General validity of Levelt's propositions reveals common computational mechanisms for visual rivalry

The mechanisms underlying conscious visual perception are often studied with either binocular rivalry or perceptual rivalry stimuli. Despite existing research into both types of rivalry, it remains unclear to what extent their underlying mechanisms involve common computational rules. Computational models of binocular rivalry mechanisms are generally tested against Levelt's four propositions, describing the psychophysical relation between stimulus strength and alternation dynamics in binocular rivalry. Here we use a bistable rotating structure-from-motion sphere, a generally studied form of perceptual rivalry, to demonstrate that Levelt's propositions also apply to the alternation dynamics of perceptual rivalry. Importantly, these findings suggest that bistability in structure-from-motion results from active cross-inhibition between neural populations with computational principles similar to those present in binocular rivalry. Thus, although the neural input to the computational mechanism of rivalry may stem from different cortical neurons and different cognitive levels the computational principles just prior to the production of visual awareness appear to be common to the two types of rivalry.     

Definitions of state variables and state space for brain–computer interface

The hypothesis is proposed that the central dynamics of the action–perception cycle has five steps: emergence from an existing macroscopic brain state of a pattern that predicts a future goal state; selection of a mesoscopic frame for action control; execution of a limb trajectory by microscopic spike activity; modification of microscopic cortical spike activity by sensory inputs; construction of mesoscopic perceptual patterns; and integration of a new macroscopic brain state. The basis is the circular causality between microscopic entities (neurons) and the mesoscopic and macroscopic entities (populations) self-organized by axosynaptic interactions. Self-organization of neural activity is bidirectional in all cortices. Upwardly the organization of mesoscopic percepts from microscopic spike input predominates in primary sensory areas. Downwardly the organization of spike outputs that direct specific limb movements is by mesoscopic fields constituting plans to achieve predicted goals. The mesoscopic fields in sensory and motor cortices emerge as frames within macroscopic activity. Part 1 describes the action–perception cycle and its derivative reflex arc qualitatively. Part 2 describes the perceptual limb of the arc from microscopic MSA to mesoscopic wave packets, and from these to macroscopic EEG and global ECoG fields that express experience-dependent knowledge in successive states. These macroscopic states are conceived to embed and control mesoscopic frames in premotor and motor cortices that are observed in local ECoG and LFP of frontoparietal areas. The fields sampled by ECoG and LFP are conceived as local patterns of neural activity in which trajectories of multiple spike activities (MSA) emerge that control limb movements. Mesoscopic frames are located by use of the analytic signal from the Hilbert transform after band pass filtering. The state variables in frames are measured to construct feature vectors by which to describe and classify frame patterns. Evidence is cited to justify use of linear analysis. The aim of the review is to enable researchers to conceive and identify goal-oriented states in brain activity for use as commands, in order to relegate the details of execution to adaptive control devices outside the brain. http://sulcus.berkeley.edu     

Single units and conscious vision.

Figures that can be seen in more than one way are invaluable tools for the study of the neural basis of visual awareness, because such stimuli permit the dissociation of the neural responses that underlie what we perceive at any given time from those forming the sensory representation of a visual pattern. To study the former type of responses, monkeys were subjected to binocular rivalry, and the response of neurons in a number of different visual areas was studied while the animals reported their alternating percepts by pulling levers. Perception-related modulations of neural activity were found to occur to different extents in different cortical visual areas. The cells that were affected by suppression were almost exclusively binocular, and their proportion was found to increase in the higher processing stages of the visual system. The strongest correlations between neural activity and perception were observed in the visual areas of the temporal lobe. A strikingly large number of neurons in the early visual areas remained active during the perceptual suppression of the stimulus, a finding suggesting that conscious visual perception might be mediated by only a subset of the cells exhibiting stimulus selective responses. These physiological findings, together with a number of recent psychophysical studies, offer a new explanation of the phenomenon of binocular rivalry. Indeed, rivalry has long been considered to be closely linked with binocular fusion and stereopsis, and the sequences of dominance and suppression have been viewed as the result of competition between the two monocular channels. The physiological data presented here are incompatible with this interpretation. Rather than reflecting interocular competition, the rivalry is most probably between the two different central neural representations generated by the dichoptically presented stimuli. The mechanisms of rivalry are probably the same as, or very similar to, those underlying multistable perception in general, and further physiological studies might reveal much about the neural mechanisms of our perceptual organization.     

Neuronal discharges and gamma oscillations explicitly reflect visual consciousness in the lateral prefrontal cortex

Neuronal discharges in the primate temporal lobe, but not in the striate and extrastriate cortex, reliably reflect stimulus awareness. However, it is not clear whether visual consciousness should be uniquely localized in the temporal association cortex. Here we used binocular flash suppression to investigate whether visual awareness is also explicitly reflected in feature-selective neural activity of the macaque lateral prefrontal cortex (LPFC), a cortical area reciprocally connected to the temporal lobe. We show that neuronal discharges in the majority of single units and recording sites in the LPFC follow the phenomenal perception of a preferred stimulus. Furthermore, visual awareness is reliably reflected in the power modulation of high-frequency (>50?Hz) local field potentials in sites where spiking activity is found to be perceptually modulated. Our results suggest that the activity of neuronal populations in at least two association cortical areas represents the content of conscious visual perception.     

Mesoscopic neurodynamics: From neuron to brain

Intelligent behavior is characterized by flexible and creative pursuit of endogenously defined goals. Intentionality is a key concept by which to link neuron and brain to goal-directed behavior through brain dynamics. An archetypal form of intentional behavior is an act of observation in space-time, by which information is sought for the guidance of future action to explore unpredictable and ever-changing environments. These acts are based in the brain dynamics that creates spatiotemporal patterns of neural activity, serving as images of goals, of command sequences by which to act to reach goals, and of expected changes in sensory input resulting from intended actions. Prediction of the sensory consequences of intended action and evaluation of performance is by reafference. An intentional act is completed upon modification of the system by itself through learning. These principles are well known among psychologists and philosophers. What is new is the development of nonlinear mesoscopic brain dynamics, by which the theory of chaos can be used to understand and simulate the constructions of meaningful patterns of neural activity that implement the process of observation. The design of neurobiological experiments, analysis of the resulting data, and synthesis of explanatory models require an understanding of the hierarchical nature of brain organization, here conceived as single neurons and neural networks at the microscopic level; clinically defined cortical and subcortical systems studied by brain imaging (for example, fMRI) at the macroscopic level, and self-organizing neural populations at an intermediate mesoscopic level, at which synaptic interactions create novel activity patterns through nonlinear state transitions. The constructive neurodynamics of sensory cortices, when they are engaged in pattern recognition, is revealed by learning-dependent spatial patterns of amplitude modulation and by newly discovered radially symmetric spatial gradients of the phase of aperiodic carrier waves in multichannel subdural EEG recordings.     

From crawling to cognition: analyzing the dynamical interactions among populations of neurons

By using multi-electrode arrays or optical imaging, investigators can now record from many individual neurons in various parts of nervous systems simultaneously while an animal performs sensory, motor or cognitive tasks. Given the large multidimensional datasets that are now routinely generated, it is often not obvious how to find meaningful results within the data. The analysis of neuronal-population recordings typically involves two steps: the extraction of relevant dynamics from neural data, and then use of the dynamics to classify and discriminate features of a stimulus or behavior. We focus on the application of techniques that emphasize interactions among the recorded neurons rather than using just the correlations between individual neurons and a perception or a behavior. An understanding of modern analysis techniques is crucially important for researchers interested in the co-varying activity among populations of neurons or even brain regions.     

What electrical microstimulation has revealed about the neural basis of cognition

Neurophysiologists have shown repeatedly that neural activity in different brain structures can be correlated with specific perceptual and cognitive functions, but the causal efficacy of the observed activity has generally been a matter of conjecture. By contrast, electrical microstimulation, which allows the experimenter to manipulate the activity of small groups of neurons with spatial and temporal precision, can now be used to demonstrate causal links between neural activity and specific cognitive functions. Here, we review this growing literature, including applications to the study of attention, visual and somatosensory perception, 'read-out' mechanisms for interpreting sensory maps, and contextual effects on perception. We also discuss potential applications of microstimulation to studies of higher cognitive functions such as decision-making and subjective experience.     

Conscious awareness of flicker in humans involves frontal and parietal cortex

Even when confined to the same spatial location, flickering and steady light evoke very different conscious experiences because of their distinct temporal patterns. The neural basis of such differences in subjective experience remains uncertain . Here, we used functional MRI in humans to examine the neural structures involved in awareness of flicker. Participants viewed a single point source of light that flickered at the critical flicker fusion (CFF) threshold, where the same stimulus is sometimes perceived as flickering and sometimes as steady (fused) . We were thus able to compare brain activity for conscious percepts that differed qualitatively (flickering or fused) but were evoked by identical physical stimuli. Greater brain activation was observed on flicker (versus fused) trials in regions of frontal and parietal cortex previously associated with visual awareness in tasks that did not require detection of temporal patterns . In contrast, greater activation was observed on fused (versus flicker) trials in occipital extrastriate cortex. Our findings indicate that activity of higher-level cortical areas is important for awareness of temporally distinct visual events in the context of a nonspatial task, and they thus suggest that frontal and parietal regions may play a general role in visual awareness.     

Robust Single Trial Identification of Conscious Percepts Triggered by Sensory Events of Variable Saliency

The neural correlates of visual awareness are elusive because of its fleeting nature. Here we have addressed this issue by using single trial statistical “brain reading” of neurophysiological event related (ERP) signatures of conscious perception of visual attributes with different levels of saliency. Behavioral reports were taken at every trial in 4 experiments addressing conscious access to color, luminance, and local phase offset cues. We found that single trial neurophysiological signatures of target presence can be observed around 300 ms at central parietal sites. Such signatures are significantly related with conscious perception, and their probability is related to sensory saliency levels. These findings identify a general neural correlate of conscious perception at the single trial level, since conscious perception can be decoded as such independently of stimulus salience and fluctuations of threshold levels. This approach can be generalized to successfully detect target presence in other individuals.     

What we see is how we are: new paradigms in visual research

As most sensory modalities, the visual system needs to deal with very fast changes in the environment. Instead of processing all sensory stimuli, the brain is able to construct a perceptual experience by combining selected sensory input with an ongoing internal activity. Thus, the study of visual perception needs to be approached by examining not only the physical properties of stimuli, but also the brain's ongoing dynamical states onto which these perturbations are imposed. At least three different models account for this internal dynamics. One model is based on cardinal cells where the activity of few cells by itself constitutes the neuronal correlate of perception, while a second model is based on a population coding that states that the neuronal correlate of perception requires distributed activity throughout many areas of the brain. A third proposition, known as the temporal correlation hypothesis states that the distributed neuronal populations that correlate with perception, are also defined by synchronization of the activity on a millisecond time scale. This would serve to encode contextual information by defining relations between the features of visual objects. If temporal properties of neural activity are important to establish the neural mechanisms of perception, then the study of appropriate dynamical stimuli should be instrumental to determine how these systems operate. The use of natural stimuli and natural behaviors such as free viewing, which features fast changes of internal brain states as seen by motor markers, is proposed as a new experimental paradigm to study visual perception.     

A Common Neurodynamical Mechanism Could Mediate Externally Induced and Intrinsically Generated Transitions in Visual Awareness

The neural correlates of conscious visual perception are commonly studied in paradigms of perceptual multistability that allow multiple perceptual interpretations during unchanged sensory stimulation. What is the source of this multistability in the content of perception? From a theoretical perspective, a fine balance between deterministic and stochastic forces has been suggested to underlie the spontaneous, intrinsically driven perceptual transitions observed during multistable perception. Deterministic forces are represented by adaptation of feature-selective neuronal populations encoding the competing percepts while stochastic forces are modeled as noise-driven processes. Here, we used a unified neuronal competition model to study the dynamics of adaptation and noise processes in binocular flash suppression (BFS), a form of externally induced perceptual suppression, and compare it with the dynamics of intrinsically driven alternations in binocular rivalry (BR). For the first time, we use electrophysiological, biologically relevant data to constrain a model of perceptual rivalry. Specifically, we show that the mean population discharge pattern of a perceptually modulated neuronal population detected in electrophysiological recordings in the lateral prefrontal cortex (LPFC) during BFS, constrains the dynamical range of externally induced perceptual transitions to a region around the bifurcation separating a noise-driven attractor regime from an adaptation-driven oscillatory regime. Most interestingly, the dynamical range of intrinsically driven perceptual transitions during BR is located in the noise-driven attractor regime, where it overlaps with BFS. Our results suggest that the neurodynamical mechanisms of externally induced and spontaneously generated perceptual alternations overlap in a narrow, noise-driven region just before a bifurcation where the system becomes adaptation-driven.     

When the brain loses its self: prefrontal inactivation during sensorimotor processing

A common theme in theories of subjective awareness poses a self-related "observer" function, or a homunculus, as a critical element without which awareness can not emerge. Here, we examined this question using fMRI. In our study, we compared brain activity patterns produced by a demanding sensory categorization paradigm to those engaged during self-reflective introspection, using similar sensory stimuli. Our results show a complete segregation between the two patterns of activity. Furthermore, regions that showed enhanced activity during introspection underwent a robust inhibition during the demanding perceptual task. The results support the notion that self-related processes are not necessarily engaged during sensory perception and can be actually suppressed.     

Reentrant Processing in Intuitive Perception

The process of perception requires not only the brain''s receipt of sensory data but also the meaningful organization of that data in relation to the perceptual experience held in memory. Although it typically results in a conscious percept, the process of perception is not fully conscious. Research on the neural substrates of human visual perception has suggested that regions of limbic cortex, including the medial orbital frontal cortex (mOFC), may contribute to intuitive judgments about perceptual events, such as guessing whether an object might be present in a briefly presented fragmented drawing. Examining dense array measures of cortical electrical activity during a modified Waterloo Gestalt Closure Task, results show, as expected, that activity in medial orbital frontal electrical responses (about 250 ms) was associated with intuitive judgments. Activity in the right temporal-parietal-occipital (TPO) region was found to predict mOFC (∼150 ms) activity and, in turn, was subsequently influenced by the mOFC at a later time (∼300 ms). The initial perception of gist or meaning of a visual stimulus in limbic networks may thus yield reentrant input to the visual areas to influence continued development of the percept. Before perception is completed, the initial representation of gist may support intuitive judgments about the ongoing perceptual process.     

Bistable Perception Modeled as Competing Stochastic Integrations at Two Levels

We propose a novel explanation for bistable perception, namely, the collective dynamics of multiple neural populations that are individually meta-stable. Distributed representations of sensory input and of perceptual state build gradually through noise-driven transitions in these populations, until the competition between alternative representations is resolved by a threshold mechanism. The perpetual repetition of this collective race to threshold renders perception bistable. This collective dynamics – which is largely uncoupled from the time-scales that govern individual populations or neurons – explains many hitherto puzzling observations about bistable perception: the wide range of mean alternation rates exhibited by bistable phenomena, the consistent variability of successive dominance periods, and the stabilizing effect of past perceptual states. It also predicts a number of previously unsuspected relationships between observable quantities characterizing bistable perception. We conclude that bistable perception reflects the collective nature of neural decision making rather than properties of individual populations or neurons.     

Predicting the stream of consciousness from activity in human visual cortex

Can the rapid stream of conscious experience be predicted from brain activity alone? Recently, spatial patterns of activity in visual cortex have been successfully used to predict feature-specific stimulus representations for both visible and invisible stimuli. However, because these studies examined only the prediction of static and unchanging perceptual states during extended periods of stimulation, it remains unclear whether activity in early visual cortex can also predict the rapidly and spontaneously changing stream of consciousness. Here, we used binocular rivalry to induce frequent spontaneous and stochastic changes in conscious experience without any corresponding changes in sensory stimulation, while measuring brain activity with fMRI. Using information that was present in the multivariate pattern of responses to stimulus features, we could accurately predict, and therefore track, participants' conscious experience from the fMRI signal alone while it underwent many spontaneous changes. Prediction in primary visual cortex primarily reflected eye-based signals, whereas prediction in higher areas reflected the color of the percept. Furthermore, accurate prediction during binocular rivalry could be established with signals recorded during stable monocular viewing, showing that prediction generalized across viewing conditions and did not require or rely on motor responses. It is therefore possible to predict the dynamically changing time course of subjective experience with only brain activity.     

Perceptual grouping of biological motion promotes binocular rivalry

Investigation of perceptual rivalry between conflicting stimuli presented one to each eye can further understanding of the neural underpinnings of conscious visual perception. During rivalry, visual awareness fluctuates between perceptions of the two stimuli. Here, we demonstrate that high-level perceptual grouping can promote rivalry between stimulus pairs that would otherwise be perceived as nonrivalrous. Perceptual grouping was generated with point-light walker stimuli that simulate human motion, visible only as lights placed on the joints. Although such walking figures are unrecognizable when stationary, recognition judgments as complex as gender and identity can accurately be made from animated displays, demonstrating the efficiency with which our visual system can group dynamic local signals into a globally coherent walking figure. We find that point-light walker stimuli presented one to each eye and in different colors and configurations results in strong rivalry. However, rivalry is minimal when the two walkers are split between the eyes or both presented to one eye. This pattern of results suggests that processing animated walker figures promotes rivalry between signals from the two eyes rather than between higher-level representations of the walkers. This leads us to hypothesize that awareness during binocular rivalry involves the integrated activity of high-level perceptual mechanisms in conjunction with lower-level ocular suppression modulated via cortical feedback.     

Can binocular rivalry reveal neural correlates of consciousness?

This essay critically examines the extent to which binocular rivalry can provide important clues about the neural correlates of conscious visual perception. Our ideas are presented within the framework of four questions about the use of rivalry for this purpose: (i) what constitutes an adequate comparison condition for gauging rivalry''s impact on awareness, (ii) how can one distinguish abolished awareness from inattention, (iii) when one obtains unequivocal evidence for a causal link between a fluctuating measure of neural activity and fluctuating perceptual states during rivalry, will it generalize to other stimulus conditions and perceptual phenomena and (iv) does such evidence necessarily indicate that this neural activity constitutes a neural correlate of consciousness? While arriving at sceptical answers to these four questions, the essay nonetheless offers some ideas about how a more nuanced utilization of binocular rivalry may still provide fundamental insights about neural dynamics, and glimpses of at least some of the ingredients comprising neural correlates of consciousness, including those involved in perceptual decision-making.     

Encoding of Naturalistic Stimuli by Local Field Potential Spectra in Networks of Excitatory and Inhibitory Neurons

Recordings of local field potentials (LFPs) reveal that the sensory cortex displays rhythmic activity and fluctuations over a wide range of frequencies and amplitudes. Yet, the role of this kind of activity in encoding sensory information remains largely unknown. To understand the rules of translation between the structure of sensory stimuli and the fluctuations of cortical responses, we simulated a sparsely connected network of excitatory and inhibitory neurons modeling a local cortical population, and we determined how the LFPs generated by the network encode information about input stimuli. We first considered simple static and periodic stimuli and then naturalistic input stimuli based on electrophysiological recordings from the thalamus of anesthetized monkeys watching natural movie scenes. We found that the simulated network produced stimulus-related LFP changes that were in striking agreement with the LFPs obtained from the primary visual cortex. Moreover, our results demonstrate that the network encoded static input spike rates into gamma-range oscillations generated by inhibitory–excitatory neural interactions and encoded slow dynamic features of the input into slow LFP fluctuations mediated by stimulus–neural interactions. The model cortical network processed dynamic stimuli with naturalistic temporal structure by using low and high response frequencies as independent communication channels, again in agreement with recent reports from visual cortex responses to naturalistic movies. One potential function of this frequency decomposition into independent information channels operated by the cortical network may be that of enhancing the capacity of the cortical column to encode our complex sensory environment.     

Negative BOLD differentiates visual imagery and perception

Recent studies emphasize the overlap between the neural substrates of visual perception and visual imagery. However, the subjective experiences of imagining and seeing are clearly different. Here we demonstrate that deactivation of auditory cortex (and to some extent of somatosensory and subcortical visual structures) as measured by BOLD functional magnetic resonance imaging unequivocally differentiates visual imagery from visual perception. During visual imagery, auditory cortex deactivation negatively correlates with activation in visual cortex and with the score in the subjective vividness of visual imagery questionnaire (VVIQ). Perception of the world requires the merging of multisensory information so that, during seeing, information from other sensory systems modifies visual cortical activity and shapes experience. We suggest that pure visual imagery corresponds to the isolated activation of visual cortical areas with concurrent deactivation of "irrelevant" sensory processing that could disrupt the image created by our "mind's eye."     

United we sense, divided we fail: context-driven perception of ambiguous visual stimuli

Ambiguous visual stimuli provide the brain with sensory information that contains conflicting evidence for multiple mutually exclusive interpretations. Two distinct aspects of the phenomenological experience associated with viewing ambiguous visual stimuli are the apparent stability of perception whenever one perceptual interpretation is dominant, and the instability of perception that causes perceptual dominance to alternate between perceptual interpretations upon extended viewing. This review summarizes several ways in which contextual information can help the brain resolve visual ambiguities and construct temporarily stable perceptual experiences. Temporal context through prior stimulation or internal brain states brought about by feedback from higher cortical processing levels may alter the response characteristics of specific neurons involved in rivalry resolution. Furthermore, spatial or crossmodal context may strengthen the neuronal representation of one of the possible perceptual interpretations and consequently bias the rivalry process towards it. We suggest that contextual influences on perceptual choices with ambiguous visual stimuli can be highly informative about the neuronal mechanisms of context-driven inference in the general processes of perceptual decision-making.