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Following the discovery of context-dependent synchronization of oscillatory neuronal responses in the visual system, the role of neural synchrony in cortical networks has been expanded to provide a general mechanism for the coordination of distributed neural activity patterns. In the current paper, we present an update of the status of this hypothesis through summarizing recent results from our laboratory that suggest important new insights regarding the mechanisms, function and relevance of this phenomenon. In the first part, we present recent results derived from animal experiments and mathematical simulations that provide novel explanations and mechanisms for zero and nero-zero phase lag synchronization. In the second part, we shall discuss the role of neural synchrony for expectancy during perceptual organization and its role in conscious experience. This will be followed by evidence that indicates that in addition to supporting conscious cognition, neural synchrony is abnormal in major brain disorders, such as schizophrenia and autism spectrum disorders. We conclude this paper with suggestions for further research as well as with critical issues that need to be addressed in future studies.
Correction to: Nature Communications https://doi.org/10.1038/s41467-017-01045-x, published online 31 October 2017
It has come to our attention that we did not specify whether the stimulation magnitudes we report in this Article are peak amplitudes or peak-to-peak. All references to intensity given in mA in the manuscript refer to peak-to-peak amplitudes, except in Fig. 2, where the model is calibrated to 1 mA peak amplitude, as stated. In the original version of the paper we incorrectly calibrated the computational models to 1 mA peak-to-peak, rather than 1 mA peak amplitude. This means that we divided by a value twice as large as we should have. The correct estimated fields are therefore twice as large as shown in the original Fig. 2 and Supplementary Fig. 11. The corrected figures are now properly calibrated to 1mA peak amplitude. Furthermore, the sentence in the first paragraph of the Results section ‘Intensity ranged from 0.5 to 2.5 mA (current density 0.125–0.625 mA mA/cm2), which is stronger than in previous reports’, should have read ‘Intensity ranged from 0.5 to 2.5 mA peak to peak (peak current density 0.0625–0.3125 mA/cm2), which is stronger than in previous reports.’ These errors do not affect any of the Article’s conclusions. Correct versions of Fig. 2 and Supplementary Fig. 11 are presented below as Figs. 1, 2.
During meditation, practitioners are required to center their attention on a specific object for extended periods of time. When their thoughts get diverted, they learn to quickly disengage from the distracter. We hypothesized that learning to respond to the dual demand of engaging attention on specific objects and disengaging quickly from distracters enhances the efficiency by which meditation practitioners can allocate attention. We tested this hypothesis in a global-to-local task while measuring electroencephalographic activity from a group of eight highly trained Buddhist monks and nuns and a group of eight age and education matched controls with no previous meditation experience. Specifically, we investigated the effect of attentional training on the global precedence effect, i.e., faster detection of targets on a global than on a local level. We expected to find a reduced global precedence effect in meditation practitioners but not in controls, reflecting that meditators can more quickly disengage their attention from the dominant global level. Analysis of reaction times confirmed this prediction. To investigate the underlying changes in brain activity and their time course, we analyzed event-related potentials. Meditators showed an enhanced ability to select the respective target level, as reflected by enhanced processing of target level information. In contrast with control group, which showed a local target selection effect only in the P1 and a global target selection effect in the P3 component, meditators showed effects of local information processing in the P1, N2, and P3 and of global processing for the N1, N2, and P3. Thus, meditators seem to display enhanced depth of processing. In addition, meditation altered the uptake of information such that meditators selected target level information earlier in the processing sequence than controls. In a longitudinal experiment, we could replicate the behavioral effects, suggesting that meditation modulates attention already after a 4-day meditation retreat. Together, these results suggest that practicing meditation enhances the speed with which attention can be allocated and relocated, thus increasing the depth of information processing and reducing response latency.
Perception is an active inferential process in which prior knowledge is combined with sensory input, the result of which determines the contents of awareness. Accordingly, previous experience is known to help the brain “decide” what to perceive. However, a critical aspect that has not been addressed is that previous experience can exert 2 opposing effects on perception: An attractive effect, sensitizing the brain to perceive the same again (hysteresis), or a repulsive effect, making it more likely to perceive something else (adaptation). We used functional magnetic resonance imaging and modeling to elucidate how the brain entertains these 2 opposing processes, and what determines the direction of such experience-dependent perceptual effects. We found that although affecting our perception concurrently, hysteresis and adaptation map into distinct cortical networks: a widespread network of higher-order visual and fronto-parietal areas was involved in perceptual stabilization, while adaptation was confined to early visual areas. This areal and hierarchical segregation may explain how the brain maintains the balance between exploiting redundancies and staying sensitive to new information. We provide a Bayesian model that accounts for the coexistence of hysteresis and adaptation by separating their causes into 2 distinct terms: Hysteresis alters the prior, whereas adaptation changes the sensory evidence (the likelihood function).
A key hallmark of visual perceptual awareness is robustness to instabilities arising from unnoticeable eye and eyelid movements. In previous human intracranial (iEEG) work (Golan et al., 2016) we found that excitatory broadband high-frequency activity transients, driven by eye blinks, are suppressed in higher-level but not early visual cortex. Here, we utilized the broad anatomical coverage of iEEG recordings in 12 eye-tracked neurosurgical patients to test whether a similar stabilizing mechanism operates following small saccades. We compared saccades (1.3°−3.7°) initiated during inspection of large individual visual objects with similarly-sized external stimulus displacements. Early visual cortex sites responded with positive transients to both conditions. In contrast, in both dorsal and ventral higher-level sites the response to saccades (but not to external displacements) was suppressed. These findings indicate that early visual cortex is highly unstable compared to higher-level visual regions which apparently constitute the main target of stabilizing extra-retinal oculomotor influences.
In 1957, Craig Mooney published a set of human face stimuli to study perceptual closure: the formation of a coherent percept on the basis of minimal visual information. Images of this type, now known as “Mooney faces”, are widely used in cognitive psychology and neuroscience because they offer a means of inducing variable perception with constant visuo-spatial characteristics (they are often not perceived as faces if viewed upside down). Mooney’s original set of 40 stimuli has been employed in several studies. However, it is often necessary to use a much larger stimulus set. We created a new set of over 500 Mooney faces and tested them on a cohort of human observers. We present the results of our tests here, and make the stimuli freely available via the internet. Our test results can be used to select subsets of the stimuli that are most suited for a given experimental purpose.
Solving the problem of consciousness remains one of the biggest challenges in modern science. One key step towards understanding consciousness is to empirically narrow down neural processes associated with the subjective experience of a particular content. To unravel these neural correlates of consciousness (NCC) a common scientific strategy is to compare perceptual conditions in which consciousness of a particular content is present with those in which it is absent, and to determine differences in measures of brain activity (the so called "contrastive analysis"). However, this comparison appears not to reveal exclusively the NCC, as the NCC proper can be confounded with prerequisites for and consequences of conscious processing of the particular content. This implies that previous results cannot be unequivocally interpreted as reflecting the neural correlates of conscious experience. Here we review evidence supporting this conjecture and suggest experimental strategies to untangle the NCC from the prerequisites and consequences of conscious experience in order to further develop the otherwise valid and valuable contrastive methodology.
Transcranial electrical stimulation has widespread clinical and research applications, yet its effect on ongoing neural activity in humans is not well established. Previous reports argue that transcranial alternating current stimulation (tACS) can entrain and enhance neural rhythms related to memory, but the evidence from non-invasive recordings has remained inconclusive. Here, we measure endogenous spindle and theta activity intracranially in humans during low-frequency tACS and find no stable entrainment of spindle power during non-REM sleep, nor of theta power during resting wakefulness. As positive controls, we find robust entrainment of spindle activity to endogenous slow-wave activity in 66% of electrodes as well as entrainment to rhythmic noise-burst acoustic stimulation in 14% of electrodes. We conclude that low-frequency tACS at common stimulation intensities neither acutely modulates spindle activity during sleep nor theta activity during waking rest, likely because of the attenuated electrical fields reaching the cortical surface.
Individual differences in perception are widespread. Considering inter-individual variability, synesthetes experience stable additional sensations; schizophrenia patients suffer perceptual deficits in, eg, perceptual organization (alongside hallucinations and delusions). Is there a unifying principle explaining inter-individual variability in perception? There is good reason to believe perceptual experience results from inferential processes whereby sensory evidence is weighted by prior knowledge about the world. Perceptual variability may result from different precision weighting of sensory evidence and prior knowledge. We tested this hypothesis by comparing visibility thresholds in a perceptual hysteresis task across medicated schizophrenia patients (N = 20), synesthetes (N = 20), and controls (N = 26). Participants rated the subjective visibility of stimuli embedded in noise while we parametrically manipulated the availability of sensory evidence. Additionally, precise long-term priors in synesthetes were leveraged by presenting either synesthesia-inducing or neutral stimuli. Schizophrenia patients showed increased visibility thresholds, consistent with overreliance on sensory evidence. In contrast, synesthetes exhibited lowered thresholds exclusively for synesthesia-inducing stimuli suggesting high-precision long-term priors. Additionally, in both synesthetes and schizophrenia patients explicit, short-term priors—introduced during the hysteresis experiment—lowered thresholds but did not normalize perception. Our results imply that perceptual variability might result from differences in the precision afforded to prior beliefs and sensory evidence, respectively.
Individual differences in perception are widespread. Considering inter-individual variability, synesthetes experience stable additional sensations; schizophrenia patients suffer perceptual deficits in e.g. perceptual organization (alongside hallucinations and delusions). Is there a unifying principle explaining inter-individual variability in perception? There is good reason to believe perceptual experience results from inferential processes whereby sensory evidence is weighted by prior knowledge about the world. Different perceptual phenotypes may result from different precision weighting of sensory evidence and prior knowledge. We tested this hypothesis by comparing visibility thresholds in a perceptual hysteresis task across medicated schizophrenia patients, synesthetes, and controls. Participants rated the subjective visibility of stimuli embedded in noise while we parametrically manipulated the availability of sensory evidence. Additionally, precise long-term priors in synesthetes were leveraged by presenting either synesthesia-inducing or neutral stimuli. Schizophrenia patients showed increased visibility thresholds, consistent with overreliance on sensory evidence. In contrast, synesthetes exhibited lowered thresholds exclusively for synesthesia-inducing stimuli suggesting high-precision long-term priors. Additionally, in both synesthetes and schizophrenia patients explicit, short-term priors – introduced during the hysteresis experiment – lowered thresholds but did not normalize perception. Our results imply that distinct perceptual phenotypes might result from differences in the precision afforded to prior beliefs and sensory evidence, respectively.
