Network mechanisms of ongoing brain activity's influence on conscious visual perception.

Sensory inputs enter a constantly active brain, whose state is always changing from one moment to the next. Currently, little is known about how ongoing, spontaneous brain activity participates in online task processing. We employed 7 Tesla fMRI and a threshold-level visual perception task to probe the effects of prestimulus ongoing brain activity on perceptual decision-making and conscious recognition. Prestimulus activity originating from distributed brain regions, including visual cortices and regions of the default-mode and cingulo-opercular networks, exerted a diverse set of effects on the sensitivity and criterion of conscious recognition, and categorization performance. We further elucidate the mechanisms underlying these behavioral effects, revealing how prestimulus activity modulates multiple aspects of stimulus processing in highly specific and network-dependent manners. These findings reveal heretofore unknown network mechanisms underlying ongoing brain activity's influence on conscious perception, and may hold implications for understanding the precise roles of spontaneous activity in other brain functions.

Integrating Consciousness Science with Cognitive Neuroscience: An Introduction to the Special Focus.

Consciousness science is experiencing a coming-of-age moment. Following 3 decades of sustained efforts by a relatively small group of consciousness researchers, the field has seen exponential growth over the past 5 years. It is increasingly recognized that although the investigation of subjective experiences is a difficult task, modern neuroscience need not and cannot shy away from the challenge of peeling away the mysteries of conscious experiences. In June 2023, with the joint support of the U.S. National Institutes of Health and the U.S. National Science Foundation, a 3-day workshop was held at the Bethesda, MD, campus of the National Institutes of Health, convening experts whose work focuses primarily on problems of consciousness, or an adjacent field, to discuss the current state of consciousness science and consider the most fruitful avenues for future research. This Special Focus features empirical and theoretical contributions from some of the invited speakers at the workshop. Here, I will cover the scope of the workshop, the content of this Special Focus, and advocate for stronger bridges between consciousness science and other subdisciplines of cognitive neuroscience.

A novel, semi-automatic procedure for generating slow change blindness stimuli.

Change blindness is the phenomenon that occurs when an observer fails to notice what would seem to be obvious changes in the features of a visual stimulus. Researchers can induce this experimentally by including visual disruptions (such as brief blanks) that coincide with the changes in question. However, change blindness can also occur in the absence of these disruptions if a change occurs sufficiently slowly. This "slow" or "gradual" change blindness phenomenon has not been extensively researched. Two plausible practical reasons for this are that there are few slow-change stimuli available, and that it is difficult to collect trial-specific responses without affecting expectations on later trials. Here, we describe a novel, semi-automatic procedure for quickly generating many slow-change stimuli. This procedure creates stimuli that have been specifically designed to allow assessment of change blindness on individual trials without influencing subsequent trials. We include the results of three validation experiments that demonstrate that these stimuli are effective and suitable for use in systematic studies of slow change blindness.

Neural Mechanisms Determining the Duration of Task-free, Self-paced Visual Perception.

Humans spend hours each day spontaneously engaging with visual content, free from specific tasks and at their own pace. Currently, the brain mechanisms determining the duration of self-paced perceptual behavior remain largely unknown. Here, participants viewed naturalistic images under task-free settings and self-paced each image's viewing duration while undergoing EEG and pupillometry recordings. Across two independent data sets, we observed large inter- and intra-individual variability in viewing duration. However, beyond an image's presentation order and category, specific image content had no consistent effects on spontaneous viewing duration across participants. Overall, longer viewing durations were associated with sustained enhanced posterior positivity and anterior negativity in the ERPs. Individual-specific variations in the spontaneous viewing duration were consistently correlated with evoked EEG activity amplitudes and pupil size changes. By contrast, presentation order was selectively correlated with baseline alpha power and baseline pupil size. Critically, spontaneous viewing duration was strongly predicted by the temporal stability in neural activity patterns starting as early as 350 msec after image onset, suggesting that early neural stability is a key predictor for sustained perceptual engagement. Interestingly, neither bottom-up nor top-down predictions about image category influenced spontaneous viewing duration. Overall, these results suggest that individual-specific factors can influence perceptual processing at a surprisingly early time point and influence the multifaceted ebb and flow of spontaneous human perceptual behavior in naturalistic settings.

Next frontiers in consciousness research.

Consciousness science has matured over the past three decades and is currently on the cusp of explosive growth, with the potential to transform medicine and technology. The global community recently met to synthesize the current state of knowledge and define the most exciting approaches to advance the field.

Spatiotemporal neural dynamics of object recognition under uncertainty in humans.

While there is a wealth of knowledge about core object recognition-our ability to recognize clear, high-contrast object images-how the brain accomplishes object recognition tasks under increased uncertainty remains poorly understood. We investigated the spatiotemporal neural dynamics underlying object recognition under increased uncertainty by combining MEG and 7 Tesla (7T) fMRI in humans during a threshold-level object recognition task. We observed an early, parallel rise of recognition-related signals across ventral visual and frontoparietal regions that preceded the emergence of category-related information. Recognition-related signals in ventral visual regions were best explained by a two-state representational format whereby brain activity bifurcated for recognized and unrecognized images. By contrast, recognition-related signals in frontoparietal regions exhibited a reduced representational space for recognized images, yet with sharper category information. These results provide a spatiotemporally resolved view of neural activity supporting object recognition under uncertainty, revealing a pattern distinct from that underlying core object recognition.

Towards a pluralistic neurobiological understanding of consciousness.

Theories of consciousness are often based on the assumption that a single, unified neurobiological account will explain different types of conscious awareness. However, recent findings show that, even within a single modality such as conscious visual perception, the anatomical location, timing, and information flow of neural activity related to conscious awareness vary depending on both external and internal factors. This suggests that the search for generic neural correlates of consciousness may not be fruitful. I argue that consciousness science requires a more pluralistic approach and propose a new framework: joint determinant theory (JDT). This theory may be capable of accommodating different brain circuit mechanisms for conscious contents as varied as percepts, wills, memories, emotions, and thoughts, as well as their integrated experience.

Frequency-specific neural signatures of perceptual content and perceptual stability.

In the natural environment, we often form stable perceptual experiences from ambiguous and fleeting sensory inputs. Which neural activity underlies the content of perception and which neural activity supports perceptual stability remains an open question. We used a bistable perception paradigm involving ambiguous images to behaviorally dissociate perceptual content from perceptual stability, and magnetoencephalography to measure whole-brain neural dynamics in humans. Combining multivariate decoding and neural state-space analyses, we found frequency-band-specific neural signatures that underlie the content of perception and promote perceptual stability, respectively. Across different types of images, non-oscillatory neural activity in the slow cortical potential (<5 Hz) range supported the content of perception. Perceptual stability was additionally influenced by the amplitude of alpha and beta oscillations. In addition, neural activity underlying perceptual memory, which supports perceptual stability when sensory input is temporally removed from view, also encodes elapsed time. Together, these results reveal distinct neural mechanisms that support the content versus stability of visual perception.

Neural oscillations promoting perceptual stability and perceptual memory during bistable perception.

Ambiguous images elicit bistable perception, wherein periods of momentary perceptual stability are interrupted by sudden perceptual switches. When intermittently presented, ambiguous images trigger a perceptual memory trace in the intervening blank periods. Understanding the neural bases of perceptual stability and perceptual memory during bistable perception may hold clues for explaining the apparent stability of visual experience in the natural world, where ambiguous and fleeting images are prevalent. Motivated by recent work showing the involvement of the right inferior frontal gyrus (rIFG) in bistable perception, we conducted a transcranial direct-current stimulation (tDCS) study with a double-blind, within-subject cross-over design to test a potential causal role of rIFG in these processes. Subjects viewed ambiguous images presented continuously or intermittently while under EEG recording. We did not find any significant tDCS effect on perceptual behavior. However, the fluctuations of oscillatory power in the alpha and beta bands predicted perceptual stability, with higher power corresponding to longer percept durations. In addition, higher alpha and beta power predicted enhanced perceptual memory during intermittent viewing. These results reveal a unified neurophysiological mechanism sustaining perceptual stability and perceptual memory when the visual system is faced with ambiguous input.

Long-term priors influence visual perception through recruitment of long-range feedback.

Perception results from the interplay of sensory input and prior knowledge. Despite behavioral evidence that long-term priors powerfully shape perception, the neural mechanisms underlying these interactions remain poorly understood. We obtained direct cortical recordings in neurosurgical patients as they viewed ambiguous images that elicit constant perceptual switching. We observe top-down influences from the temporal to occipital cortex, during the preferred percept that is congruent with the long-term prior. By contrast, stronger feedforward drive is observed during the non-preferred percept, consistent with a prediction error signal. A computational model based on hierarchical predictive coding and attractor networks reproduces all key experimental findings. These results suggest a pattern of large-scale information flow change underlying long-term priors' influence on perception and provide constraints on theories about long-term priors' influence on perception.

State-related neural influences on fMRI connectivity estimation.

The spatiotemporal structure of functional magnetic resonance imaging (fMRI) signals has provided a valuable window into the network underpinnings of human brain function and dysfunction. Although some cross-regional temporal correlation patterns (functional connectivity; FC) exhibit a high degree of stability across individuals and species, there is growing acknowledgment that measures of FC can exhibit marked changes over a range of temporal scales. Further, FC can co-vary with experimental task demands and ongoing neural processes linked to arousal, consciousness and perception, cognitive and affective state, and brain-body interactions. The increased recognition that such interrelated neural processes modulate FC measurements has raised both challenges and new opportunities in using FC to investigate brain function. Here, we review recent advances in the quantification of neural effects that shape fMRI FC and discuss the broad implications of these findings in the design and analysis of fMRI studies. We also discuss how a more complete understanding of the neural factors that shape FC measurements can resolve apparent inconsistencies in the literature and lead to more interpretable conclusions from fMRI studies.

Spontaneous perception: a framework for task-free, self-paced perception.

Flipping through social media feeds, viewing exhibitions in a museum, or walking through the botanical gardens, people consistently choose to engage with and disengage from visual content. Yet, in most laboratory settings, the visual stimuli, their presentation duration, and the task at hand are all controlled by the researcher. Such settings largely overlook the spontaneous nature of human visual experience, in which perception takes place independently from specific task constraints and its time course is determined by the observer as a self-governing agent. Currently, much remains unknown about how spontaneous perceptual experiences unfold in the brain. Are all perceptual categories extracted during spontaneous perception? Does spontaneous perception inherently involve volition? Is spontaneous perception segmented into discrete episodes? How do different neural networks interact over time during spontaneous perception? These questions are imperative to understand our conscious visual experience in daily life. In this article we propose a framework for spontaneous perception. We first define spontaneous perception as a task-free and self-paced experience. We propose that spontaneous perception is guided by four organizing principles that grant it temporal and spatial structures. These principles include coarse-to-fine processing, continuity and segmentation, agency and volition, and associative processing. We provide key suggestions illustrating how these principles may interact with one another in guiding the multifaceted experience of spontaneous perception. We point to testable predictions derived from this framework, including (but not limited to) the roles of the default-mode network and slow cortical potentials in underlying spontaneous perception. We conclude by suggesting several outstanding questions for future research, extending the relevance of this framework to consciousness and spontaneous brain activity. In conclusion, the spontaneous perception framework proposed herein integrates components in human perception and cognition, which have been traditionally studied in isolation, and opens the door to understand how visual perception unfolds in its most natural context.

Spectral signature and behavioral consequence of spontaneous shifts of pupil-linked arousal in human.

Arousal levels perpetually rise and fall spontaneously. How markers of arousal-pupil size and frequency content of brain activity-relate to each other and influence behavior in humans is poorly understood. We simultaneously monitored magnetoencephalography and pupil in healthy volunteers at rest and during a visual perceptual decision-making task. Spontaneously varying pupil size correlates with power of brain activity in most frequency bands across large-scale resting state cortical networks. Pupil size recorded at prestimulus baseline correlates with subsequent shifts in detection bias (c) and sensitivity (d'). When dissociated from pupil-linked state, prestimulus spectral power of resting state networks still predicts perceptual behavior. Fast spontaneous pupil constriction and dilation correlate with large-scale brain activity as well but not perceptual behavior. Our results illuminate the relation between central and peripheral arousal markers and their respective roles in human perceptual decision-making.

One-trial perceptual learning in the absence of conscious remembering and independent of the medial temporal lobe.

A degraded, black-and-white image of an object, which appears meaningless on first presentation, is easily identified after a single exposure to the original, intact image. This striking example of perceptual learning reflects a rapid (one-trial) change in performance, but the kind of learning that is involved is not known. We asked whether this learning depends on conscious (hippocampus-dependent) memory for the images that have been presented or on an unconscious (hippocampus-independent) change in the perception of images, independently of the ability to remember them. We tested five memory-impaired patients with hippocampal lesions or larger medial temporal lobe (MTL) lesions. In comparison to volunteers, the patients were fully intact at perceptual learning, and their improvement persisted without decrement from 1 d to more than 5 mo. Yet, the patients were impaired at remembering the test format and, even after 1 d, were impaired at remembering the images themselves. To compare perceptual learning and remembering directly, at 7 d after seeing degraded images and their solutions, patients and volunteers took either a naming test or a recognition memory test with these images. The patients improved as much as the volunteers at identifying the degraded images but were severely impaired at remembering them. Notably, the patient with the most severe memory impairment and the largest MTL lesions performed worse than the other patients on the memory tests but was the best at perceptual learning. The findings show that one-trial, long-lasting perceptual learning relies on hippocampus-independent (nondeclarative) memory, independent of any requirement to consciously remember.

Neural integration underlying naturalistic prediction flexibly adapts to varying sensory input rate.

Prediction of future sensory input based on past sensory information is essential for organisms to effectively adapt their behavior in dynamic environments. Humans successfully predict future stimuli in various natural settings. Yet, it remains elusive how the brain achieves effective prediction despite enormous variations in sensory input rate, which directly affect how fast sensory information can accumulate. We presented participants with acoustic sequences capturing temporal statistical regularities prevalent in nature and investigated neural mechanisms underlying predictive computation using MEG. By parametrically manipulating sequence presentation speed, we tested two hypotheses: neural prediction relies on integrating past sensory information over fixed time periods or fixed amounts of information. We demonstrate that across halved and doubled presentation speeds, predictive information in neural activity stems from integration over fixed amounts of information. Our findings reveal the neural mechanisms enabling humans to robustly predict dynamic stimuli in natural environments despite large sensory input rate variations.

Cortical and subcortical signatures of conscious object recognition.

The neural mechanisms underlying conscious recognition remain unclear, particularly the roles played by the prefrontal cortex, deactivated brain areas and subcortical regions. We investigated neural activity during conscious object recognition using 7 Tesla fMRI while human participants viewed object images presented at liminal contrasts. Here, we show both recognized and unrecognized images recruit widely distributed cortical and subcortical regions; however, recognized images elicit enhanced activation of visual, frontoparietal, and subcortical networks and stronger deactivation of the default-mode network. For recognized images, object category information can be decoded from all of the involved cortical networks but not from subcortical regions. Phase-scrambled images trigger strong involvement of inferior frontal junction, anterior cingulate cortex and default-mode network, implicating these regions in inferential processing under increased uncertainty. Our results indicate that content-specific activity in both activated and deactivated cortical networks and non-content-specific subcortical activity support conscious recognition.

A Gradient of Sharpening Effects by Perceptual Prior across the Human Cortical Hierarchy.

Prior knowledge profoundly influences perceptual processing. Previous studies have revealed consistent suppression of predicted stimulus information in sensory areas, but how prior knowledge modulates processing higher up in the cortical hierarchy remains poorly understood. In addition, the mechanism leading to suppression of predicted sensory information remains unclear, and studies thus far have revealed a mixed pattern of results in support of either the "sharpening" or "dampening" model. Here, using 7T fMRI in humans (both sexes), we observed that prior knowledge acquired from fast, one-shot perceptual learning sharpens neural representation throughout the ventral visual stream, generating suppressed sensory responses. In contrast, the frontoparietal and default mode networks exhibit similar sharpening of content-specific neural representation, but in the context of unchanged and enhanced activity magnitudes, respectively: a pattern we refer to as "selective enhancement." Together, these results reveal a heretofore unknown macroscopic gradient of prior knowledge's sharpening effect on neural representations across the cortical hierarchy.SIGNIFICANCE STATEMENT A fundamental question in neuroscience is how prior knowledge shapes perceptual processing. Perception is constantly informed by internal priors in the brain acquired from past experiences, but the neural mechanisms underlying this process are poorly understood. To date, research on this question has focused on early visual regions, reporting a consistent downregulation when predicted stimuli are encountered. Here, using a dramatic one-shot perceptual learning paradigm, we observed that prior knowledge results in sharper neural representations across the cortical hierarchy of the human brain through a gradient of mechanisms. In visual regions, neural responses tuned away from internal predictions are suppressed. In frontoparietal regions, neural activity consistent with priors is selectively enhanced. These results deepen our understanding of how prior knowledge informs perception.

Task-evoked activity quenches neural correlations and variability across cortical areas.

Many large-scale functional connectivity studies have emphasized the importance of communication through increased inter-region correlations during task states. In contrast, local circuit studies have demonstrated that task states primarily reduce correlations among pairs of neurons, likely enhancing their information coding by suppressing shared spontaneous activity. Here we sought to adjudicate between these conflicting perspectives, assessing whether co-active brain regions during task states tend to increase or decrease their correlations. We found that variability and correlations primarily decrease across a variety of cortical regions in two highly distinct data sets: non-human primate spiking data and human functional magnetic resonance imaging data. Moreover, this observed variability and correlation reduction was accompanied by an overall increase in dimensionality (reflecting less information redundancy) during task states, suggesting that decreased correlations increased information coding capacity. We further found in both spiking and neural mass computational models that task-evoked activity increased the stability around a stable attractor, globally quenching neural variability and correlations. Together, our results provide an integrative mechanistic account that encompasses measures of large-scale neural activity, variability, and correlations during resting and task states.

Neuromodulation of Brain State and Behavior.

Neural activity and behavior are both notoriously variable, with responses differing widely between repeated presentation of identical stimuli or trials. Recent results in humans and animals reveal that these variations are not random in their nature, but may in fact be due in large part to rapid shifts in neural, cognitive, and behavioral states. Here we review recent advances in the understanding of rapid variations in the waking state, how variations are generated, and how they modulate neural and behavioral responses in both mice and humans. We propose that the brain has an identifiable set of states through which it wanders continuously in a nonrandom fashion, owing to the activity of both ascending modulatory and fast-acting corticocortical and subcortical-cortical neural pathways. These state variations provide the backdrop upon which the brain operates, and understanding them is critical to making progress in revealing the neural mechanisms underlying cognition and behavior.

A dual role of prestimulus spontaneous neural activity in visual object recognition.

Vision relies on both specific knowledge of visual attributes, such as object categories, and general brain states, such as those reflecting arousal. We hypothesized that these phenomena independently influence recognition of forthcoming stimuli through distinct processes reflected in spontaneous neural activity. Here, we recorded magnetoencephalographic (MEG) activity in participants (N = 24) who viewed images of objects presented at recognition threshold. Using multivariate analysis applied to sensor-level activity patterns recorded before stimulus presentation, we identified two neural processes influencing subsequent subjective recognition: a general process, which disregards stimulus category and correlates with pupil size, and a specific process, which facilitates category-specific recognition. The two processes are doubly-dissociable: the general process correlates with changes in criterion but not in sensitivity, whereas the specific process correlates with changes in sensitivity but not in criterion. Our findings reveal distinct mechanisms of how spontaneous neural activity influences perception and provide a framework to integrate previous findings.