BRAIN COMPLEXITY
& CONSCIOUSNESS
Lay Summary: The conventional wisdom that sleep is a global state, affecting the whole brain uniformly and simultaneously, was overturned by the discovery of local sleep, where individual neuronal populations were found to be asleep and the rest of the brain awake. However, due to the difficulty of monitoring local neuronal states in humans, our understanding of local sleep remains limited. Using simultaneous functional MRI (fMRI) and electroencephalography, we find that the oscillations of brain hemodynamic activity provide signatures of sleep at a local neuronal population level. We show that the fMRI signatures of sleep can be employed to monitor local neuronal states and investigate which brain regions are the first to fall asleep or wake up at wake-sleep transitions.
Abstract: Sleep can be distinguished from wake by changes in brain electrical activity, typically assessed using electroencephalography (EEG). The hallmark of non-rapid-eye-movement (NREM) sleep is the shift from high-frequency, low-amplitude wake EEG to low-frequency, high-amplitude sleep EEG dominated by spindles and slow waves. Here we identified signatures of sleep in brain hemodynamic activity, using simultaneous functional MRI (fMRI) and EEG. We found that, at the transition from wake to sleep, fMRI blood oxygen level–dependent (BOLD) activity evolved from a mixed-frequency pattern to one dominated by two distinct oscillations: a low-frequency (<0.1Hz) oscillation prominent in light sleep and correlated with the occurrence of spindles, and a high-frequency oscillation (>0.1Hz) prominent in deep sleep and correlated with the occurrence of slow waves. The two oscillations were both detectable across the brain but exhibited distinct spatiotemporal patterns. During the falling-asleep process, the low-frequency oscillation first appeared in the thalamus, then the posterior cortex, and lastly the frontal cortex, while the high-frequency oscillation first appeared in the midbrain, then the frontal cortex, and lastly the posterior cortex. During the waking-up process, both oscillations disappeared first from the thalamus, then the frontal cortex, and lastly the posterior cortex. The BOLD oscillations provide local signatures of spindle and slow wave activity. They may be employed to monitor the regional occurrence of sleep or wakefulness, track which regions are the first to fall asleep or wake up at the wake-sleep transitions, and investigate local homeostatic sleep processes.
Abstract: In this Correspondence article, we discussed the key challenges in linking human behaviour to brain structure. The field is challenged, in our opinion, by a lack of one-to-one mapping from MRI to brain structure and from brain structure to behaviour. Progress, therefore, relies largely on the ability to bridge the gap from MRI to brain structure and examine the multiple realizability of behaviour on brain structure. Recent developments along these lines, such as advanced MRI techniques and advanced statistical approaches, provide opportunities for a better conceptual understanding of how multifaceted human behaviour emerges from human brain structure.
Abstract: Structure shapes function. Understanding what is structurally special about the brain that allows it to generate consciousness remains a fundamental scientific challenge. Recently, advances in brain imaging techniques have made it possible to measure the structure of human brain, from the morphology of neurons and neuronal connections to the gross anatomy of brain regions, in-vivo and non-invasively. Using advanced brain imaging techniques, it was discovered that the structural diversity between neurons and the topology of neuronal connections, as opposed to the sheer number of neurons or neuronal connections, are key to consciousness. When the structural diversity is high and the connections follow a modular topology, neurons will become functionally differentiable and functionally integrable with one another. The high levels of differentiation and integration, in turn, enable the brain to produce the richest conscious experiences from the smallest number of neurons and neuronal connections. Consequently, across individuals, those with a smaller brain volume but a higher structural diversity tend to have richer conscious experiences than those with a larger brain volume but a lower structural diversity. Moreover, within individuals, a reduction in neuronal connections, if accompanied by an increase in structural diversity, will result in richer conscious experiences, and vice versa. These findings suggest that having a larger number of neurons and neuronal connections is not necessarily beneficial for consciousness; in contrast, an optimal brain architecture for consciousness is one where the richest conscious experiences are generated from the smallest number of neurons and neuronal connections, at the minimal cost of biological material, physical space, and metabolic energy.
Abstract: Sleep and wakefulness are traditionally considered as two mutually exclusive states with contrasting behavioural manifestations and complementary neurobiological functions. However, the discoveries of local sleep in global wakefulness and local wakefulness in global sleep have challenged this classical view and raised questions about the nature and functions of sleep. Here, we review the contributions from recent multimodal imaging studies of human sleep towards understanding the relationship between the nature and functions of sleep. Through simultaneous tracking of brain state and mapping of brain activity, these studies revealed that the sleeping brain can carry out covert cognitive processing that was thought to be wake-specific (wake-like function in the sleeping brain). Conversely, the awake brain can perform housekeeping functions through local sleep of neural populations (sleep-like function in the awake brain). We discuss how the blurred boundary between sleep and wakefulness highlights the need to radically rethink the definition of brain states, and how the recently discovered fMRI signatures of global and local sleep can help to address these outstanding questions.
Abstract: Understanding how people rate their confidence is critical for the characterization of a wide range of perceptual, memory, motor and cognitive processes. To enable the continued exploration of these processes, we created a large database of confidence studies spanning a broad set of paradigms, participant populations and fields of study. The data from each study are structured in a common, easy-to-use format that can be easily imported and analysed using multiple software packages. Each dataset is accompanied by an explanation regarding the nature of the collected data. At the time of publication, the Confidence Database (which is available at https://osf.io/s46pr/) contained 145 datasets with data from more than 8,700 participants and almost 4 million trials. The database will remain open for new submissions indefinitely and is expected to continue to grow. Here we show the usefulness of this large collection of datasets in four different analyses that provide precise estimations of several foundational confidence-related effects.
Abstract: The integration of inputs across the entire visual field into a single conscious experience is fundamental to human visual perception. This integrated nature of visual experience is illustrated by contextual illusions such as the tilt illusion, in which the perceived orientation of a central grating appears tilted away from its physical orientation, due to the modulation by a surrounding grating with a different orientation. Here we investigated the relative contribution of local, intra-hemispheric and global, inter-hemispheric integration mechanisms to perception of the tilt illusion. We used Dynamic Causal Modelling of fMRI signals to estimate effective connectivity in human early visual cortices (V1, V2, V3) during bilateral presentation of a tilt illusion stimulus. Our analysis revealed that neural responses associated with the tilt illusion were modulated by intra- rather than inter-hemispheric connectivity. Crucially, across participants, intra-hemispheric connectivity in V1 correlated with the magnitude of the tilt illusion, while no such correlation was observed for V1 inter-hemispheric connectivity, or V2, V3 connectivity. Moreover, when the illusion stimulus was presented unilaterally rather than bilaterally, the illusion magnitude did not change. Together our findings suggest that perception of the tilt illusion reflects an intra-hemispheric integration mechanism. This is in contrast to the existing literature, which suggests inter-hemispheric modulation of neural activity as early as V1. This discrepancy with our findings may reflect the diversity and complexity of integration mechanisms involved in visual processing and visual perception.
Abstract: The concept of prediction error - the difference between what occurred and was expected - is key to understanding the cognitive processes of human decision making. Expectations have to be learned so the concept of prediction error critically depends on context, specifically the temporal context of probabilistically related events and their changes across time (i.e. volatility). While past research suggests context differently affects some cognitive processes in East Asian and Western individuals, it is currently unknown whether this extends to computationally-grounded measures of learning and prediction error. Here we compared Chinese and British nationals in an associative learning task that quantifies behavioural effects of prediction error, and, through a hierarchical Bayesian learning model, also captures how individuals learn about probabilistic relationships and their volatility. For comparison, we also administered a psychophysical task, the tilt illusion, to assess cultural differences in susceptibility to spatial context. We found no cultural differences in the effect of spatial context on perception. In the domain of temporal context there was no effect of culture on sensitivity to prediction error, or learning about volatility, but some suggestion that Chinese individuals may learn more readily about probabilistic relationships.
Lay Summary: GABA, the primary inhibitory neurotransmitter in human visual system, varies substantially across individuals. This interindividual variability in GABA level is linked to interindividual differences in many aspects of visual perception. However, the widespread influence of GABA raises the question of whether interindividual variability in GABA reflects an overall variability in visual inhibition and has a general influence on visual perception or whether the GABA levels of different cortical regions have selective influence on perception of different visual features. Here we report a region- and feature-dependent influence of GABA level on human visual perception. Our findings suggest that GABA level of a cortical region selectively influences perception of visual features that are topographically mapped in this region through intraregional lateral connections.
Abstract: GABA is the primary inhibitory neurotransmitter in human brain. The level of GABA varies substantially across individuals, and this variability is associated with interindividual differences in visual perception. However, it remains unclear whether the association between GABA level and visual perception reflects a general influence of visual inhibition or whether the GABA levels of different cortical regions selectively influence perception of different visual features. To address this, we studied how the GABA levels of parietal and occipital cortices related to interindividual differences in size, orientation, and brightness perception. We used visual contextual illusion as a perceptual assay since the illusion dissociates perceptual content from stimulus content and the magnitude of the illusion reflects the effect of visual inhibition. Across individuals, we observed selective correlations between the level of GABA and the magnitude of contextual illusion. Specifically, parietal GABA level correlated with size illusion magnitude but not with orientation or brightness illusion magnitude; in contrast, occipital GABA level correlated with orientation illusion magnitude but not with size or brightness illusion magnitude. Our findings reveal a region- and feature-dependent influence of GABA level on human visual perception. Parietal and occipital cortices contain, respectively, topographic maps of size and orientation preference in which neural responses to stimulus sizes and stimulus orientations are modulated by intraregional lateral connections. We propose that these lateral connections may underlie the selective influence of GABA on visual perception.
Lay Summary: Given that visual space underlies visual perception, it is easy to take its topographical structure for granted. Indeed, most studies focus on object or feature perception that happens within visual space, without first considering the structure of visual space itself. Here we studied plasticity in the structure of visual space. We found that a local strengthening of lateral connections between retinotopically tuned visual cortical neurons, induced by synchronized, repetitive presentation of two-point stimuli, could lead to a contraction in perceived distance and a change in visual space structure. We propose lateral connections in the visual cortex as the mechanism that relates locations perceptually and shapes the structure of visual space.
Abstract: Visual space embodies all visual experiences, yet what determines the topographical structure of visual space remains unclear. Here we test a novel theoretical framework that proposes intrinsic lateral connections in the visual cortex as the mechanism underlying the structure of visual space. The framework suggests that the strength of lateral connections between neurons in the visual cortex shapes the experience of spatial relatedness between locations in the visual field. As such, an increase in lateral connection strength shall lead to an increase in perceived relatedness and a contraction in perceived distance. To test this framework through human psychophysics experiments, we used a Hebbian training protocol in which two-point stimuli were flashed in synchrony at separate locations in the visual field, to strengthen the lateral connections between two separate groups of neurons in the visual cortex. After training, participants experienced a contraction in perceived distance. Intriguingly, the perceptual contraction occurred not only between the two training locations that were linked directly by the changed connections, but also between the outward untrained locations that were linked indirectly through the changed connections. Moreover, the effect of training greatly decreased if the two training locations were too close together or too far apart and went beyond the extent of lateral connections. These findings suggest that a local change in the strength of lateral connections is sufficient to alter the topographical structure of visual space.
Abstract: Unconscious processing of subliminal visual information, as illustrated by the above-chance accuracy in discriminating invisible visual stimuli, is evident in both blindsight patients and healthy human observers. However, the dependence of such unconscious processing on stimulus properties remains unclear. Here we studied the impact of stimulus luminance and stimulus complexity on the extent of unconscious processing. A testing stimulus presented to one eye was rendered invisible by a masking stimulus presented to the other eye, and healthy human participants made a forced-choice discrimination of the stimulus identity followed by a report of the perceptual awareness. Without awareness of the stimulus existence, participants could nevertheless reach above-chance accuracy in discriminating the stimulus identity. Importantly, the discrimination accuracy for invisible stimuli increased with the stimulus luminance and decreased with the stimulus complexity. These findings suggested that the input signal strength and the input signal complexity can affect the extent of unconscious processing without altering the subjective awareness.
Lay Summary: Song et al. showed that large brains are not necessarily advantageous. Instead, the two dimensions, thickness and surface area, of human brain have opposite impacts on visual perception. A perceptually advantageous brain is a thinned one with enlarged surface area.
Abstract: The anatomy of cerebral cortex is characterized by two genetically independent variables, cortical thickness and cortical surface area, that jointly determine cortical volume. It remains unclear how cortical anatomy might influence neural response properties and whether such influences would have behavioral consequences. Here, we report that the thickness and the surface area of human early visual cortices exert opposite influences on neural population tuning with behavioral consequences for perceptual acuity. We found that visual cortical thickness correlated negatively with the sharpness of neural population tuning and the accuracy of perceptual discrimination. In contrast, visual cortical surface area correlated positively with neural population tuning sharpness and perceptual discrimination accuracy. Our findings reveal a central role for neural population tuning in linking visual cortical anatomy to visual perception and suggest that a perceptually advantageous visual cortex is a thinned one with an enlarged surface area.
Abstract: Executive control of attention regulates our thoughts, emotion and behavior. Individual differences in executive control are associated with task-related differences in brain activity. But it is unknown whether attentional differences depend on endogenous, resting-state brain activity and to what extent regional fluctuations and functional connectivity contribute to individual variations in executive control processing. Here, we explored the potential contribution of intrinsic brain activity to executive control by using resting-state functional magnetic resonance imaging. Using the amplitude of low-frequency fluctuations as an index of spontaneous brain activity, we found that the amplitude of low-frequency fluctuations in right precuneus and left superior frontal gyrus was significantly correlated with the efficiency of executive control processing. Crucially, the strengths of functional connectivity between right precuneus / left superior frontal gyrus and distributed brain regions, including left fusiform gyrus, right inferior frontal gyrus, left superior frontal gyrus and right precentral gyrus, were correlated with individual differences in executive performance. Together, the amplitude of low-frequency fluctuations and the functional connectivity accounted for 67% of the variability in behavioral performance. Our findings suggest that spontaneous brain activity may reflect or underpin executive control of attention. It will provide new insights into the origins of inter-individual variability in human executive control processing.
Abstract: Visual perception depends strongly on spatial context. A classic example is the tilt illusion where the perceived orientation of a central stimulus differs from its physical orientation when surrounded by tilted spatial contexts. Here we show that such contextual modulation of orientation perception exhibits trait-like interindividual diversity that correlates with interindividual differences in effective connectivity within human primary visual cortex. We found that the degree to which spatial contexts induced illusory orientation perception, namely, the magnitude of the tilt illusion, varied across healthy human adults in a trait-like fashion independent of stimulus size or contrast. Parallel to contextual modulation of orientation perception, the presence of spatial contexts affected effective connectivity within human primary visual cortex between peripheral and foveal representations that responded to spatial context and central stimulus, respectively. Importantly, this effective connectivity from peripheral to foveal primary visual cortex correlated with interindividual differences in the magnitude of the tilt illusion. Moreover, this correlation with illusion perception was observed for effective connectivity under tilted contextual stimulation but not for that under iso-oriented contextual stimulation, suggesting that it reflected the impact of orientation-dependent intra-areal connections. Our findings revealed an interindividual correlation between intra-areal connectivity within primary visual cortex and contextual influence on orientation perception. This correlation provides empirical evidence for theoretical proposals that intra-areal connections in early visual cortices are involved in contextual modulation of visual perception.
Abstract: The surface area of early visual cortices varies several fold across healthy adult humans and is genetically heritable. But the functional consequences of this anatomical variability are still largely unexplored. Here we show that interindividual variability in human visual cortical surface area reflects a tradeoff between sensitivity to visual details and susceptibility to visual context. Specifically, individuals with larger primary visual cortices can discriminate finer orientation differences, whereas individuals with smaller primary visual cortices experience stronger perceptual modulation by global orientation contexts. This anatomically correlated tradeoff between discrimination sensitivity and contextual modulation of orientation perception, however, does not generalize to contrast perception or luminance perception. Neural field simulations based on a scaling of intracortical circuits reproduce our empirical observations. Together our findings reveal a feature-specific shift in the scope of visual perception from context-oriented to detail-oriented with increased visual cortical surface area.
Abstract: The structural and functional architecture of the human brain is characterized by considerable variability, which has consequences for visual perception. However, the neurophysiological events mediating the relationship between interindividual differences in cortical surface area and visual perception have, until now, remained unknown. Here, we show that the retinotopically defined surface areas of central V1 and V2 are correlated with the peak frequency of visually induced oscillations in the gamma band, as measured with magnetoencephalography. Gamma-band oscillations are thought to play an important role in visual processing. We propose that individual differences in macroscopic gamma frequency may be attributed to interindividual variability in the microscopic architecture of visual cortex.
Lay Summary: Cerebral cortex has expanded over the course of hominid evolution, but not uniformly: anterior prefrontal cortex (aPFC), which is involved in problem-solving and complex planning, is especially enlarged in humans, whereas primary visual cortex (V1) has expanded less. The size of these and other brain areas varies greatly across individuals—up to threefold for V1. Most studies of interindividual differences have asked whether variations in the size of an area correlate with variation in performance on tasks associated with that area. Such correlations have been found. Song et al. asked whether expansion of one cortical area correlated with expansion of other areas in the same person. They found the opposite: V1 volume was inversely correlated with the volume of aPFC and of the gray matter of the entire brain. The volume of aPFC was positively correlated with whole-brain volume, however. Thus, the same volume correlations that occur across species also occur across individual humans.
Abstract: The human brain exhibits remarkable interindividual variability in cortical architecture. Despite extensive evidence for the behavioral consequences of such anatomical variability in individual cortical regions, it is unclear whether and how different cortical regions covary in morphology. Using a novel approach that combined noninvasive cortical functional mapping with whole-brain voxel-based morphometric analyses, we investigated the anatomical relationship between the functionally mapped visual cortices and other cortical structures in healthy humans. We found a striking anticorrelation between the gray matter volume of primary visual cortex and that of anterior prefrontal cortex, independent from individual differences in overall brain volume. Notably, this negative correlation formed along anatomically separate pathways, as the dorsal and ventral parts of primary visual cortex showed focal anticorrelation with the dorsolateral and ventromedial parts of anterior prefrontal cortex, respectively. Moreover, a similar inverse correlation was found between primary auditory cortex and anterior prefrontal cortex, but no anatomical relationship was observed between other visual cortices and anterior prefrontal cortex. Together, these findings indicate that an anatomical trade-off exists between primary sensory cortices and anterior prefrontal cortex as a possible general principle of human cortical organization. Our finding challenges the traditional view that the sizes of different brain areas simply scale with overall brain size and suggests the existence of shared genetic or developmental factors that contributes to the formation of anatomically and functionally distant cortical regions.
Abstract: The perception of even the most elementary features of the visual environment depends strongly on their spatial context. In the study reported here, we asked at what level of abstraction such effects require conscious processing of the context. We compared two visual illusions that alter subjective judgments of brightness: the simultaneous brightness contrast illusion, in which two circles of identical physical brightness appear different because of different surround luminance, and the Kanizsa triangle illusion, which occurs when the visual system extrapolates a surface without actual physical stimulation. We used a novel interocular masking technique that allowed us to selectively render only the context invisible. Simultaneous brightness contrast persisted even when the surround was masked from awareness. In contrast, participants did not experience illusory contours when the inducing context was masked. Our findings show that invisible context is resolvable by low-level processes involved in surface-brightness perception, but not by high-level processes that assign surface borders through perceptual completion.
Abstract: Human behavior depends on the ability to effectively introspect about our performance. For simple perceptual decisions, this introspective or metacognitive ability varies substantially across individuals and correlates with the structure of focal areas in prefrontal cortex. This raises the possibility that the ability to introspect about different perceptual decisions might be mediated by a common cognitive process. To test this hypothesis, we examined whether inter-individual differences in metacognitive ability were correlated across two different perceptual tasks where individuals made judgments about different and unrelated visual stimulus properties. We found that inter-individual differences were strongly correlated between the two tasks for metacognitive ability but not objective performance. Such stability of an individual's metacognitive ability across different perceptual tasks indicates a general mechanism supporting metacognition independent of the specific task.
Abstract: Visual perception is strongly determined by accumulated experience with the world, which has been shown for shape, color, and position perception, in the field of visuomotor learning, and in neural computation. In addition, visual perception is tuned to statistics of natural scenes. Such prior experience is modulated by neuronal top-down control the temporal properties of which had been subject to recent studies. Here, we deal with these temporal properties and address the question how early in time accumulated past experience can modulate visual perception. We performed stimulus discrimination experiments and compared a group of Chinese participants with a German control group. The perception of our briefly presented visual objects (targets) was disturbed by masking stimuli which appeared in close spatio-temporal proximity. These masking stimuli were either intact or scrambled Chinese characters and did not overlap with the targets. In contrast to German controls, Chinese participants show substantial performance differences for real versus scrambled Chinese characters if these masking stimuli were presented as early as less than 100 milliseconds after the onset of the target. For Chinese observers, it even occurred that meaningful masking stimuli enhanced target identification if they were shown at least 100 milliseconds after target onset while the same stimuli impaired recognition if presented in close temporal proximity to the target. The latter finding challenges interpretations of our data that solely rely on stimulus contours or geometric properties and emphasizes the impact of prior experience on the very early temporal dynamics of the visual system. Our findings demonstrate that prior experience which had been accumulated long before the experiments can modulate the time course of perception intriguingly early, namely already immediately after the perceptual onset of a visual event. This modulation cannot solely operate as a feedback in response to the visual event but is rather a permanent effect.
Abstract: The perceived size of objects not only depends on their physical size but also on the surroundings in which they appear. For example, an object surrounded by small items looks larger than a physically identical object surrounded by big items (Ebbinghaus illusion), and a physically identical but distant object looks larger than an object that appears closer in space (Ponzo illusion). Activity in human primary visual cortex (V1) reflects the perceived rather than the physical size of objects, indicating an involvement of V1 in illusory size perception. Here we investigate the role of eye-specific signals in two common size illusions in order to provide further information about the mechanisms underlying illusory size perception. We devised stimuli so that an object and its spatial context associated with illusory size perception could be presented together to one eye or separately to two eyes. We found that the Ponzo illusion had an equivalent magnitude whether the objects and contexts were presented to the same or different eyes, indicating that it may be largely mediated by binocular neurons. In contrast, the Ebbinghaus illusion became much weaker when objects and their contexts were presented to different eyes, indicating important contributions to the illusion from monocular neurons early in the visual pathway. Our findings show that two well-known size illusions - the Ponzo illusion and the Ebbinghaus illusion - are mediated by different neuronal populations, and suggest that the underlying neural mechanisms associated with illusory size perception differ and can be dependent on monocular channels in the early visual pathway.
Abstract: The surface area of human primary visual cortex (V1) varies substantially between individuals for unknown reasons. We found that this variability was strongly and negatively correlated with the magnitude of two common visual illusions, where two physically identical objects appear different in size as a result of their context. Because such illusions dissociate conscious perception from physical stimulation, our findings indicate that the surface area of V1 predicts variability in conscious experience.
Abstract: Visual perception is usually stable and accurate. However, when the two eyes are simultaneously presented with conflicting stimuli, perception falls into a sequence of spontaneous alternations, switching between one stimulus and the other every few seconds. Known as binocular rivalry, this visual illusion decouples subjective experience from physical stimulation and provides a unique opportunity to study the neural correlates of consciousness. The temporal properties of this alternating perception have been intensively investigated for decades, yet the relationship between two fundamental properties - the sequence of percepts and the duration of each percept - remains largely unexplored. Here we examine the relationship between the percept sequence and the percept duration by quantifying their sensitivity to the strength imbalance between two monocular stimuli. We found that the percept sequence is far more susceptible to the stimulus imbalance than does the percept duration. The percept sequence always begins with the stronger stimulus, even when the stimulus imbalance is too weak to cause a significant bias in the percept duration. Therefore, introducing a small stimulus imbalance affects the percept sequence, whereas increasing the imbalance affects the percept duration, but not vice versa. To investigate why the percept sequence is so vulnerable to the stimulus imbalance, we further measured the interval between the stimulus onset and the first percept, during which subjects experienced the fusion of two monocular stimuli. We found that this interval is dramatically shortened with increased stimulus imbalance. Our study shows that in binocular rivalry, the strength imblanace between monocular stimuli has a much greater impact on the percept sequence than on the percept duration, and increasing this imbalance can accelerate the process responsible for the percept sequence.