low oral dose (20 mg) of methylphenidate affected convergent and divergent creative processes in a sample of young healthy participants. Also, we explored whether such effects depended on individual differences in ADHD symptoms and working memory capacity. Contrary to our expectations, methylphenidate did not affect participants' creative performance on any of the tasks. Also, methylphenidate effects did not depend on individual differences in trait hyperactivity-impulsivity or baseline working memory capacity. Thus, although the effects of methylphenidate on creativity might be underestimated in our study due to several methodological factors, our findings do not suggest that methylphenidate impairs people's ability to be creative.

No Evidence that Predictions and Attention Modulate the First Feedforward Sweep of Cortical Information Processing.

Predictive coding models propose that predictions (stimulus likelihood) reduce sensory signals as early as primary visual cortex (V1), and that attention (stimulus relevance) can modulate these effects. Indeed, both prediction and attention have been shown to modulate V1 activity, albeit with fMRI, which has low temporal resolution. This leaves it unclear whether these effects reflect a modulation of the first feedforward sweep of visual information processing and/or later, feedback-related activity. In two experiments, we used electroencephalography and orthogonally manipulated spatial predictions and attention to address this issue. Although clear top-down biases were found, as reflected in pre-stimulus alpha-band activity, we found no evidence for top-down effects on the earliest visual cortical processing stage (<80 ms post-stimulus), as indexed by the amplitude of the C1 event-related potential component and multivariate pattern analyses. These findings indicate that initial visual afferent activity may be impenetrable to top-down influences by spatial prediction and attention.

Dynamic Interactions between Top-Down Expectations and Conscious Awareness.

It is well known that top-down expectations affect perceptual processes. Yet, remarkably little is known about the relationship between expectations and conscious awareness. We address three crucial outstanding questions: (1) how do expectations affect the likelihood of conscious stimulus perception?; (2) does the brain register violations of expectations nonconsciously?; and (3) do expectations need to be conscious to influence perceptual decisions? Using human participants, we performed three experiments in which we manipulated stimulus predictability within the attentional blink paradigm, while combining visual psychophysics with electrophysiological recordings. We found that valid stimulus expectations increase the likelihood of conscious access of stimuli. Furthermore, our findings suggest a clear dissociation in the interaction between expectations and consciousness: conscious awareness seems crucial for the implementation of top-down expectations, but not for the generation of bottom-up stimulus-evoked prediction errors. These results constrain and update influential theories about the role of consciousness in the predictive brain.SIGNIFICANCE STATEMENT While the relationship between expectations and conscious awareness plays a major role in many prediction-based theories of brain functioning, thus far few empirical studies have examined this relationship. Here, we address this gap in knowledge in a set of three experiments. Our results suggest that the effect of expectations on conscious awareness varies between different steps of the hierarchy of predictive processing. While the active use of top-down expectations for perceptual decisions requires conscious awareness, prediction errors can be triggered outside of conscious awareness. These results constrain and update influential theories about the role of consciousness in the predictive brain.

How the Level of Reward Awareness Changes the Computational and Electrophysiological Signatures of Reinforcement Learning.

The extent to which subjective awareness influences reward processing, and thereby affects future decisions, is currently largely unknown. In the present report, we investigated this question in a reinforcement learning framework, combining perceptual masking, computational modeling, and electroencephalographic recordings (human male and female participants). Our results indicate that degrading the visibility of the reward decreased, without completely obliterating, the ability of participants to learn from outcomes, but concurrently increased their tendency to repeat previous choices. We dissociated electrophysiological signatures evoked by the reward-based learning processes from those elicited by the reward-independent repetition of previous choices and showed that these neural activities were significantly modulated by reward visibility. Overall, this report sheds new light on the neural computations underlying reward-based learning and decision-making and highlights that awareness is beneficial for the trial-by-trial adjustment of decision-making strategies.SIGNIFICANCE STATEMENT The notion of reward is strongly associated with subjective evaluation, related to conscious processes such as "pleasure," "liking," and "wanting." Here we show that degrading reward visibility in a reinforcement learning task decreases, without completely obliterating, the ability of participants to learn from outcomes, but concurrently increases subjects' tendency to repeat previous choices. Electrophysiological recordings, in combination with computational modeling, show that neural activities were significantly modulated by reward visibility. Overall, we dissociate different neural computations underlying reward-based learning and decision-making, which highlights a beneficial role of reward awareness in adjusting decision-making strategies.

No language unification without neural feedback: How awareness affects sentence processing.

How does the human brain combine a finite number of words to form an infinite variety of sentences? According to the Memory, Unification and Control (MUC) model, sentence processing requires long-range feedback from the left inferior frontal cortex (LIFC) to left posterior temporal cortex (LPTC). Single word processing however may only require feedforward propagation of semantic information from sensory regions to LPTC. Here we tested the claim that long-range feedback is required for sentence processing by reducing visual awareness of words using a masking technique. Masking disrupts feedback processing while leaving feedforward processing relatively intact. Previous studies have shown that masked single words still elicit an N400 ERP effect, a neural signature of semantic incongruency. However, whether multiple words can be combined to form a sentence under reduced levels of awareness is controversial. To investigate this issue, we performed two experiments in which we measured electroencephalography (EEG) while 40 subjects performed a masked priming task. Words were presented either successively or simultaneously, thereby forming a short sentence that could be congruent or incongruent with a target picture. This sentence condition was compared with a typical single word condition. In the masked condition we only found an N400 effect for single words, whereas in the unmasked condition we observed an N400 effect for both unmasked sentences and single words. Our findings suggest that long-range feedback processing is required for sentence processing, but not for single word processing.

The relationship between conflict awareness and behavioral and oscillatory signatures of immediate and delayed cognitive control.

Cognitive control over conflict, mediated by the prefrontal cortex, is an important skill for successful decision-making. Although it has been shown that cognitive control may operate unconsciously, it has recently been proposed that control operations may be driven by the metacognitive awareness of conflict, e.g. arising from the feeling of task difficulty or the ease of action selection, and therefore crucially depends on conflict awareness. Behavioral and electroencephalography (EEG) data are presented from 64 subjects performing a masked priming paradigm to test this hypothesis. Although the subjective experience of conflict elicited behavioral adaptation, this was also the case when conflict was present, but not experienced. In EEG, typical oscillatory markers of conflict processing in the theta-, alpha- and beta-band were observed (relative broadband), but these were differentially modulated by conflict experience. This demonstrates that conflict adaptation does not depend on conflict experience, but that conflict experience is associated with increased cognitive control.

Event-Related Potential, Time-frequency, and Functional Connectivity Facets of Local and Global Auditory Novelty Processing: An Intracranial Study in Humans.

Auditory novelty detection has been associated with different cognitive processes. Bekinschtein et al. (2009) developed an experimental paradigm to dissociate these processes, using local and global novelty, which were associated, respectively, with automatic versus strategic perceptual processing. They have mostly been studied using event-related potentials (ERPs), but local spiking activity as indexed by gamma (60-120 Hz) power and interactions between brain regions as indexed by modulations in beta-band (13-25 Hz) power and functional connectivity have not been explored. We thus recorded 9 epileptic patients with intracranial electrodes to compare the precise dynamics of the responses to local and global novelty. Local novelty triggered an early response observed as an intracranial mismatch negativity (MMN) contemporary with a strong power increase in the gamma band and an increase in connectivity in the beta band. Importantly, all these responses were strictly confined to the temporal auditory cortex. In contrast, global novelty gave rise to a late ERP response distributed across brain areas, contemporary with a sustained power decrease in the beta band (13-25 Hz) and an increase in connectivity in the alpha band (8-13 Hz) within the frontal lobe. We discuss these multi-facet signatures in terms of conscious access to perceptual information.

Conflict awareness dissociates theta-band neural dynamics of the medial frontal and lateral frontal cortex during trial-by-trial cognitive control.

Recent findings have refuted the common assumption that executive control functions of the prefrontal cortex exclusively operate consciously, suggesting that many, if not all, cognitive processes could potentially operate unconsciously. However, although many cognitive functions can be launched unconsciously, several theoretical models of consciousness assume that there are crucial qualitative differences between conscious and unconscious processes. We hypothesized that the potential benefit of awareness in cognitive control mechanisms might become apparent when high control has to be maintained across time and requires the interaction between a set of distant frontal brain regions. To test this, we extracted oscillatory power dynamics from electroencephalographic data recorded while participants performed a task in which conflict awareness was manipulated by masking the conflict-inducing stimulus. We observed that instantaneous conflict as well as across trial conflict adaptation mechanisms were associated with medial frontal theta-band power modulations, irrespective of conflict awareness. However, and crucially, across-trial conflict adaptation processes reflected in increased theta-band power over dorsolateral frontal cortex were observed after fully conscious conflict only. This suggests that initial conflict detection and subsequent control adaptation by the medial frontal cortex are automatic and unconscious, whereas the routing of information from the medial frontal cortex to the lateral prefrontal cortex is a unique feature of conscious cognitive control.

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.