ABSTRACT
An ability to build structured mental maps of the world underpins our capacity to imagine relationships between objects that extend beyond experience. In rodents, such representations are supported by sequential place cell reactivations during rest, known as replay. Schizophrenia is proposed to reflect a compromise in structured mental representations, with animal models reporting abnormalities in hippocampal replay and associated ripple activity during rest. Here, utilizing magnetoencephalography (MEG), we tasked patients with schizophrenia and control participants to infer unobserved relationships between objects by reorganizing visual experiences containing these objects. During a post-task rest session, controls exhibited fast spontaneous neural reactivation of presented objects that replayed inferred relationships. Replay was coincident with increased ripple power in hippocampus. Patients showed both reduced replay and augmented ripple power relative to controls, convergent with findings in animal models. These abnormalities are linked to impairments in behavioral acquisition and subsequent neural representation of task structure.
Subject(s)
Learning , Neurons/pathology , Schizophrenia/pathology , Schizophrenia/physiopathology , Alpha Rhythm/physiology , Behavior , Brain Mapping , Female , Hippocampus/physiopathology , Humans , Magnetoencephalography , Male , Models, Biological , Task Performance and AnalysisABSTRACT
Alpha oscillations play a vital role in managing the brain's resources, inhibiting neural activity as a function of their phase and amplitude, and are changed in many brain disorders. Developing minimally invasive tools to modulate alpha activity and identifying the parameters that determine its response to exogenous modulators is essential for the implementation of focussed interventions. We introduce Alpha Closed-Loop Auditory Stimulation (αCLAS) as an EEG-based method to modulate and investigate these brain rhythms in humans with specificity and selectivity, using targeted auditory stimulation. Across a series of independent experiments, we demonstrate that αCLAS alters alpha power, frequency, and connectivity in a phase, amplitude, and topography-dependent manner. Using single-pulse-αCLAS, we show that the effects of auditory stimuli on alpha oscillations can be explained within the theoretical framework of oscillator theory and a phase-reset mechanism. Finally, we demonstrate the functional relevance of our approach by showing that αCLAS can interfere with sleep onset dynamics in a phase-dependent manner.
Subject(s)
Acoustic Stimulation , Alpha Rhythm , Electroencephalography , Humans , Acoustic Stimulation/methods , Male , Adult , Alpha Rhythm/physiology , Electroencephalography/methods , Female , Young Adult , Sleep/physiology , Brain/physiologyABSTRACT
Perception is a probabilistic process dependent on external stimulus properties and one's internal state. However, which internal states influence perception and via what mechanisms remain debated. We studied how spontaneous alpha-band activity (8-13â Hz) and pupil fluctuations impact visual detection and confidence across stimulus contrast levels (i.e., the contrast response function, CRF). In human subjects of both sexes, we found that low prestimulus alpha power induced an "additive" shift in the CRF, whereby stimuli were reported present more frequently at all contrast levels, including contrast of zero (i.e., false alarms). Conversely, prestimulus pupil size had a "multiplicative" effect on detection such that stimuli occurring during large pupil states (putatively corresponding to higher arousal) were perceived more frequently as contrast increased. Signal detection modeling reveals that alpha power changes detection criteria equally across the CRF but not detection sensitivity (d'), whereas pupil-linked arousal modulated sensitivity, particularly for higher contrasts. Interestingly, pupil size and alpha power were positively correlated, meaning that some of the effect of alpha on detection may be mediated by pupil fluctuations. However, pupil-independent alpha still induced an additive shift in the CRF corresponding to a criterion effect. Our data imply that low alpha boosts detection and confidence by an additive factor, rather than by a multiplicative scaling of contrast responses, a profile which captures the effect of pupil-linked arousal. We suggest that alpha power and arousal fluctuations have dissociable effects on behavior. Alpha reflects the baseline level of visual excitability, which can vary independent of arousal.
Subject(s)
Alpha Rhythm , Arousal , Pupil , Humans , Female , Male , Pupil/physiology , Arousal/physiology , Adult , Alpha Rhythm/physiology , Young Adult , Photic Stimulation/methods , Visual Perception/physiology , Contrast Sensitivity/physiologyABSTRACT
Attentional control over sensory processing has been linked to neural alpha oscillations and related inhibition of cerebral cortex. Despite the wide consensus on the functional relevance of alpha oscillations for attention, precise neural mechanisms of how alpha oscillations shape perception and how this top-down modulation is implemented in cortical networks remain unclear. Here, we tested the hypothesis that alpha oscillations in frontal eye fields (FEFs) are causally involved in the top-down regulation of visual processing in humans (male and female). We applied sham-controlled, intermittent transcranial alternating current stimulation (tACS) over bilateral FEF at either 10â Hz (alpha) or 40â Hz (gamma) to manipulate attentional preparation in a visual discrimination task. Under each stimulation condition, we measured psychometric functions for contrast perception and introduced a novel linear mixed modeling approach for statistical control of neurosensory side effects of the electric stimulation. tACS at alpha frequency reduced the slope of the psychometric function, resulting in improved subthreshold and impaired superthreshold contrast perception. Side effects on the psychometric functions were complex and showed large interindividual variability. Controlling for the impact of side effects on the psychometric parameters by using covariates in the linear mixed model analysis reduced this variability and strengthened the perceptual effect. We propose that alpha tACS over FEF mimicked a state of endogenous attention by strengthening a fronto-occipitoparietal network in the alpha band. We speculate that this network modulation enhanced phasic gating in occipitoparietal cortex leading to increased variability of single-trial psychometric thresholds, measurable as a reduction of psychometric slope.
Subject(s)
Alpha Rhythm , Attention , Transcranial Direct Current Stimulation , Visual Perception , Humans , Female , Male , Attention/physiology , Transcranial Direct Current Stimulation/methods , Adult , Visual Perception/physiology , Young Adult , Alpha Rhythm/physiology , Frontal Lobe/physiology , Photic Stimulation/methods , Visual Fields/physiologyABSTRACT
Research on selective attention has largely focused on the enhancement of behaviorally important information, with less focus on the suppression of distracting information. Enhancement and suppression can operate through a push-pull relationship attributable to competitive interactions among neural populations. There has been considerable debate, however, regarding (1) whether suppression can be voluntarily deployed, independent of enhancement, and (2) whether voluntary deployment of suppression is associated with neural processes occurring prior to the distractor onset. Here, we investigated the interplay between pre- and post-distractor neural processes, while male and female human subjects performed a visual search task with a cue that indicated the location of an upcoming distractor. We utilized two established EEG markers of suppression: the distractor positivity (PD) and alpha power (â¼8-15â Hz). The PD-a component of event-related potentials-has been linked with successful distractor suppression, and increased alpha power has been linked with attenuated sensory processing. Cueing the location of an upcoming distractor speeded responses and led to an earlier PD, consistent with earlier suppression due to strategic use of a spatial cue. In comparison, higher predistractor alpha power contralateral to distractors led to a later PD, consistent with later suppression. Lower alpha power contralateral to distractors instead led to distractor-related attentional capture. Lateralization of alpha power was not linked to the spatial cue. This observation, combined with differences in the timing of suppression-as indexed by earlier and later PD components-demonstrates that cue-related, voluntary suppression can occur separate from alpha-related gating of sensory processing.
Subject(s)
Alpha Rhythm , Attention , Cues , Humans , Male , Female , Attention/physiology , Alpha Rhythm/physiology , Adult , Young Adult , Electroencephalography , Photic Stimulation/methods , Reaction Time/physiology , Visual Perception/physiology , Evoked Potentials/physiologyABSTRACT
The intricate relationship between prestimulus alpha oscillations and visual contrast detection variability has been the focus of numerous studies. However, the causal impact of prestimulus alpha traveling waves on visual contrast detection remains largely unexplored. In our research, we sought to discern the causal link between prestimulus alpha traveling waves and visual contrast detection across different levels of mental fatigue. Using electroencephalography alongside a visual detection task with 30 healthy adults (13 females; 17 males), we identified a robust negative correlation between prestimulus alpha forward traveling waves (FTWs) and visual contrast threshold (VCT). Inspired by this correlation, we utilized 45/-45° phase-shifted transcranial alternating current stimulation (tACS) in a sham-controlled, double-blind, within-subject experiment with 33 healthy adults (23 females; 10 males) to directly modulate these alpha traveling waves. After the application of 45° phase-shifted tACS, we observed a substantial decrease in FTW and an increase in backward traveling waves, along with a concurrent increase in VCT, compared with the sham condition. These changes were particularly pronounced under a low fatigue state. The findings of state-dependent tACS effects reveal the potential causal role of prestimulus alpha traveling waves in visual contrast detection. Moreover, our study highlights the potential of 45/-45° phase-shifted tACS in cognitive modulation and therapeutic applications.
Subject(s)
Alpha Rhythm , Contrast Sensitivity , Transcranial Direct Current Stimulation , Humans , Female , Male , Adult , Alpha Rhythm/physiology , Transcranial Direct Current Stimulation/methods , Contrast Sensitivity/physiology , Young Adult , Double-Blind Method , Electroencephalography/methods , Photic Stimulation/methods , Visual Perception/physiology , Mental Fatigue/physiopathologyABSTRACT
Measures of intrinsic brain function at rest show promise as predictors of cognitive decline in humans, including EEG metrics such as individual α peak frequency (IAPF) and the aperiodic exponent, reflecting the strongest frequency of α oscillations and the relative balance of excitatory/inhibitory neural activity, respectively. Both IAPF and the aperiodic exponent decrease with age and have been associated with worse executive function and working memory. However, few studies have jointly examined their associations with cognitive function, and none have examined their association with longitudinal cognitive decline rather than cross-sectional impairment. In a preregistered secondary analysis of data from the longitudinal Midlife in the United States (MIDUS) study, we tested whether IAPF and aperiodic exponent measured at rest predict cognitive function (N = 235; age at EEG recording M = 55.10, SD = 10.71) over 10 years. The IAPF and the aperiodic exponent interacted to predict decline in overall cognitive ability, even after controlling for age, sex, education, and lag between data collection time points. Post hoc tests showed that "mismatched" IAPF and aperiodic exponents (e.g., higher exponent with lower IAPF) predicted greater cognitive decline compared to "matching" IAPF and aperiodic exponents (e.g., higher exponent with higher IAPF; lower IAPF with lower aperiodic exponent). These effects were largely driven by measures of executive function. Our findings provide the first evidence that IAPF and the aperiodic exponent are joint predictors of cognitive decline from midlife into old age and thus may offer a useful clinical tool for predicting cognitive risk in aging.
Subject(s)
Alpha Rhythm , Cognitive Dysfunction , Humans , Child , Cross-Sectional Studies , Cognition , Aging , Cognitive Dysfunction/diagnosis , ElectroencephalographyABSTRACT
Alpha is the strongest electrophysiological rhythm in awake humans at rest. Despite its predominance in the EEG signal, large variations can be observed in alpha properties during development, with an increase in alpha frequency over childhood and adulthood. Here, we tested the hypothesis that these changes in alpha rhythm are related to the maturation of visual white matter pathways. We capitalized on a large diffusion MRI (dMRI)-EEG dataset (dMRI n = 2,747, EEG n = 2,561) of children and adolescents of either sex (age range, 5-21 years old) and showed that maturation of the optic radiation specifically accounts for developmental changes of alpha frequency. Behavioral analyses also confirmed that variations of alpha frequency are related to maturational changes in visual perception. The present findings demonstrate the close link between developmental variations in white matter tissue properties, electrophysiological responses, and behavior.
Subject(s)
White Matter , Humans , Child , Adolescent , Child, Preschool , Young Adult , Adult , White Matter/diagnostic imaging , Alpha Rhythm , Diffusion Magnetic Resonance Imaging , Visual Perception , Visual Pathways , Brain/physiologyABSTRACT
The human hand possesses both consolidated motor skills and remarkable flexibility in adapting to ongoing task demands. However, the underlying mechanisms by which the brain balances stability and flexibility remain unknown. In the absence of external input or behavior, spontaneous (intrinsic) brain connectivity is thought to represent a prior of stored memories. In this study, we investigated how manual dexterity modulates spontaneous functional connectivity in the motor cortex during hand movement. Using magnetoencephalography, in 47 human participants (both sexes), we examined connectivity modulations in the α and ß frequency bands at rest and during two motor tasks (i.e., finger tapping or toe squeezing). The flexibility and stability of such modulations allowed us to identify two groups of participants with different levels of performance (high and low performers) on the nine-hole peg test, a test of manual dexterity. In the α band, participants with higher manual dexterity showed distributed decreases of connectivity, specifically in the motor cortex, increased segregation, and reduced nodal centrality. Participants with lower manual dexterity showed an opposite pattern. Notably, these patterns from the brain to behavior are mirrored by results from behavior to the brain. Indeed, when participants were divided using the median split of the dexterity score, we found the same connectivity patterns. In summary, this experiment shows that a long-term motor skill-manual dexterity-influences the way the motor systems respond during movements.
Subject(s)
Magnetoencephalography , Motor Cortex , Motor Skills , Humans , Male , Female , Adult , Motor Cortex/physiology , Motor Skills/physiology , Young Adult , Magnetoencephalography/methods , Alpha Rhythm/physiology , Hand/physiology , Psychomotor Performance/physiology , Movement/physiology , Neural Pathways/physiologyABSTRACT
Synchronous neural oscillations are strongly associated with a variety of perceptual, cognitive, and behavioural processes. It has been proposed that the role of the synchronous oscillations in these processes is to facilitate information transmission between brain areas, the 'communication through coherence,' or CTC hypothesis. The details of how this mechanism would work, however, and its causal status, are still unclear. Here we investigate computationally a proposed mechanism for selective attention that directly implicates the CTC as causal. The mechanism involves alpha band (about 10 Hz) oscillations, originating in the pulvinar nucleus of the thalamus, being sent to communicating cortical areas, organizing gamma (about 40 Hz) oscillations there, and thus facilitating phase coherence and communication between them. This is proposed to happen contingent on control signals sent from higher-level cortical areas to the thalamic reticular nucleus, which controls the alpha oscillations sent to cortex by the pulvinar. We studied the scope of this mechanism in parameter space, and limitations implied by this scope, using a computational implementation of our conceptual model. Our results indicate that, although the CTC-based mechanism can account for some effects of top-down and bottom-up attentional selection, its limitations indicate that an alternative mechanism, in which oscillatory coherence is caused by communication between brain areas rather than being a causal factor for it, might operate in addition to, or even instead of, the CTC mechanism.
Subject(s)
Attention , Models, Neurological , Attention/physiology , Humans , Computational Biology , Computer Simulation , Brain/physiology , Alpha Rhythm/physiology , Pulvinar/physiologyABSTRACT
While it is well known that mental fatigue impairs fine motor performance, the investigation into its neural basis remains scant. Here, we investigate the impact of mental fatigue on fine motor performance and explore its underlying neural network connectivity mechanisms. A total of 24 healthy male university students were recruited and randomly divided into two groups: a mental fatigue group (MF) and a control group (Control). Both groups completed 50 dart throws, while electroencephalography (EEG) data were collected. Following the Stroop intervention, participants in the MF group exhibited a decrease in Stroop task accuracy and throwing performance, and an increase in reaction time along with VAS and NASA scores. The EEG data during dart-throwing revealed that the network connectivity strength of theta oscillations in the frontal and left central regions was significantly higher in the MF group compared with the Control group, while the network connectivity strength of alpha oscillations in the left parietal region was significantly enhanced. The interregional connectivity within the theta and alpha rhythm bands, particularly in the frontal-central-parietal network connections, also showed a significant increase in the MF group. Mental fatigue impairs dart throwing performance and is accompanied by increased connectivity in alpha and theta.
Subject(s)
Electroencephalography , Parietal Lobe , Humans , Male , Reaction Time , Alpha Rhythm , Mental FatigueABSTRACT
Numerous studies on perceptual training exist, however, most have focused on the precision of temporal audiovisual perception, while fewer have concentrated on ability promotion for audiovisual integration (AVI). To investigate these issues, continuous 5-day audiovisual perceptual training was applied, during which electroencephalography was performed in response to auditory-only (A), visual-only (V) and audiovisual (AV) stimuli before and after training. The results showed that the perceptual sensitivity was greater for training group than for control group and was greater in the posttest than in the pretest. The response to the AV stimulus was significantly faster in the posttest than in the pretest for the older training group but was significantly greater for A and V stimuli for the younger training group. Electroencephalography analysis found higher P3 AVI amplitudes [AV-(A + V)] in the posttest than in the pretest for training group, which were subsequently reflected by an increased alpha (8-12 Hz) oscillatory response and strengthened global functional connectivity (weighted phase lag index). Furthermore, these facilitations were greater for older training groups than for younger training groups. These results confirm the age-related compensatory mechanism for AVI may be strengthened as audiovisual perceptual training progresses, providing an effective candidate for cognitive intervention in older adults.
Subject(s)
Acoustic Stimulation , Alpha Rhythm , Auditory Perception , Photic Stimulation , Visual Perception , Humans , Male , Female , Visual Perception/physiology , Auditory Perception/physiology , Aged , Alpha Rhythm/physiology , Photic Stimulation/methods , Electroencephalography , Middle Aged , Aging/physiology , Young Adult , Brain/physiology , AdultABSTRACT
The spectral composition of EEG provides important information on the function of the developing brain. For example, the frequency of the dominant rhythm, a salient features of EEG data, increases from infancy to adulthood. Changes of the dominant rhythm during infancy are yet to be fully characterized, in terms of their developmental trajectory and spectral characteristics. In this study, the development of dominant rhythm frequency was examined during a novel sustained attention task across 6-month-old (n = 39), 9-month-old (n = 30), and 12-month-old (n = 28) infants. During this task, computer-generated objects and faces floated down a computer screen for 10 s after a 5-second fixation cross. The peak frequency in the range between 5 and 9 Hz was calculated using center of gravity (CoG) and examined in response to faces and objects. Results indicated that peak frequency increased from 6 to 9 to 12 months of age in face and object conditions. We replicated the same result for the baseline. There was high reliability between the CoGs in the face, object, and baseline conditions across all channels. The developmental increase in CoG was more reliable than measures of mode frequency across different conditions. These findings suggest that CoG is a robust index of brain development across infancy.
Subject(s)
Attention , Brain , Infant , Humans , Reproducibility of Results , Brain/physiology , Attention/physiology , Electroencephalography , Alpha Rhythm/physiologyABSTRACT
States of consciousness are likely mediated by multiple parallel yet interacting cortico-subcortical recurrent networks. Although the mesocircuit model has implicated the pallidocortical circuit as one such network, this circuit has not been extensively evaluated to identify network-level electrophysiological changes related to loss of consciousness (LOC). We characterize changes in the mesocircuit in awake versus propofol-induced LOC in humans by directly simultaneously recording from sensorimotor cortices (S1/M1) and globus pallidus interna and externa (GPi/GPe) in 12 patients with Parkinson disease undergoing deep brain stimulator implantation. Propofol-induced LOC is associated with increases in local power up to 20 Hz in GPi, 35 Hz in GPe, and 100 Hz in S1/M1. LOC is likewise marked by increased pallidocortical alpha synchrony across all nodes, with increased alpha/low beta Granger causal (GC) flow from GPe to all other nodes. In contrast, LOC is associated with decreased network-wide beta coupling and beta GC from M1 to the rest of the network. Results implicate an important and possibly central role of GPe in mediating LOC-related increases in alpha power, supporting a significant role of the GPe in modulating cortico-subcortical circuits for consciousness. Simultaneous LOC-related suppression of beta synchrony highlights that distinct oscillatory frequencies act independently, conveying unique network activity.
Subject(s)
Alpha Rhythm , Globus Pallidus , Propofol , Unconsciousness , Humans , Propofol/pharmacology , Globus Pallidus/drug effects , Globus Pallidus/physiology , Male , Female , Middle Aged , Unconsciousness/chemically induced , Unconsciousness/physiopathology , Alpha Rhythm/drug effects , Alpha Rhythm/physiology , Aged , Parkinson Disease/physiopathology , Deep Brain Stimulation/methods , Anesthetics, Intravenous/pharmacology , Nerve Net/drug effects , Nerve Net/physiology , ElectroencephalographyABSTRACT
Increasingly, in the field of communication, education, and business, people are switching to video interaction, and interlocutors frequently complain that the perception of nonverbal information and concentration suffer. We investigated this issue by analyzing electroencephalogram (EEG) oscillations of the sensorimotor (mu rhythm) and visual (alpha rhythm) cortex of the brain in an experiment with action observation live and on video. The mu rhythm reflects the activity of the mirror neuron system, and the occipital alpha rhythm shows the level of visual attention. We used 32-channel EEG recorded during live and video action observation in 83 healthy volunteers. The ICA method was used for selecting the mu- and alpha-components; the Fourier Transform was used to calculate the suppression index relative to the baseline (stationary demonstrator) of the rhythms. The main range of the mu rhythm was indeed sensitive to social movement and was highly dependent on the conditions of interaction-live or video. The upper mu-range appeared to be less sensitive to the conditions, but more sensitive to different movements. The alpha rhythm did not depend on the type of movement; however, a live performance initially caused a stronger concentration of visual attention. Thus, subtle social and nonverbal perceptions may suffer in remote video interactions.
Subject(s)
Electroencephalography , Humans , Male , Female , Adult , Young Adult , Electroencephalography/methods , Attention/physiology , Visual Cortex/physiology , Alpha Rhythm/physiology , Sensorimotor Cortex/physiology , Visual Perception/physiology , Photic Stimulation/methodsABSTRACT
One of the early markers of minimal hepatic encephalopathy (MHE) is the disruption of alpha rhythm observed in electroencephalogram (EEG) signals. However, the underlying mechanisms responsible for this occurrence remain poorly understood. To address this gap, we develop a novel biophysical model MHE-AWD-NCM, encompassing the communication dynamics between a cortical neuron population (CNP) and an astrocyte population (AP), aimed at investigating the relationship between alpha wave disturbance (AWD) and mechanistical principles, specifically concerning astrocyte-neuronal communication in the context of MHE. In addition, we introduce the concepts of peak power density and peak frequency within the alpha band as quantitative measures of AWD. Our model faithfully reproduces the characteristic EEG phenomenology during MHE and shows how impairments of communication between CNP and AP could promote AWD. The results suggest that the disruptions in feedback neurotransmission from AP to CNP, along with the inhibition of GABA uptake by AP from the extracellular space, contribute to the observed AWD. Moreover, we found that the variation of external excitatory stimuli on CNP may play a key role in AWD in MHE. Finally, the sensitivity analysis is also performed to assess the relative significance of above factors in influencing AWD. Our findings align with the physiological observations and provide a more comprehensive understanding of the complex interplay of astrocyte-neuronal communication that underlies the AWD observed in MHE, which potentially may help to explore the targeted therapeutic interventions for the early stage of hepatic encephalopathy.
Subject(s)
Hepatic Encephalopathy , Humans , Hepatic Encephalopathy/drug therapy , Alpha Rhythm , Electroencephalography , NeuronsABSTRACT
Alpha rhythmic activity is often suggested to exert an inhibitory influence on information processing. However, relatively little is known about how reported alpha-related effects are influenced by a potential confounding element of the neural signal, power-law scaling. In the current study, we systematically examine the effect of accounting for 1/f activity on the relation between prestimulus alpha power and human behavior during both auditory and visual detection (N = 27; 19 female, 6 male, 2 nonbinary). The results suggest that, at least in the scalp-recorded EEG signal, the difference in alpha power often reported before visual hits versus misses is probably best thought of as a combination of narrowband alpha and broadband shifts. That is, changes in broadband parameters (exponent and offset of 1/f-like activity) also appear to be strong predictors of the subsequent awareness of visual stimuli. Neither changes in posterior alpha power nor changes in 1/f-like activity reliably predicted detection of auditory stimuli. These results appear consistent with suggestions that broadband changes in the scalp-recorded EEG signal may account for a portion of prior results linking alpha band dynamics to visuospatial attention and behavior, and suggest that systematic re-examination of existing data may be warranted.Significance Statement Fluctuations in alpha band (â¼8-12 Hz) activity systematically follow the allocation of attention across space and sensory modality. Increases in alpha amplitude, which often precede failures to report awareness of threshold visual stimuli, are suggested to exert an inhibitory influence on information processing. However, fluctuations in alpha activity are often confounded with changes in the broadband 1/f-like pattern of the neural signal. When both factors are considered, we find that changes in broadband activity are as effective as narrowband alpha activity as predictors of subsequent visual detection. These results are consistent with emerging understanding of the potential functional importance of broadband changes in the neural signal and may have significant consequences for our understanding of alpha rhythmic activity.
Subject(s)
Alpha Rhythm , Cognition , Humans , Female , Male , ElectroencephalographyABSTRACT
Across species, neurons track time over the course of seconds to minutes, which may feed the sense of time passing. Here, we asked whether neural signatures of time-tracking could be found in humans. Participants stayed quietly awake for a few minutes while being recorded with magnetoencephalography (MEG). They were unaware they would be asked how long the recording lasted (retrospective time) or instructed beforehand to estimate how long it will last (prospective timing). At rest, rhythmic brain activity is nonstationary and displays bursts of activity in the alpha range (α: 7-14 Hz). When participants were not instructed to attend to time, the relative duration of α bursts linearly predicted individuals' retrospective estimates of how long their quiet wakefulness lasted. The relative duration of α bursts was a better predictor than α power or burst amplitude. No other rhythmic or arrhythmic activity predicted retrospective duration. However, when participants timed prospectively, the relative duration of α bursts failed to predict their duration estimates. Consistent with this, the amount of α bursts was discriminant between prospective and retrospective timing. Last, with a control experiment, we demonstrate that the relation between α bursts and retrospective time is preserved even when participants are engaged in a visual counting task. Thus, at the time scale of minutes, we report that the relative time of spontaneous α burstiness predicts conscious retrospective time. We conclude that in the absence of overt attention to time, α bursts embody discrete states of awareness constitutive of episodic timing.SIGNIFICANCE STATEMENT The feeling that time passes is a core component of consciousness and episodic memory. A century ago, brain rhythms called "α" were hypothesized to embody an internal clock. However, rhythmic brain activity is nonstationary and displays on-and-off oscillatory bursts, which would serve irregular ticks to the hypothetical clock. Here, we discovered that in a given lapse of time, the relative bursting time of α rhythms is a good indicator of how much time an individual will report to have elapsed. Remarkably, this relation only holds true when the individual does not attend to time and vanishes when attending to it. Our observations suggest that at the scale of minutes, α brain activity tracks episodic time.
Subject(s)
Alpha Rhythm , Brain , Humans , Retrospective Studies , Alpha Rhythm/physiology , Magnetoencephalography , Neurons/physiologyABSTRACT
Hierarchical predictive coding networks are a general model of sensory processing in the brain. Under neural delays, these networks have been suggested to naturally generate oscillatory activity in approximately the α frequency range (â¼8-12 Hz). This suggests that α oscillations, a prominent feature of EEG recordings, may be a spectral "fingerprint" of predictive sensory processing. Here, we probed this possibility by investigating whether oscillations over the visual cortex predictively encode visual information. Specifically, we examined whether their power carries information about the position of a moving stimulus, in a temporally predictive fashion. In two experiments (N = 32, 18 female; N = 34, 17 female), participants viewed an apparent-motion stimulus moving along a circular path while EEG was recorded. To investigate the encoding of stimulus-position information, we developed a method of deriving probabilistic spatial maps from oscillatory power estimates. With this method, we demonstrate that it is possible to reconstruct the trajectory of a moving stimulus from α/low-ß oscillations, tracking its position even across unexpected motion reversals. We also show that future position representations are activated in the absence of direct visual input, demonstrating that temporally predictive mechanisms manifest in α/ß band oscillations. In a second experiment, we replicate these findings and show that the encoding of information in this range is not driven by visual entrainment. By demonstrating that occipital α/ß oscillations carry stimulus-related information, in a temporally predictive fashion, we provide empirical evidence of these rhythms as a spectral "fingerprint" of hierarchical predictive processing in the human visual system.SIGNIFICANCE STATEMENT "Hierarchical predictive coding" is a general model of sensory information processing in the brain. When in silico predictive coding models are constrained by neural transmission delays, their activity naturally oscillates in roughly the α range (â¼8-12 Hz). Using time-resolved EEG decoding, we show that neural rhythms in this approximate range (α/low-ß) over the human visual cortex predictively encode the position of a moving stimulus. From the amplitude of these oscillations, we are able to reconstruct the stimulus' trajectory, revealing signatures of temporally predictive processing. This provides direct neural evidence linking occipital α/ß rhythms to predictive visual processing, supporting the emerging view of such oscillations as a potential spectral "fingerprint" of hierarchical predictive processing in the human visual system.
Subject(s)
Alpha Rhythm , Visual Cortex , Humans , Female , Visual Perception , Brain , Sensation , ElectroencephalographyABSTRACT
Behavioral consequences and neural underpinnings of visuospatial attention have long been investigated. Classical studies using the Posner paradigm have found that visual perception systematically benefits from the use of a spatially informative cue pointing to the to-be-attended spatial location, compared with a noninformative cue. Lateralized α amplitude modulation during visuospatial attention shifts has been suggested to account for such perceptual gain. However, recent studies on spontaneous fluctuations of prestimulus α amplitude have challenged this notion. These studies showed that spontaneous fluctuations of prestimulus α amplitude were associated with the subjective appreciation of stimulus occurrence, while objective accuracy was instead best predicted by the frequency of α oscillations, with faster prestimulus α frequency accounting for better perceptual performance. Here, in male and female humans, by using an informative cue in anticipation of lateralized stimulus presentation, we found that the predictive cue not only modulates preparatory α amplitude but also α frequency in a retinotopic manner. Behaviorally, the cue significantly impacted subjective performance measures (metacognitive abilities [meta-d']) and objective performance gain (d'). Importantly, α amplitude directly accounted for confidence levels, with ipsilateral synchronization and contralateral desynchronization coding for high-confidence responses. Crucially, the contralateral α amplitude selectively predicted interindividual differences in metacognitive abilities (meta-d'), thus anticipating decision strategy and not perceptual sensitivity, probably via excitability modulations. Instead, higher perceptual accuracy both within and across participants (d') was associated with faster contralateral α frequency, likely by implementing higher sampling at the attended location. These findings provide critical new insights into the neural mechanisms of attention control and its perceptual consequences.SIGNIFICANCE STATEMENT Prior knowledge serves the anticipation of sensory input to reduce sensory ambiguity. The growing interest in the neural mechanisms governing the integration of sensory input into our internal representations has highlighted a pivotal role of brain oscillations. Here we show that distinct but interacting oscillatory mechanisms are engaged during attentional deployment: one relying on α amplitude modulations and reflecting internal decision processes, associated with subjective perceptual experience and metacognitive abilities; the other relying on α frequency modulations and enabling mechanistic sampling of the sensory input at the attended location to influence objective performance. These insights are crucial for understanding how we reduce sensory ambiguity to maximize the efficiency of our conscious experience, but also in interpreting the mechanisms of atypical perceptual experiences.