Intracranial neural representation of phenomenal and access consciousness in the human brain.

After more than 30 years of extensive investigation, impressive progress has been made in identifying the neural correlates of consciousness (NCC). However, the functional role of spatiotemporally distinct consciousness-related neural activity in conscious perception is debated. An influential framework proposed that consciousness-related neural activities could be dissociated into two distinct processes: phenomenal and access consciousness. However, though hotly debated, its authenticity has not been examined in a single paradigm with more informative intracranial recordings. In the present study, we employed a visual awareness task and recorded the local field potential (LFP) of patients with electrodes implanted in cortical and subcortical regions. Overall, we found that the latency of visual awareness-related activity exhibited a bimodal distribution, and the recording sites with short and long latencies were largely separated in location, except in the lateral prefrontal cortex (lPFC). The mixture of short and long latencies in the lPFC indicates that it plays a critical role in linking phenomenal and access consciousness. However, the division between the two is not as simple as the central sulcus, as proposed previously. Moreover, in 4 patients with electrodes implanted in the bilateral prefrontal cortex, early awareness-related activity was confined to the contralateral side, while late awareness-related activity appeared on both sides. Finally, Granger causality analysis showed that awareness-related information flowed from the early sites to the late sites. These results provide the first LFP evidence of neural correlates of phenomenal and access consciousness, which sheds light on the spatiotemporal dynamics of NCC in the human brain.

Task-based EEG and fMRI paradigms in a multimodal clinical diagnostic framework for disorders of consciousness.

Disorders of consciousness (DoC) are generally diagnosed by clinical assessment, which is a predominantly motor-driven process and accounts for up to 40 % of non-communication being misdiagnosed as unresponsive wakefulness syndrome (UWS) (previously known as prolonged/persistent vegetative state). Given the consequences of misdiagnosis, a more reliable and objective multimodal protocol to diagnosing DoC is needed, but has not been produced due to concerns regarding their interpretation and reliability. Of the techniques commonly used to detect consciousness in DoC, task-based paradigms (active paradigms) produce the most unequivocal result when findings are positive. It is well-established that command following (CF) reliably reflects preserved consciousness. Task-based electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) can detect motor-independent CF and reveal preserved covert consciousness in up to 14 % of UWS patients. Accordingly, to improve the diagnostic accuracy of DoC, we propose a practical multimodal clinical decision framework centered on task-based EEG and fMRI, and complemented by measures like transcranial magnetic stimulation (TMS-EEG).

Late Positivity Correlates with Subjective Reports: Evidence from the Low-frequency and High-frequency Reporting Tasks.

Identifying the neural correlates of consciousness (NCCs) is an important way to understand the fundamental nature of consciousness. By recording event-related potentials (ERPs) using EEG, researchers have found three potential electrophysiological NCCs: early positive correlate of consciousness (enhanced P1), visual awareness negativity (VAN), and late positivity (LP). However, LP may reflect post-perceptual processing associated with subjective reports rather than consciousness per se. The present experiment investigated the relationship between LP and subjective reports. We adopted two subjective reporting tasks that differed in the requirement for subjective reports. In the low-frequency reporting task, participants needed to report whether they saw the target picture in 25% of trials, whereas in the high-frequency reporting task, participants needed to report whether they saw the target picture in each trial. Behavioral results showed that the hit rates were lower and false alarm rates were higher on reporting trials in low-frequency reporting tasks than on reporting trials in high-frequency reporting tasks. Unexpectedly, VAN was larger on reporting trials in the low-frequency reporting task than on reporting trials in the high-frequency reporting task. Importantly, our ERP results showed that LP was larger on reporting trials in the high-frequency reporting task than on reporting trials in the low-frequency reporting task. Thus, our findings indicated that when the frequency of reports was increased, the task relevance of the stimuli increased, which led to larger LP amplitudes. These findings suggest that LP correlates with subjective reports.

A mechanistic alternative to minimal sufficiency as the guiding principle for NCC research.

A central project for the neuroscience of consciousness is to reveal the neural basis of consciousness. For the past 20-odd years, this project has been conceptualized in terms of minimal sufficiency. Recently, a number of authors have suggested that the project is better conceived in mechanistic terms as the search for difference-makers. In this paper, I (i) motivate this mechanistic alternative to minimal sufficiency, (ii) develop it further by clarifying debates about the prospects of leveraging mutual manipulability to distinguish constitutive difference-makers from those that are merely causal, and (iii) explore the implications this has for recent debates concerning the status of the prefrontal cortex. I argue that adopting a mechanistic approach to the neuroscience of consciousness suggests that the prefrontal cortex is part of the neural mechanisms underlying consciousness even if it is not strictly speaking a necessary part.

Conscious perception of fear in faces: Insights from high-density EEG and perceptual awareness scale with threshold stimuli.

Contrary to the extensive research on processing subliminal and/or unattended emotional facial expressions, only a minority of studies have investigated the neural correlates of consciousness (NCCs) of emotions conveyed by faces. In the present high-density electroencephalography (EEG) study, we first employed a staircase procedure to identify each participant's perceptual threshold of the emotion expressed by the face and then compared the EEG signals elicited in trials where the participants were aware with the activity elicited in trials where participants were unaware of the emotions expressed by these, otherwise identical, faces. Drawing on existing knowledge of the neural mechanisms of face processing and NCCs, we hypothesized that activity in frontal electrodes would be modulated in relation to participants' awareness of facial emotional content. More specifically, we hypothesized that the NCC of fear seen on someone else's face could be detected as a modulation of a later and more anterior (i.e., at frontal sites) event-related potential (ERP) than the face-sensitive N170. By adopting a data-driven approach and cluster-based statistics to the analysis of EEG signals, the results were clear-cut in showing that visual awareness of fear was associated with the modulation of a frontal ERP component in a 150-300 msec interval. These insights are dissected and contextualized in relation to prevailing theories of visual consciousness and their proposed NCC benchmarks.

Beyond task response-Pre-stimulus activity modulates contents of consciousness.

The current discussion on the neural correlates of the contents of consciousness (NCCc) focuses mainly on the post-stimulus period of task-related activity. This neglects the substantial impact of the spontaneous or ongoing activity of the brain as manifest in pre-stimulus activity. Does the interaction of pre- and post-stimulus activity shape the contents of consciousness? Addressing this gap in our knowledge, we review and converge two recent lines of findings, that is, pre-stimulus alpha power and pre- and post-stimulus alpha trial-to-trial variability (TTV). The data show that pre-stimulus alpha power modulates post-stimulus activity including specifically the subjective features of conscious contents like confidence and vividness. At the same time, alpha pre-stimulus variability shapes post-stimulus TTV reduction including the associated contents of consciousness. We propose that non-additive rather than merely additive interaction of the internal pre-stimulus activity with the external stimulus in the alpha band is key for contents to become conscious. This is mediated by mechanisms on different levels including neurophysiological, neurocomputational, neurodynamic, neuropsychological and neurophenomenal levels. Overall, considering the interplay of pre-stimulus intrinsic and post-stimulus extrinsic activity across wider timescales, not just evoked responses in the post-stimulus period, is critical for identifying neural correlates of consciousness. This is well in line with both processing and especially the Temporo-spatial theory of consciousness (TTC).

A Mechanistic Model of Perceptual Binding Predicts That Binding Mechanism Is Robust against Noise.

The concept of the brain's own time and space is central to many models and theories that aim to explain how the brain generates consciousness. For example, the temporo-spatial theory of consciousness postulates that the brain implements its own inner time and space for conscious processing of the outside world. Furthermore, our perception and cognition of time and space can be different from actual time and space. This study presents a mechanistic model of mutually connected processes that encode phenomenal representations of space and time. The model is used to elaborate the binding mechanism between two sets of processes representing internal space and time, respectively. Further, a stochastic version of the model is developed to investigate the interplay between binding strength and noise. Spectral entropy is used to characterize noise effects on the systems of interacting processes when the binding strength between them is varied. The stochastic modeling results reveal that the spectral entropy values for strongly bound systems are similar to those for weakly bound or even decoupled systems. Thus, the analysis performed in this study allows us to conclude that the binding mechanism is noise-resilient.

The exclusionary approach to consciousness.

The standard approach in the field of consciousness research involves identifying the neural correlates of consciousness (NCCs) by comparing neural activity between conscious and unconscious trials. However, this method has been met with criticism due to the lack of consensus on how to operationalize and measure consciousness. In this paper, I propose an alternative approach: the exclusionary approach. Rather than utilizing near-threshold conditions to contrast conscious and unconscious trials, this approach leverages the widely accepted notion that subjective reports are reliable under normal conditions. I propose that this can be done by assessing whether consciousness remains stable across trials while manipulating other factors such as reports, tasks, stimulation, or attention. We can use the resulting contrast to exclude certain kinds of neural activity as candidate NCCs. This method produces results that are less contentious, allowing for the establishment of hard criteria for theories of consciousness. Additionally, this approach does not require the development of new research paradigms, but can incorporate existing studies, particularly those aimed at identifying confounding factors in the standard approach. It is important to note, however, that the proposed exclusionary approach does not negate the value of the identification approach. Rather, they should be considered as complementary methods.

What Is It like to Be a Brain Organoid? Phenomenal Consciousness in a Biological Neural Network.

It has been shown that three-dimensional self-assembled multicellular structures derived from human pluripotent stem cells show electrical activity similar to EEG. More recently, neurons were successfully embedded in digital game worlds. The biologically inspired neural network (BNN), expressing human cortical cells, was able to show internal modification and learn the task at hand (predicting the trajectory of a digital ball while moving a digital paddle). In other words, the system allowed to read motor information and write sensory data into cell cultures. In this article, we discuss Neural Correlates of Consciousness (NCC) theories, and their capacity to predict or even allow for consciousness in a BNN. We found that Information Integration Theory (IIT) is the only NCC that offers the possibility for a BNN to show consciousness, since the Φ value in the BNN is >0. In other words, the recording of real-time neural activity responding to environmental stimuli. IIT argues that any system capable of integrating information will have some degree of phenomenal consciousness. We argue that the pattern of activity appearing in the BNN, with increased density of sensory information leading to better performance, implies that the BNN could be conscious. This may have profound implications from a psychological, philosophical, and ethical perspective.

Distinct ventral stream and prefrontal cortex representational dynamics during sustained conscious visual perception.

Instances of sustained stationary sensory input are ubiquitous. However, previous work focused almost exclusively on transient onset responses. This presents a critical challenge for neural theories of consciousness, which should account for the full temporal extent of experience. To address this question, we use intracranial recordings from ten human patients with epilepsy to view diverse images of multiple durations. We reveal that, in sensory regions, despite dramatic changes in activation magnitude, the distributed representation of categories and exemplars remains sustained and stable. In contrast, in frontoparietal regions, we find transient content representation at stimulus onset. Our results highlight the connection between the anatomical and temporal correlates of experience. To the extent perception is sustained, it may rely on sensory representations and to the extent perception is discrete, centered on perceptual updating, it may rely on frontoparietal representations.

Piecing together the puzzle of emotional consciousness.

The search for neural correlates of emotional consciousness has gained momentum in the last decades. Nonetheless, disagreements concerning the mechanisms that determine the experiential qualities of emotional consciousness-the "what is it like" to feel an emotion-as well as on their neural correlates have far-reaching consequences on how researchers study and measure emotion, sometimes leading to seemingly irresolvable impasses. The current paper lays out in a balanced way the viewpoint of both cognitive and precognitive approaches to emotional consciousness on the basis of commonalities and differences between the claims of some relevant theories of emotions. We examine the sufficiency of the existing evidence in support of the proposed theories of emotional consciousness by going through the methodological specificity of the study of emotional consciousness and its unique challenges and highlighting what can and cannot be imported by advances in research on perceptual consciousness. We propose that there are three key experimental contrasts that are each equally necessary in the search for the neural correlates of emotional consciousness and each contrast alone coming with its own limitations. We conclude by acknowledging some of the most promising avenues in the field, which may help go beyond the current limitations and collaboratively piece together the puzzle of emotional consciousness.

Towards causal mechanisms of consciousness through focused transcranial brain stimulation.

Conscious experience represents one of the most elusive problems of empirical science, namely neuroscience. The main objective of empirical studies of consciousness has been to describe the minimal sets of neural events necessary for a specific neuronal state to become consciously experienced. The current state of the art still does not meet this objective but rather consists of highly speculative theories based on correlates of consciousness and an ever-growing list of knowledge gaps. The current state of the art is defined by the limitations of past stimulation techniques and the emphasis on the observational approach. However, looking at the current stimulation technologies that are becoming more accurate, it is time to consider an alternative approach to studying consciousness, which builds on the methodology of causal explanations via causal alterations. The aim of this methodology is to move beyond the correlates of consciousness and focus directly on the mechanisms of consciousness with the help of the currently focused brain stimulation techniques, such as geodesic transcranial electric neuromodulation. This approach not only overcomes the limitations of the correlational methodology but will also become another firm step in the following science of consciousness.

Erratum: Frontal and parietal lobes play crucial roles in understanding the disorder of consciousness: A perspective from electroencephalogram studies.

[This corrects the article DOI: 10.3389/fnins.2022.1024278.].

Highly connected and highly variable: A Core brain network during resting state supports Propofol-induced unconsciousness.

Despite that leading theories of consciousness make diverging predictions for where and how neural activity gives rise to subjective experience, they all seem to partially agree that the neural correlates of consciousness (NCC) require globally integrated brain activity across a network of functionally specialized modules. However, it is not clear yet whether such functional configurations would be able to identify the NCC. We scanned resting-state fMRI data from 21 subjects during wakefulness, propofol-induced sedation, and anesthesia. Graph-theoretical analyses were conducted on awake fMRI data to search for the NCC candidates as brain regions that exhibit both high rich-clubness and high modular variability, which were found to locate in prefrontal and temporoparietal cortices. Another independent data set of 10 highly-sampled subjects was used to validate the NCC distribution at the individual level. Brain module-based dynamic analysis revealed two discrete reoccurring brain states, one of which was dominated by the NCC candidates (state 1), while the other state was predominately composed of primary sensory/motor regions (state 2). Moreover, state 1 appeared to be temporally more stable than state 2, suggesting that the identified NCC members could sustain conscious content as metastable network representations. Finally, we showed that the identified NCC was modulated in terms of functional connectedness and modular variability in response to the loss of consciousness induced by propofol anesthesia. This work offers a framework to search for neural correlates of consciousness by charting the brain network topology and provides new insights into understanding the roles of different regions in underpinning human consciousness.

How much consciousness is there in complexity?

The notion of complexity currently receives significant attention in neuroscience, mainly through the popularity of the Integrated Information Theory (IIT). It has proven successful in research centred on discriminating states of consciousness, while little theoretical and experimental effort was directed toward studying the content. In this paper, we argue that exploring the relationship between complexity and conscious content is necessary to understand the importance of information-theoretic measures for consciousness research properly. We outline how content could be experimentally operationalised and how rudimental testable hypotheses can be formulated without requiring IIT formalisms. This approach would not only allow for a better understanding of aspects of consciousness captured by complexity but could also facilitate comparison efforts for theories of consciousness.

Awareness and consciousness in humans and animals - neural and behavioral correlates in an evolutionary perspective.

Awareness or consciousness in the context of stimulus perception can directly be assessed in well controlled test situations with humans via the persons' reports about their subjective experiences with the stimuli. Since we have no direct access to subjective experiences in animals, their possible awareness or consciousness in stimulus perception tasks has often been inferred from behavior and cognitive abilities previously observed in aware and conscious humans. Here, we analyze published human data primarily on event-related potentials and brain-wave generation during perception and responding to sensory stimuli and extract neural markers (mainly latencies of evoked-potential peaks and of gamma-wave occurrence) indicating that a person became aware or conscious of the perceived stimulus. These neural correlates of consciousness were then applied to sets of corresponding data from various animals including several species of mammals, and one species each of birds, fish, cephalopods, and insects. We found that the neural markers from studies in humans could also successfully be applied to the mammal and bird data suggesting that species in these animal groups can become subjectively aware of and conscious about perceived stimuli. Fish, cephalopod and insect data remained inconclusive. In an evolutionary perspective we have to consider that both awareness of and consciousness about perceived stimuli appear as evolved, attention-dependent options added to the ongoing neural activities of stimulus processing and action generation. Since gamma-wave generation for functional coupling of brain areas in aware/conscious states is energetically highly cost-intensive, it remains to be shown which animal species under which conditions of lifestyle and ecological niche may achieve significant advantages in reproductive fitness by drawing upon these options. Hence, we started our discussion about awareness and consciousness in animals with the question in how far these expressions of brain activity are necessary attributes for perceiving stimuli and responding in an adaptive way.

A voice without a mouth no more: The neurobiology of language and consciousness.

Most research on the neurobiology of language ignores consciousness and vice versa. Here, language, with an emphasis on inner speech, is hypothesised to generate and sustain self-awareness, i.e., higher-order consciousness. Converging evidence supporting this hypothesis is reviewed. To account for these findings, a 'HOLISTIC' model of neurobiology of language, inner speech, and consciousness is proposed. It involves a 'core' set of inner speech production regions that initiate the experience of feeling and hearing words. These take on affective qualities, deriving from activation of associated sensory, motor, and emotional representations, involving a largely unconscious dynamic 'periphery', distributed throughout the whole brain. Responding to those words forms the basis for sustained network activity, involving 'default mode' activation and prefrontal and thalamic/brainstem selection of contextually relevant responses. Evidence for the model is reviewed, supporting neuroimaging meta-analyses conducted, and comparisons with other theories of consciousness made. The HOLISTIC model constitutes a more parsimonious and complete account of the 'neural correlates of consciousness' that has implications for a mechanistic account of mental health and wellbeing.

Consciousness as the Temporal Propagation of Information.

Our ability to understand the mind and its relation to the body is highly dependent on the way we define consciousness and the lens through which we study it. We argue that looking at conscious experience from an information-theory perspective can help obtain a unified and parsimonious account of the mind. Today's dominant models consider consciousness to be a specialized function of the brain characterized by a discrete neural event. Against this background, we consider subjective experience through information theory, presenting consciousness as the propagation of information from the past to the future. We examine through this perspective major characteristics of consciousness. We demonstrate that without any additional assumptions, temporal continuity in perception can explain the emergence of volition, subjectivity, higher order thoughts, and body boundaries. Finally, we discuss the broader implications for the mind-body question and the appeal of embodied cognition.

A leaky evidence accumulation process for perceptual experience.

The neural correlates supporting our perceptual experience of the world remain largely unknown. Recent studies have shown how stimulus detection and related confidence involve evidence accumulation (EA) processes similar to those involved in perceptual decision-making. Here, we propose that independently from any tasks, percepts are not static but fade in and out of consciousness according to the dynamics of a leaky evidence accumulation process (LEAP), and that confidence corresponds to the maximal evidence accumulated by this process. We discuss the implications and limitations of our proposal, assess how it may qualify as a neural correlate of consciousness, and illustrate how it brings us closer to a mechanistic understanding of phenomenal aspects of perceptual experience like intensity and duration, beyond mere detection.