Human perceptual and metacognitive decision-making rely on distinct brain networks.

Perceptual decisions depend on the ability to exploit available sensory information in order to select the most adaptive option from a set of alternatives. Such decisions depend on the perceptual sensitivity of the organism, which is generally accompanied by a corresponding level of certainty about the choice made. Here, by use of corticocortical paired associative transcranial magnetic stimulation protocol (ccPAS) aimed at inducing plastic changes, we shaped perceptual sensitivity and metacognitive ability in a motion discrimination task depending on the targeted network, demonstrating their functional dissociation. Neurostimulation aimed at boosting V5/MT+-to-V1/V2 back-projections enhanced motion sensitivity without impacting metacognition, whereas boosting IPS/LIP-to-V1/V2 back-projections increased metacognitive efficiency without impacting motion sensitivity. This double-dissociation provides causal evidence of distinct networks for perceptual sensitivity and metacognitive ability in humans.

Two Oscillatory Correlates of Attention Control in the Alpha-Band with Distinct Consequences on Perceptual Gain and Metacognition.

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.

Alpha-Band Frequency and Temporal Windows in Perception: A Review and Living Meta-analysis of 27 Experiments (and Counting).

Temporal windows in perception refer to windows of time within which distinct stimuli interact to influence perception. A simple example is two temporally proximal stimuli fusing into a single percept. It has long been hypothesized that the human alpha rhythm (an 8- to 13-Hz neural oscillation maximal over posterior cortex) is linked to temporal windows, with higher frequencies corresponding to shorter windows and finer-grained temporal resolution. This hypothesis has garnered support from studies demonstrating a correlation between individual differences in alpha-band frequency (IAF) and behavioral measures of temporal processing. However, nonsignificant effects have also been reported. Here, we review and meta-analyze 27 experiments correlating IAF with measures of visual and audiovisual temporal processing. Our results estimate the true correlation in the population to be between .39 and .53, a medium-to-large effect. The effect held when considering visual or audiovisual experiments separately, when examining different IAF estimation protocols (i.e., eyes open and eyes closed), and when using analysis choices that favor a null result. Our review shows that (1) effects have been internally and independently replicated, (2) several positive effects are based on larger sample sizes than the null effects, and (3) many reported null effects are actually in the direction predicted by the hypothesis. A free interactive web app was developed to allow users to replicate our meta-analysis and change or update the study selection at will, making this a "living" meta-analysis (randfxmeta.streamlit.app). We discuss possible factors underlying null reports, design recommendations, and open questions for future research.

Individual Alpha Frequency Contributes to the Precision of Human Visual Processing.

Brain oscillatory activity within the alpha band has been associated with a wide range of processes encompassing perception, memory, decision-making, and overall cognitive functioning. Individual alpha frequency (IAF) is a specific parameter accounting for the mean velocity of the alpha cycling activity, conventionally ranging between ∼7 and ∼13 Hz. One influential hypothesis has proposed a fundamental role of this cycling activity in the segmentation of sensory input and in the regulation of the speed of sensory processing, with faster alpha oscillations resulting in greater temporal resolution and more refined perceptual experience. However, although several recent theoretical and empirical studies would support this account, contradictory evidence suggests caution and more systematic approaches in the assessment and interpretation of this hypothesis. For example, it remains to be explored to what degree IAF shapes perceptual outcomes. In the present study, we investigated whether inter-individual differences in bias-free visual contrast detection threshold in a large sample of individuals in the general population (n = 122) could be explained by inter-individual differences in alpha pace. Our results show that the contrast needed to correctly identify target stimuli (individual perceptual threshold) is associated with alpha peak frequency (not amplitude). Specifically, individuals who require reduced contrast show higher IAF than individuals requiring higher contrasts. This suggests that inter-individual differences in alpha frequency contribute to performance variability in low-level perceptual tasks, supporting the hypothesis that IAF underlies a fundamental temporal sampling mechanism that shapes visual objective performance, with higher frequencies promoting enhanced sensory evidence per time unit.

Alpha-band Brain Dynamics and Temporal Processing: An Introduction to the Special Focus.

For decades, the intriguing connection between the human alpha rhythm (an 8- to 13-Hz oscillation maximal over posterior cortex) and temporal processes in perception has furnished a rich landscape of proposals. The past decade, however, has seen a surge in interest in the topic, bringing new theoretical, analytic, and methodological developments alongside fresh controversies. This Special Focus on alpha-band dynamics and temporal processing provides an up-to-date snapshot of the playing field, with contributions from leading researchers in the field spanning original perspectives, new evidence, comprehensive reviews and meta-analyses, as well as discussion of ongoing controversies and paths forward. We hope that the perspectives captured here will help catalyze future research and shape the pathways toward a theoretically grounded and mechanistic account of the link between alpha dynamics and temporal properties of perception.

The independence and predictivity of resting pain-free slow alpha frequency as a biomarker of pain: A reply to Mazaheri et al.

In response to Mazaheri et al.'s critique, we revisited our study (Valentini et al., 2022) on the relationship between peak alpha frequency (PAF) and pain. Their commentary prompted us to reassess our data to address the independence between slow and slowing alpha brain oscillations, as well as the predictivity of slow alpha oscillations in pain perception. Bayesian correlation analyses revealed mixed support for independence. Investigating predictivity, we found inconsistent associations between pre-PAF and unpleasantness ratings. We critically reflected on methodological and theoretical issues on the path to PAF validation as a pain biomarker. We emphasized the need for diversified methodology and analytical approaches as well as robust findings across research groups.

Hierarchical psychophysiological pathways subtend perceptual asymmetries in Neglect.

Stroke patients with left Hemispatial Neglect (LHN) show deficits in perceiving left contralesional stimuli with biased visuospatial perception towards the right hemifield. However, very little is known about the functional organization of the visuospatial perceptual neural network and how this can account for the profound reorganization of space representation in LHN. In the present work, we aimed at (1) identifying EEG measures that discriminate LHN patients against controls and (2) devise a causative neurophysiological model between the discriminative EEG measures. To these aims, EEG was recorded during exposure to lateralized visual stimuli which allowed for pre-and post-stimulus activity investigation across three groups: LHN patients, lesioned controls, and healthy individuals. Moreover, all participants performed a standard behavioral test assessing the perceptual asymmetry index in detecting lateralized stimuli. The between-groups discriminative EEG patterns were entered into a Structural Equation Model for the identification of causative hierarchical associations (i.e., pathways) between EEG measures and the perceptual asymmetry index. The model identified two pathways. A first pathway showed that the combined contribution of pre-stimulus frontoparietal connectivity and individual-alpha-frequency predicts post-stimulus processing, as measured by visual-evoked N100, which, in turn, predicts the perceptual asymmetry index. A second pathway directly links the inter-hemispheric distribution of alpha-amplitude with the perceptual asymmetry index. The two pathways can collectively explain 83.1% of the variance in the perceptual asymmetry index. Using causative modeling, the present study identified how psychophysiological correlates of visuospatial perception are organized and predict the degree of behavioral asymmetry in LHN patients and controls.

From touch to tingles: Assessing ASMR triggers and their consistency over time with the ASMR Trigger Checklist (ATC).

Autonomous Sensory Meridian Response (ASMR) is a term describing a complex sensory-perceptual phenomena characterised by relaxing and pleasurable scalp tingling sensations. A central defining feature of ASMR is that the sensation is elicited by a core set of stimuli or so-called "triggers". The idea that ASMR is triggered by specific external stimuli is frequently invoked in conceptual definitions of ASMR and implicit in its operationalisation as a trait and state; however, it is rarely explicitly measured. In this paper, we present the 37-item ASMR Trigger Checklist (ATC), a new tool to assist researchers in ASMR-responder identification and to capture individual differences in the number and intensity of ASMR triggers across auditory (vocal, non-vocal), visual, and tactile/interpersonal stimulus domains. The ATC is related to existing measures of trait-ASMR that tap into the sensations and phenomenological aspects of the experience (ASMR-15 and AEQ) and provides a complementary assessment for researchers interested in common ASMR elicitors. Importantly, the ATC addresses concerns regarding the over-reliance of audio-visual ASMR stimuli in existing measures and conceptualisations of ASMR by emphasising tactile and interpersonal stimuli. Physical touch to the body was both the most endorsed (98%) and intense (average 5/6) ASMR trigger. 24 of the 37 ATC items were endorsed by 75% of the sample and might therefore be considered prototypical ASMR triggers. The ATC has appropriate convergent validity through its association with other individual differences known to be related to ASMR (e.g., absorption, openness to experience, aesthetic experiences). Re-administration of the ATC after 5 months showed high consistency in reports of ASMR triggers with 84% of endorsements remaining the same over time. We hope that the ATC will prove a useful tool for researchers in participant selection and recruitment as well as for measuring individual differences within the ASMR population.

Excitation-Inhibition Imbalance in Migraine: From Neurotransmitters to Brain Oscillations.

Migraine is among the most common and debilitating neurological disorders typically affecting people of working age. It is characterised by a unilateral, pulsating headache often associated with severe pain. Despite the intensive research, there is still little understanding of the pathophysiology of migraine. At the electrophysiological level, altered oscillatory parameters have been reported within the alpha and gamma bands. At the molecular level, altered glutamate and GABA concentrations have been reported. However, there has been little cross-talk between these lines of research. Thus, the relationship between oscillatory activity and neurotransmitter concentrations remains to be empirically traced. Importantly, how these indices link back to altered sensory processing has to be clearly established as yet. Accordingly, pharmacologic treatments have been mostly symptom-based, and yet sometimes proving ineffective in resolving pain or related issues. This review provides an integrative theoretical framework of excitation-inhibition imbalance for the understanding of current evidence and to address outstanding questions concerning the pathophysiology of migraine. We propose the use of computational modelling for the rigorous formulation of testable hypotheses on mechanisms of homeostatic imbalance and for the development of mechanism-based pharmacological treatments and neurostimulation interventions.

Assessing the specificity of the relationship between brain alpha oscillations and tonic pain.

Recent research proposed that the slowing of individual alpha frequency (IAF) could be an objective marker of pain. However, it is unclear whether this research can fully address the requirements of specificity and sensitivity of IAF to the pain experience. Here, we sought to develop a robust methodology for assessing the specificity of the relationship between alpha oscillations and acute tonic pain in healthy individuals. We recorded electroencephalography (EEG) of 36 volunteers during consecutive 5-minute sessions of painful hot water immersion, innocuous warm water immersion and aversive, non-painful auditory stimulus, matched by unpleasantness to the painful condition. Participants rated stimulus unpleasantness throughout each condition. We isolated two regions of the scalp displaying peak alpha activity across participants: centro-parietal (CP) and parieto-occipital (PO) ROI. In line with previous research our findings revealed decreased IAF during hot compared with warm stimulation, however the effect was not specific for pain as we found no difference between hot and sound in the CP ROI (compared to baseline). In contrast, the PO ROI reported the same pattern of differences, but their direction was opposite to the CP in that this ROI revealed faster frequency during hot condition than controls. Finally, we show that IAF in both ROIs did not mediate the relationship between the experimental manipulation and the affective experience. Altogether, these findings emphasize the importance of a robust methodological and analytical design to disclose the functional role of alpha oscillations during affective processing. Likewise, they suggest the absence of a causal role of IAF in the generation of acute pain experience in healthy individuals.

Touching you, touching me: Higher incidence of mirror-touch synaesthesia and positive (but not negative) reactions to social touch in Autonomous Sensory Meridian Response.

The characterisation of autonomous sensory meridian response (ASMR) as an audio-visual phenomenon overlooks how tactile experiences are not just perceptual concurrents of ASMR (i.e., tingling) but also commonly strong ASMR inducers. Here we systematically investigated whether ASMR-responders show altered tactile processing compared to controls. Using a screening measure of vicarious touch with a predefined cut-off for mirror-touch synaesthesia (MTS; a condition where tactile sensations are experienced when viewing, but not receiving, touch), we found that ASMR-responders had more frequent and intense vicarious touch experiences, as well as a strikingly higher incidence of MTS, than non-responders. ASMR-responders also reported greater reactivity to positive, but not negative, interpersonal touch. Correlations further showed these patterns to be more prevalent in those responders with stronger ASMR. We discuss the implications of our findings in terms of heightened sensory sensitivity, bodily awareness, and the underlying neuro-cognitive mechanisms driving vicarious tactile perception in ASMR and MTS.

The speed of parietal theta frequency drives visuospatial working memory capacity.

The speed of theta brain oscillatory activity is thought to play a key role in determining working memory (WM) capacity. Individual differences in the length of a theta cycle (ranging between 4 and 7 Hz) might determine how many gamma cycles (>30 Hz) can be nested into a theta wave. Gamma cycles are thought to represent single memory items; therefore, this interplay could determine individual memory capacity. We directly tested this hypothesis by means of parietal transcranial alternating current stimulation (tACS) set at slower (4 Hz) and faster (7 Hz) theta frequencies during a visuospatial WM paradigm. Accordingly, we found that 4-Hz tACS enhanced WM capacity, while 7-Hz tACS reduced WM capacity. Notably, these effects were found only for items presented to the hemifield contralateral to the stimulation site. This provides causal evidence for a frequency-dependent and spatially specific organization of WM storage, supporting the theta-gamma phase coupling theory of WM capacity.

The temporal sensitivity to the tactile-induced double flash illusion mediates the impact of beta oscillations on schizotypal personality traits.

The coherent experience of the self and the world depends on the ability to integrate vs. segregate sensory information. Optimal temporal integration between the senses is mediated by oscillatory properties of neural activity. Previous research showed reduced temporal sensitivity to multisensory events in schizotypy, a personality trait linked to schizophrenia. Here we used the tactile-induced Double-Flash-Illusion (tDFI) to investigate the tactile-to-visual temporal sensitivity in schizotypy, as indexed by the temporal window of illusion (TWI) and its neural underpinnings. We measured EEG oscillations within the beta band, recently shown to correlate with the tDFI. We found individuals with higher schizotypal traits to have wider TWI and slower beta waves accounting for the temporal window within which they perceive the illusion. Our results indicate reduced tactile-to-visual temporal sensitivity to mediate the effect of slowed oscillatory beta activity on schizotypal personality traits. We conclude that slowed oscillatory patterns might constitute an early marker for psychosis proneness.

Oscillatory Properties of Functional Connections Between Sensory Areas Mediate Cross-Modal Illusory Perception.

The presentation of simple auditory stimuli can significantly impact visual processing and even induce visual illusions, such as the auditory-induced double flash illusion (DFI). These cross-modal processes have been shown to be driven by occipital oscillatory activity within the alpha band. Whether this phenomenon is network specific or can be generalized to other sensory interactions remains unknown. The aim of the current study was to test whether cross-modal interactions between somatosensory-to-visual areas leading to the same (but tactile-induced) DFI share similar properties with the auditory DFI. We hypothesized that if the effects are mediated by the oscillatory properties of early visual areas per se, then the two versions of the illusion should be subtended by the same neurophysiological mechanism (i.e., the speed of the alpha frequency). Alternatively, if the oscillatory activity in visual areas predicting this phenomenon is dependent on the specific neural network involved, then it should reflect network-specific oscillatory properties. In line with the latter, results recorded in humans (both sexes) show a network-specific oscillatory profile linking the auditory DFI to occipital alpha oscillations, replicating previous findings, and tactile DFI to occipital beta oscillations, a rhythm typical of somatosensory processes. These frequency-specific effects are observed for visual (but not auditory or somatosensory) areas and account for auditory-visual connectivity in the alpha band and somatosensory-visual connectivity in the beta band. We conclude that task-dependent visual oscillations reflect network-specific oscillatory properties favoring optimal directional neural communication timing for sensory binding.SIGNIFICANCE STATEMENT We investigated the oscillatory correlates of the auditory- and tactile-induced double flash illusion (DFI), a phenomenon where two interleaved beeps (taps) set within 100 ms apart and paired with one visual flash induce the sensation of a second illusory flash. Results confirm previous evidence that the speed of individual occipital alpha oscillations predict the temporal window of the auditory-induced illusion. Importantly, they provide novel evidence that the tactile-induced DFI is instead mediated by the speed of individual occipital beta oscillations. These task-dependent occipital oscillations are shown to be mediated by the oscillatory properties of the neural network engaged in the task to favor optimal temporal integration between the senses.

Individual Alpha Frequency Predicts Perceived Visuotactile Simultaneity.

Temporal encoding is a key feature in multisensory processing that leads to the integration versus segregation of perceived events over time. Whether or not two events presented at different offsets are perceived as simultaneous varies widely across the general population. Such tolerance to temporal delays is known as the temporal binding window (TBW). It has been recently suggested that individual oscillatory alpha frequency (IAF) peak may represent the electrophysiological correlate of TBW, with IAF also showing a wide variability in the general population (8-12 Hz). In our work, we directly tested this hypothesis by measuring each individual's TBW during a visuotactile simultaneity judgment task while concurrently recording their electrophysiological activity. We found that the individual's TBW significantly correlated with their left parietal IAF, such that faster IAF accounted for narrower TBW. Furthermore, we found that higher prestimulus alpha power measured over the same left parietal regions accounted for more veridical responses of non-simultaneity, which may be explained either by accuracy in perceptual simultaneity or, alternatively, in line with recent proposals by a shift in response bias from more conservative (high alpha power) to more liberal (low alpha power). We propose that the length of an alpha cycle constrains the temporal resolution within which perceptual processes take place.

Individual differences in sensory integration predict differences in time perception and individual levels of schizotypy.

To interact functionally with our environment, our perception must locate events in time, including discerning whether sensory events are simultaneous. The Temporal Binding Window (TBW; the time window within which two stimuli tend to be integrated into one event) has been shown to relate to individual differences in perception, including schizotypy, but the relationship with subjective estimates of duration is unclear. We compare individual TBWs with individual differences in the filled duration illusion, exploiting differences in perception between empty and filled durations (the latter typically being perceived as longer). Schizotypy has been related to both these measures and is included to explore a potential link between these tasks and enduring perceptual differences. Results suggest that individuals with a narrower TBW make longer estimates for empty durations and demonstrate less variability in both conditions. Exploratory analysis of schizotypy data suggests a relationship with the TBW but is inconclusive regarding time perception.

Alpha Oscillations Are Causally Linked to Inhibitory Abilities in Ageing.

Aging adults typically show reduced ability to ignore task-irrelevant information, an essential skill for optimal performance in many cognitive operations, including those requiring working memory (WM) resources. In a first experiment, young and elderly human participants of both genders performed an established WM paradigm probing inhibitory abilities by means of valid, invalid, and neutral retro-cues. Elderly participants showed an overall cost, especially in performing invalid trials, whereas younger participants' general performance was comparatively higher, as expected.Inhibitory abilities have been linked to alpha brain oscillations but it is yet unknown whether in aging these oscillations (also typically impoverished) and inhibitory abilities are causally linked. To probe this possible causal link in aging, we compared in a second experiment parietal alpha-transcranial alternating current stimulation (tACS) with either no stimulation (Sham) or with two control stimulation frequencies (theta- and gamma-tACS) in the elderly group while performing the same WM paradigm. Alpha- (but not theta- or gamma-) tACS selectively and significantly improved performance (now comparable to younger adults' performance in the first experiment), particularly for invalid cues where initially elderly showed the highest costs. Alpha oscillations are therefore causally linked to inhibitory abilities and frequency-tuned alpha-tACS interventions can selectively change these abilities in the elderly.SIGNIFICANCE STATEMENT Ignoring task-irrelevant information, an ability associated to rhythmic brain activity in the alpha frequency band, is fundamental for optimal performance. Indeed, impoverished inhibitory abilities contribute to age-related decline in cognitive functions like working memory (WM), the capacity to briefly hold information in mind. Whether in aging adults alpha oscillations and inhibitory abilities are causally linked is yet unknown. We experimentally manipulated frequency-tuned brain activity using transcranial alternating current stimulation (tACS), combined with a retro-cue paradigm assessing WM and inhibition. We found that alpha-tACS induced a significant improvement in target responses and misbinding errors, two indexes of inhibition. We concluded that in aging alpha oscillations are causally linked to inhibitory abilities, and that despite being impoverished, these abilities are still malleable.

Slow Theta tACS of the Right Parietal Cortex Enhances Contralateral Visual Working Memory Capacity.

Recent research suggests alteration of visual working memory capacity by modulation of parietal theta frequency via transcranial alternating current stimulation (tACS). However, it remains to be clarified whether this effect is partly driven by co-stimulation of prefrontal cortex and subcortical structures. It was hypothesized that focal tACS over the parietal lobe without additional prefrontal or subcortical stimulation should lead to similar effects as reported in the literature. Healthy, young participants were tested on a visual working memory paradigm while receiving either focal parietal tACS at 4 Hz, at 7 Hz or sham stimulation. Focal right posterior 4 Hz tACS led to increased working memory capacity strictly for the visual hemifield contralateral to stimulation. Exclusive stimulation of posterior cortex by 4 Hz tACS replicates effects recently reported in literature, confirming that stimulation of the prefrontal cortex or subcortical structures are not a primary driver of these observations.

Higher proneness to multisensory illusions is driven by reduced temporal sensitivity in people with high schizotypal traits.

A coherent sense of self, typically altered in schizophrenia, is accompanied by a coherent ability to integrate sensory information. According to the idea of a psychosis continuum, high schizotypal traits in the general population may be associated to higher proneness to multisensory illusions, akin to schizophrenia. We directly tested this hypothesis by means of the double-flash illusion in participants with low and high schizotypal scores. We confirmed the higher proneness to illusions in the high-schizotypal group. Crucially, such higher proneness was fully explained by a significantly reduced temporal sensitivity to integrate sensory information. We conclude that reduced temporal sensitivity accounts for enhanced proneness to illusions in people at higher risk and represents an early marker of psychosis.

Causal evidence that intrinsic beta-frequency is relevant for enhanced signal propagation in the motor system as shown through rhythmic TMS.

Correlative evidence provides support for the idea that brain oscillations underpin neural computations. Recent work using rhythmic stimulation techniques in humans provide causal evidence but the interactions of these external signals with intrinsic rhythmicity remain unclear. Here, we show that sensorimotor cortex follows externally applied rhythmic TMS (rTMS) stimulation in the beta-band but that the elicited responses are strongest at the intrinsic individual beta peak frequency. While these entrainment effects are of short duration, even subthreshold rTMS pulses propagate through the network and elicit significant cortico-spinal coupling, particularly when stimulated at the individual beta-frequency. Our results show that externally enforced rhythmicity interacts with intrinsic brain rhythms such that the individual peak frequency determines the effect of rTMS. The observed downstream spinal effect at the resonance frequency provides evidence for the causal role of brain rhythms for signal propagation.