Neural signs and mechanisms of consciousness: Is there a potential convergence of theories of consciousness in sight?

Various theories for the neural basis of consciousness have been proposed, suggesting a diversity of neural signs and mechanisms. We ask to what extent this diversity is real, or whether many theories share the same basic ideas with a potential for convergence towards a more unified theory of the neural basis of consciousness. For that purpose, we review and compare the various neural signs, measures, and mechanisms proposed in the different theories. We demonstrate that different theories focus on neural signs and measures of distinct aspects of neural activity including stimulus-related, prestimulus, and resting state activity as well as on distinct features of consciousness. Therefore, the various mechanisms proposed in the different theories may, in part, complement each other. Together, we provide insight into the shared basis and convergences (and, in part, discrepancies) of the different theories of consciousness. We conclude that the different theories concern distinct aspects of both neural activity and consciousness which, as we suppose, may be integrated and nested within the brain's overall temporo-spatial dynamics.

Split-Brain: What We Know Now and Why This is Important for Understanding Consciousness.

Recently, the discussion regarding the consequences of cutting the corpus callosum ("split-brain") has regained momentum (Corballis, Corballis, Berlucchi, & Marzi, Brain, 141(6), e46, 2018; Pinto et al., Brain, 140(5), 1231-1237, 2017a; Pinto, Lamme, & de Haan, Brain, 140(11), e68, 2017; Volz & Gazzaniga, Brain, 140(7), 2051-2060, 2017; Volz, Hillyard, Miller, & Gazzaniga, Brain, 141(3), e15, 2018). This collective review paper aims to summarize the empirical common ground, to delineate the different interpretations, and to identify the remaining questions. In short, callosotomy leads to a broad breakdown of functional integration ranging from perception to attention. However, the breakdown is not absolute as several processes, such as action control, seem to remain unified. Disagreement exists about the responsible mechanisms for this remaining unity. The main issue concerns the first-person perspective of a split-brain patient. Does a split-brain harbor a split consciousness or is consciousness unified? The current consensus is that the body of evidence is insufficient to answer this question, and different suggestions are made with respect to how future studies might address this paucity. In addition, it is suggested that the answers might not be a simple yes or no but that intermediate conceptualizations need to be considered.

Visual Functions Generating Conscious Seeing.

Visual functions are reviewed that coincide with conscious as opposed to unconscious vision. Four stages of vision are identified, going from the fully invisible, to subjectively invisible, unattended, and clearly visible. It is proposed that feature extraction, categorization, and some aspects of visual inference occur during full and subjective invisibility. Functions related to perceptual organization, such as grouping and figure-ground segregation, occur during inattention as well as full visibility. It is argued that perceptual organization is the function that is central to understanding the transition from unconscious to conscious seeing. It is discussed what this implies for theories of consciousness such as Recurrent Processing Theory, Higher Order Thought Theory, Integrated Information Theory, and Global Neuronal Workspace Theory.

Challenges for theories of consciousness: seeing or knowing, the missing ingredient and how to deal with panpsychism.

Significant progress has been made in the study of consciousness. Promising theories have been developed and a wealth of experimental data has been generated, both guiding us towards a better understanding of this complex phenomenon. However, new challenges have surfaced. Is visual consciousness about the seeing or the knowing that you see? Controversy about whether the conscious experience is better explained by theories that focus on phenomenal (P-consciousness) or cognitive aspects (A-consciousness) remains, and the debate seems to reach a stalemate. Can we ever resolve this? A further challenge is that many theories of consciousness seem to endorse high degrees of panpsychism-the notion that all beings or even lifeless objects have conscious experience. Should we accept this, or does it imply that these theories require further ingredients that would put a lower bound on beings or devices that have conscious experience? If so, what could these 'missing ingredients' be? These challenges are discussed, and potential solutions are offered.This article is part of the theme issue 'Perceptual consciousness and cognitive access'.

Scene complexity modulates degree of feedback activity during object detection in natural scenes.

Selective brain responses to objects arise within a few hundreds of milliseconds of neural processing, suggesting that visual object recognition is mediated by rapid feed-forward activations. Yet disruption of neural responses in early visual cortex beyond feed-forward processing stages affects object recognition performance. Here, we unite these discrepant findings by reporting that object recognition involves enhanced feedback activity (recurrent processing within early visual cortex) when target objects are embedded in natural scenes that are characterized by high complexity. Human participants performed an animal target detection task on natural scenes with low, medium or high complexity as determined by a computational model of low-level contrast statistics. Three converging lines of evidence indicate that feedback was selectively enhanced for high complexity scenes. First, functional magnetic resonance imaging (fMRI) activity in early visual cortex (V1) was enhanced for target objects in scenes with high, but not low or medium complexity. Second, event-related potentials (ERPs) evoked by target objects were selectively enhanced at feedback stages of visual processing (from ~220 ms onwards) for high complexity scenes only. Third, behavioral performance for high complexity scenes deteriorated when participants were pressed for time and thus less able to incorporate the feedback activity. Modeling of the reaction time distributions using drift diffusion revealed that object information accumulated more slowly for high complexity scenes, with evidence accumulation being coupled to trial-to-trial variation in the EEG feedback response. Together, these results suggest that while feed-forward activity may suffice to recognize isolated objects, the brain employs recurrent processing more adaptively in naturalistic settings, using minimal feedback for simple scenes and increasing feedback for complex scenes.

The Split-Brain Phenomenon Revisited: A Single Conscious Agent with Split Perception.

The split-brain phenomenon is caused by the surgical severing of the corpus callosum, the main route of communication between the cerebral hemispheres. The classical view of this syndrome asserts that conscious unity is abolished. The left hemisphere consciously experiences and functions independently of the right hemisphere. This view is a cornerstone of current consciousness research. In this review, we first discuss the evidence for the classical view. We then propose an alternative, the 'conscious unity, split perception' model. This model asserts that a split brain produces one conscious agent who experiences two parallel, unintegrated streams of information. In addition to changing our view of the split-brain phenomenon, this new model also poses a serious challenge for current dominant theories of consciousness.

Split brain: divided perception but undivided consciousness.

In extensive studies with two split-brain patients we replicate the standard finding that stimuli cannot be compared across visual half-fields, indicating that each hemisphere processes information independently of the other. Yet, crucially, we show that the canonical textbook findings that a split-brain patient can only respond to stimuli in the left visual half-field with the left hand, and to stimuli in the right visual half-field with the right hand and verbally, are not universally true. Across a wide variety of tasks, split-brain patients with a complete and radiologically confirmed transection of the corpus callosum showed full awareness of presence, and well above chance-level recognition of location, orientation and identity of stimuli throughout the entire visual field, irrespective of response type (left hand, right hand, or verbally). Crucially, we used confidence ratings to assess conscious awareness. This revealed that also on high confidence trials, indicative of conscious perception, response type did not affect performance. These findings suggest that severing the cortical connections between hemispheres splits visual perception, but does not create two independent conscious perceivers within one brain.

Conscious visual memory with minimal attention.

Is conscious visual perception limited to the locations that a person attends? The remarkable phenomenon of change blindness, which shows that people miss nearly all unattended changes in a visual scene, suggests the answer is yes. However, change blindness is found after visual interference (a mask or a new scene), so that subjects have to rely on working memory (WM), which has limited capacity, to detect the change. Before such interference, however, a much larger capacity store, called fragile memory (FM), which is easily overwritten by newly presented visual information, is present. Whether these different stores depend equally on spatial attention is central to the debate on the role of attention in conscious vision. In 2 experiments, we found that minimizing spatial attention almost entirely erases visual WM, as expected. Critically, FM remains largely intact. Moreover, minimally attended FM responses yield accurate metacognition, suggesting that conscious memory persists with limited spatial attention. Together, our findings help resolve the fundamental issue of how attention affects perception: Both visual consciousness and memory can be supported by only minimal attention. (PsycINFO Database Record

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.

The time course of natural scene perception with reduced attention.

Attention is thought to impose an informational bottleneck on vision by selecting particular information from visual scenes for enhanced processing. Behavioral evidence suggests, however, that some scene information is extracted even when attention is directed elsewhere. Here, we investigated the neural correlates of this ability by examining how attention affects electrophysiological markers of scene perception. In two electro-encephalography (EEG) experiments, human subjects categorized real-world scenes as manmade or natural (full attention condition) or performed tasks on unrelated stimuli in the center or periphery of the scenes (reduced attention conditions). Scene processing was examined in two ways: traditional trial averaging was used to assess the presence of a categorical manmade/natural distinction in event-related potentials, whereas single-trial analyses assessed whether EEG activity was modulated by scene statistics that are diagnostic of naturalness of individual scenes. The results indicated that evoked activity up to 250 ms was unaffected by reduced attention, showing intact categorical differences between manmade and natural scenes and strong modulations of single-trial activity by scene statistics in all conditions. Thus initial processing of both categorical and individual scene information remained intact with reduced attention. Importantly, however, attention did have profound effects on later evoked activity; full attention on the scene resulted in prolonged manmade/natural differences, increased neural sensitivity to scene statistics, and enhanced scene memory. These results show that initial processing of real-world scene information is intact with diminished attention but that the depth of processing of this information does depend on attention.

No-Report Paradigms: Extracting the True Neural Correlates of Consciousness.

The goal of consciousness research is to reveal the neural basis of phenomenal experience. To study phenomenology, experimenters seem obliged to ask reports from the subjects to ascertain what they experience. However, we argue that the requirement of reports has biased the search for the neural correlates of consciousness over the past decades. More recent studies attempt to dissociate neural activity that gives rise to consciousness from the activity that enables the report; in particular, no-report paradigms have been utilized to study conscious experience in the full absence of any report. We discuss the advantages and disadvantages of report-based and no-report paradigms, and ask how these jointly bring us closer to understanding the true neural basis of consciousness.

Neural Correlates of Visual Short-term Memory Dissociate between Fragile and Working Memory Representations.

Evidence is accumulating that the classic two-stage model of visual STM (VSTM), comprising iconic memory (IM) and visual working memory (WM), is incomplete. A third memory stage, termed fragile VSTM (FM), seems to exist in between IM and WM [Vandenbroucke, A. R. E., Sligte, I. G., & Lamme, V. A. F. Manipulations of attention dissociate fragile visual STM from visual working memory. Neuropsychologia, 49, 1559-1568, 2011; Sligte, I. G., Scholte, H. S., & Lamme, V. A. F. Are there multiple visual STM stores? PLoS One, 3, e1699, 2008]. Although FM can be distinguished from IM using behavioral and fMRI methods, the question remains whether FM is a weak expression of WM or a separate form of memory with its own neural signature. Here, we tested whether FM and WM in humans are supported by dissociable time-frequency features of EEG recordings. Participants performed a partial-report change detection task, from which individual differences in FM and WM capacity were estimated. These individual FM and WM capacities were correlated with time-frequency characteristics of the EEG signal before and during encoding and maintenance of the memory display. FM capacity showed negative alpha correlations over peri-occipital electrodes, whereas WM capacity was positively related, suggesting increased visual processing (lower alpha) to be related to FM capacity. Furthermore, FM capacity correlated with an increase in theta power over central electrodes during preparation and processing of the memory display, whereas WM did not. In addition to a difference in visual processing characteristics, a positive relation between gamma power and FM capacity was observed during both preparation and maintenance periods of the task. On the other hand, we observed that theta-gamma coupling was negatively correlated with FM capacity, whereas it was slightly positively correlated with WM. These data show clear differences in the neural substrates of FM versus WM and suggest that FM depends more on visual processing mechanisms compared with WM. This study thus provides novel evidence for a dissociation between different stages in VSTM.

Expectations accelerate entry of visual stimuli into awareness.

How do expectations influence transitions between unconscious and conscious perceptual processing? According to the influential predictive processing framework, perceptual content is determined by predictive models of the causes of sensory signals. On one interpretation, conscious contents arise when predictive models are verified by matching sensory input (minimizing prediction error). On another, conscious contents arise when surprising events falsify current perceptual predictions. Finally, the cognitive impenetrability account posits that conscious perception is not affected by such higher level factors. To discriminate these positions, we combined predictive cueing with continuous flash suppression (CFS) in which the relative contrast of a target image gradually increases over time. In four experiments we established that expected stimuli enter consciousness faster than neutral or unexpected stimuli. These effects are difficult to account for in terms of response priming, pre-existing stimulus associations, or the attentional mechanisms that cause asynchronous temporal order judgments (of simultaneously presented stimuli). Our results further suggest that top-down expectations play a larger role when bottom-up input is ambiguous, in line with predictive processing accounts of perception. Taken together, our findings support the hypothesis that conscious access depends on verification of perceptual predictions.

Forgotten but not gone: Retro-cue costs and benefits in a double-cueing paradigm suggest multiple states in visual short-term memory.

Visual short-term memory (VSTM) performance is enhanced when the to-be-tested item is cued after encoding. This so-called retro-cue benefit is typically accompanied by a cost for the noncued items, suggesting that information is lost from VSTM upon presentation of a retrospective cue. Here we assessed whether noncued items can be restored to VSTM when made relevant again by a subsequent second cue. We presented either 1 or 2 consecutive retro-cues (80% valid) during the retention interval of a change-detection task. Relative to no cue, a valid cue increased VSTM capacity by 2 items, while an invalid cue decreased capacity by 2. Importantly, when a second, valid cue followed an invalid cue, capacity regained 2 items, so that performance was back on par. In addition, when the second cue was also invalid, there was no extra loss of information from VSTM, suggesting that those items that survived a first invalid cue, automatically also survived a second. We conclude that these results are in support of a very versatile VSTM system, in which memoranda adopt different representational states depending on whether they are deemed relevant now, in the future, or not at all. We discuss a neural model that is consistent with this conclusion.

Pupil size tracks perceptual content and surprise.

Changes in pupil size at constant light levels reflect the activity of neuromodulatory brainstem centers that control global brain state. These endogenously driven pupil dynamics can be synchronized with cognitive acts. For example, the pupil dilates during the spontaneous switches of perception of a constant sensory input in bistable perceptual illusions. It is unknown whether this pupil dilation only indicates the occurrence of perceptual switches, or also their content. Here, we measured pupil diameter in human subjects reporting the subjective disappearance and re-appearance of a physically constant visual target surrounded by a moving pattern ('motion-induced blindness' illusion). We show that the pupil dilates during the perceptual switches in the illusion and a stimulus-evoked 'replay' of that illusion. Critically, the switch-related pupil dilation encodes perceptual content, with larger amplitude for disappearance than re-appearance. This difference in pupil response amplitude enables prediction of the type of report (disappearance vs. re-appearance) on individual switches (receiver-operating characteristic: 61%). The amplitude difference is independent of the relative durations of target-visible and target-invisible intervals and subjects' overt behavioral report of the perceptual switches. Further, we show that pupil dilation during the replay also scales with the level of surprise about the timing of switches, but there is no evidence for an interaction between the effects of surprise and perceptual content on the pupil response. Taken together, our results suggest that pupil-linked brain systems track both the content of, and surprise about, perceptual events.

Consciousness is not necessary for visual feature binding.

When visual information enters the brain, it is relayed to different specialized regions, processing features such as shape, color, or motion. And yet, in our conscious experience of a colored, moving shape, all the different features seem to be integrated into one unified percept. Therefore, it has been hypothesized that consciousness and feature binding share an intimate relationship. To study this relationship, we used a paradigm in which the behavioral effects of feature binding can be measured. Using masks, we investigated whether spontaneous binding between the orientation and location of a Gabor patch takes place when the Gabor patch is processed consciously or unconsciously. The results of our study suggest that orientation and location of a visually presented object are automatically integrated, even when subjects are unaware of that object. We conclude that binding and consciousness share a less intimate relationship than previously hypothesized, since consciousness is not a necessary condition for binding to occur.