Developmental changes in individual alpha frequency: Recording EEG data during public engagement events.

Statistical power in cognitive neuroimaging experiments is often very low. Low sample size can reduce the likelihood of detecting real effects (false negatives) and increase the risk of detecting non-existing effects by chance (false positives). Here, we document our experience of leveraging a relatively unexplored method of collecting a large sample size for simple electroencephalography (EEG) studies: by recording EEG in the community during public engagement and outreach events. We collected data from 346 participants (189 females, age range 6-76 years) over 6 days, totalling 29 hours, at local science festivals. Alpha activity (6-15 Hz) was filtered from 30 seconds of signal, recorded from a single electrode placed between the occipital midline (Oz) and inion (Iz) while the participants rested with their eyes closed. A total of 289 good-quality datasets were obtained. Using this community-based approach, we were able to replicate controlled, lab-based findings: individual alpha frequency (IAF) increased during childhood, reaching a peak frequency of 10.28 Hz at 28.1 years old, and slowed again in middle and older age. Total alpha power decreased linearly, but the aperiodic-adjusted alpha power did not change over the lifespan. Aperiodic slopes and intercepts were highest in the youngest participants. There were no associations between these EEG indexes and self-reported fatigue, measured by the Multidimensional Fatigue Inventory. Finally, we present a set of important considerations for researchers who wish to collect EEG data within public engagement and outreach environments.

Can we manipulate brain connectivity? A systematic review of cortico-cortical paired associative stimulation effects.

OBJECTIVE: Cortico-cortical paired associative stimulation (ccPAS) is a form of dual-site transcranial magnetic stimulation (TMS) entailing a series of single-TMS pulses paired at specific interstimulus intervals (ISI) delivered to distant cortical areas. The goal of this article is to systematically review its efficacy in inducing plasticity in humans focusing on stimulation parameters and hypotheses of underlying neurophysiology. METHODS: A systematic review of the literature from 2009-2023 was undertaken to identify all articles utilizing ccPAS to study brain plasticity and connectivity. Six electronic databases were searched and included. RESULTS: 32 studies were identified. The studies targeted connections within the same hemisphere or between hemispheres. 28 ccPAS studies were in healthy participants, 1 study in schizophrenia, and 1 in Alzheimer's disease (AD) patients. 2 additional studies used cortico-cortical repetitive paired associative stimulation (cc-rPAS) in generalized anxiety disorder (GAD) patients. Outcome measures include electromyography (EMG), behavioral measures, electroencephalography (EEG), and functional magnetic resonance imaging (fMRI). ccPAS seems to be able to modulate brain connectivity depending on the ISI. CONCLUSIONS: ccPAS can be used to modulate corticospinal excitability, brain activity, and behavior. Although the stimulation parameters used across studies reviewed in this paper are varied, ccPAS is a promising approach for basic research and potential clinical applications. SIGNIFICANCE: Recent advances in neuroscience have caused a shift of interest from the study of single areas to a more complex approach focusing on networks of areas that orchestrate brain activity. Consequently, the TMS community is also witnessing a change, with a growing interest in targeting multiple brain areas rather than a single locus, as evidenced by an increasing number of papers using ccPAS. In light of this new enthusiasm for brain connectivity, this review summarizes existing literature and stimulation parameters that have proven effective in changing electrophysiological, behavioral, or neuroimaging-derived measures.

Distinct frequencies balance segregation with interaction between different memory types within a prefrontal circuit.

Once formed, the fate of memory is uncertain. Subsequent offline interactions between even different memory types (actions versus words) modify retention.1,2,3,4,5,6 These interactions may occur due to different oscillations functionally linking together different memory types within a circuit.7,8,9,10,11,12,13 With memory processing driving the circuit, it may become less susceptible to external influences.14 We tested this prediction by perturbing the human brain with single pulses of transcranial magnetic stimulation (TMS) and simultaneously measuring the brain activity changes with electroencephalography (EEG15,16,17). Stimulation was applied over brain areas that contribute to memory processing (dorsolateral prefrontal cortex, DLPFC; primary motor cortex, M1) at baseline and offline, after memory formation, when memory interactions are known to occur.1,4,6,10,18 The EEG response decreased offline (compared with baseline) within the alpha/beta frequency bands when stimulation was applied to the DLPFC, but not to M1. This decrease exclusively followed memory tasks that interact, revealing that it was due specifically to the interaction, not task performance. It remained even when the order of the memory tasks was changed and so was present, regardless of how the memory interaction was produced. Finally, the decrease within alpha power (but not beta) was correlated with impairment in motor memory, whereas the decrease in beta power (but not alpha) was correlated with impairment in word-list memory. Thus, different memory types are linked to different frequency bands within a DLPFC circuit, and the power of these bands shapes the balance between interaction and segregation between these memories.

Challenging inhibitory control with high- and low-calorie food: A behavioural and TMS study.

Most people are often tempted by their impulses to "indulge" in high-calorie food, even if this behaviour is not consistent with their goal to control weight in the long term and might not be healthy. The outcome of this conflict is strongly dependent on inhibitory control. It has already been reported that individuals with weaker inhibitory control consume more high-calorie food, are more often unsuccessful dieters, overweight or obese compared to people with more effective inhibitory control. In the present study, we aimed at investigating inhibitory control in the context of human eating behaviour. A sample of 20 healthy normal-weight adults performed a 50% probability visual affective Go/NoGo task involving food (high- and low-calorie) and non-food images as stimuli. Single-pulse transcranial magnetic stimulation (TMS) was administered over the right primary motor cortex (M1) either 300 ms after image presentation to measure corticospinal excitability during the different stimulus categories or 300 ms after the appearance of a fixation point, as a control stimulation condition. The experimental session consisted of a food target and a non-food target block. Behavioural outcomes showed a natural implicit inclination towards high-calorie food in that participants were faster and more accurate compared to the other categories. This advantage was selectively deleted by TMS, which slowed down reaction times. MEPs did not differ according to the stimulus category, but, as expected, were bigger for Go compared to NoGo trials. Participants judged high-calorie food also as more appetising than low-calorie food images. Overall, our results point to a differential modulation when targeting inhibitory control, in favour of the more palatable food category (high-calorie). Present data suggest that the activity of the motor system is modulated by food nutritional value, being more engaged by appetising food. Future work should explore to what extent these processes are affected in patients with eating disorders and should aim to better characterise the related dynamics of cortical connectivity within the motor network.

TMS combined with EEG: Recommendations and open issues for data collection and analysis.

Transcranial magnetic stimulation (TMS) evokes neuronal activity in the targeted cortex and connected brain regions. The evoked brain response can be measured with electroencephalography (EEG). TMS combined with simultaneous EEG (TMS-EEG) is widely used for studying cortical reactivity and connectivity at high spatiotemporal resolution. Methodologically, the combination of TMS with EEG is challenging, and there are many open questions in the field. Different TMS-EEG equipment and approaches for data collection and analysis are used. The lack of standardization may affect reproducibility and limit the comparability of results produced in different research laboratories. In addition, there is controversy about the extent to which auditory and somatosensory inputs contribute to transcranially evoked EEG. This review provides a guide for researchers who wish to use TMS-EEG to study the reactivity of the human cortex. A worldwide panel of experts working on TMS-EEG covered all aspects that should be considered in TMS-EEG experiments, providing methodological recommendations (when possible) for effective TMS-EEG recordings and analysis. The panel identified and discussed the challenges of the technique, particularly regarding recording procedures, artifact correction, analysis, and interpretation of the transcranial evoked potentials (TEPs). Therefore, this work offers an extensive overview of TMS-EEG methodology and thus may promote standardization of experimental and computational procedures across groups.

Effects of Rhythmic Transcranial Magnetic Stimulation in the Alpha-Band on Visual Perception Depend on Deviation From Alpha-Peak Frequency: Faster Relative Transcranial Magnetic Stimulation Alpha-Pace Improves Performance.

Alpha-band oscillatory activity over occipito-parietal areas is involved in shaping perceptual and cognitive processes, with a growing body of electroencephalographic (EEG) evidence indicating that pre-stimulus alpha-band amplitude relates to the subjective perceptual experience, but not to objective measures of visual task performance (discrimination accuracy). The primary aim of the present transcranial magnetic stimulation (TMS) study was to investigate whether causality can be established for this relationship, using rhythmic (alpha-band) TMS entrainment protocols. It was anticipated that pre-stimulus 10 Hz-TMS would induce changes in subjective awareness ratings but not accuracy, in the visual hemifield contralateral to TMS. To test this, we administered 10 Hz-TMS over the right intraparietal sulcus prior to visual stimulus presentation in 17 participants, while measuring their objective performance and subjective awareness in a visual discrimination task. Arrhythmic and 10 Hz sham-TMS served as control conditions (within-participant design). Resting EEG was used to record individual alpha frequency (IAF). A study conducted in parallel to ours with a similar design but reported after we completed data collection informed further, secondary analyses for a causal relationship between pre-stimulus alpha-frequency and discrimination accuracy. This was explored through a regression analysis between rhythmic-TMS alpha-pace relative to IAF and performance measures. Our results revealed that contrary to our primary expectation, pre-stimulus 10 Hz-TMS did not affect subjective measures of performance, nor accuracy, relative to control-TMS. This null result is in accord with a recent finding showing that for influencing subjective measures of performance, alpha-TMS needs to be applied post-stimulus. In addition, our secondary analysis showed that IAF was positively correlated with task accuracy across participants, and that 10 Hz-TMS effects on accuracy-but not awareness ratings-depended on IAF: The slower (or faster) the IAF, relative to the fixed 10 Hz TMS frequency, the stronger the TMS-induced performance improvement (or worsening), indicating that 10 Hz-TMS produced a gain (or a loss) in individual performance, directly depending on TMS-pace relative to IAF. In support of recent reports, this is evidence for alpha-frequency playing a causal role in perceptual sensitivity likely through regulating the speed of sensory sampling.

Parietal alpha tACS shows inconsistent effects on visuospatial attention.

Transcranial alternating current stimulation (tACS) is a popular technique that has been used for manipulating brain oscillations and inferring causality regarding the brain-behaviour relationship. Although it is a promising tool, the variability of tACS results has raised questions regarding the robustness and reproducibility of its effects. Building on recent research using tACS to modulate visuospatial attention, we here attempted to replicate findings of lateralized parietal tACS at alpha frequency to induce a change in attention bias away from the contra- towards the ipsilateral visual hemifield. 40 healthy participants underwent tACS in two separate sessions where either 10 Hz tACS or sham was applied via a high-density montage over the left parietal cortex at 1.5 mA for 20 min, while performance was assessed in an endogenous attention task. Task and tACS parameters were chosen to match those of previous studies reporting positive effects. Unlike these studies, we did not observe lateralized parietal alpha tACS to affect attention deployment or visual processing across the hemifields as compared to sham. Likewise, additional resting electroencephalography immediately offline to tACS did not reveal any notable effects on individual alpha power or frequency. Our study emphasizes the need for more replication studies and systematic investigations of the factors that drive tACS effects.

Top-down control of visual cortex by the frontal eye fields through oscillatory realignment.

Voluntary allocation of visual attention is controlled by top-down signals generated within the Frontal Eye Fields (FEFs) that can change the excitability of lower-level visual areas. However, the mechanism through which this control is achieved remains elusive. Here, we emulated the generation of an attentional signal using single-pulse transcranial magnetic stimulation to activate the FEFs and tracked its consequences over the visual cortex. First, we documented changes to brain oscillations using electroencephalography and found evidence for a phase reset over occipital sites at beta frequency. We then probed for perceptual consequences of this top-down triggered phase reset and assessed its anatomical specificity. We show that FEF activation leads to cyclic modulation of visual perception and extrastriate but not primary visual cortex excitability, again at beta frequency. We conclude that top-down signals originating in FEF causally shape visual cortex activity and perception through mechanisms of oscillatory realignment.

Perceptual and Physiological Consequences of Dark Adaptation: A TMS-EEG Study.

Existing literature on sensory deprivation suggests that short-lasting periods of dark adaptation (DA) can cause changes in visual cortex excitability. DA cortical effects have previously been assessed through phosphene perception, i.e., the ability to report visual sensations when a transcranial magnetic stimulation (TMS) pulse is delivered over the visual cortex. However, phosphenes represent an indirect measure of visual cortical excitability which relies on a subjective report. Here, we aimed at overcoming this limitation by assessing visual cortical excitability by combining subjective (i.e., TMS-induced phosphenes) and objective (i.e., TMS-evoked potentials - TEPs) measurements in a TMS-EEG protocol after 30 min of DA. DA effects were compared to a control condition, entailing 30 min of controlled light exposure. TMS was applied at 11 intensities in order to estimate the psychometric function of phosphene report and explore the relationship between TEPs and TMS intensity. Compared to light adaptation, after DA the slope of the psychometric function was significantly steeper, and the amplitude of a TEP component (P60) was lower, only for high TMS intensities. The perceptual threshold was not affected by DA. These results support the idea that DA leads to a change in the excitability of the visual cortex, accompanied by a behavioral modification of visual perception. Furthermore, this study provides a first valuable description of the relationship between TMS intensity and visual TEPs.

Both dorsal and ventral attention network nodes are implicated in exogenously driven visuospatial anticipation.

Neuroimaging and transcranial magnetic stimulation (TMS) studies have implicated a dorsal fronto-parietal network in endogenous attention control and a more ventral set of areas in exogenous attention shifts. However, the extent and circumstances under which these cortical networks overlap and/or interact remain unclear. Crucially, whereas previous studies employed experimental designs that tend to confound exogenous with endogenous attentional engagement, we used a cued target discrimination paradigm that behaviourally dissociates exogenous from endogenous attention processes. Participants engaged with endogenous attention cues, while simultaneous apparent motion cues were driving exogenous attention along the motion path towards or away from the target position. To interfere with dorsal or ventral attention networks, we delivered neuronavigated double-pulse TMS over either right intraparietal sulcus (rIPS) or right temporo-parietal junction (rTPJ) towards the end of the cue target interval, and compared the effects to a sham-TMS condition. For sham-TMS, endogenous and exogenous cueing both benefitted discrimination accuracy. Target discrimination was enhanced at validly versus invalidly cued locations (endogenous cueing benefit) as well as when targets appeared in versus out of the motion path (exogenous cueing benefit), despite motion being uninformative and task-irrelevant, replicating previous findings. Interestingly, both rIPS- and rTPJ-TMS abolished attention benefits from exogenous cueing, while endogenous cueing benefits were unaffected. Our findings provide evidence against independent involvement of the dorsal and ventral attention network nodes in exogenous attention processes.

Frequency and power of human alpha oscillations drift systematically with time-on-task.

Oscillatory neural activity is a fundamental characteristic of the mammalian brain spanning multiple levels of spatial and temporal scale. Current theories of neural oscillations and analysis techniques employed to investigate their functional significance are based on an often implicit assumption: In the absence of experimental manipulation, the spectral content of any given EEG- or MEG-recorded neural oscillator remains approximately stationary over the course of a typical experimental session (∼1 h), spontaneously fluctuating only around its dominant frequency. Here, we examined this assumption for ongoing neural oscillations in the alpha-band (8-13 Hz). We found that alpha peak frequency systematically decreased over time, while alpha-power increased. Intriguingly, these systematic changes showed partial independence of each other: Statistical source separation (independent component analysis) revealed that while some alpha components displayed concomitant power increases and peak frequency decreases, other components showed either unique power increases or frequency decreases. Interestingly, we also found these components to differ in frequency. Components that showed mixed frequency/power changes oscillated primarily in the lower alpha-band (∼8-10 Hz), while components with unique changes oscillated primarily in the higher alpha-band (∼9-13 Hz). Our findings provide novel clues on the time-varying intrinsic properties of large-scale neural networks as measured by M/EEG, with implications for the analysis and interpretation of studies that aim at identifying functionally relevant oscillatory networks or at driving them through external stimulation.

The EEG signature of sensory evidence accumulation during decision formation closely tracks subjective perceptual experience.

How neural representations of low-level visual information are accessed by higher-order processes to inform decisions and give rise to conscious experience is a longstanding question. Research on perceptual decision making has revealed a late event-related EEG potential (the Centro-Parietal Positivity, CPP) to be a correlate of the accumulation of sensory evidence. We tested how this evidence accumulation signal relates to externally presented (physical) and internally experienced (subjective) sensory evidence. Our results show that the known relationship between the physical strength of the external evidence and the evidence accumulation signal (reflected in the CPP amplitude) is mediated by the level of subjective experience of stimulus strength. This shows that the CPP closely tracks the subjective perceptual evidence, over and above the physically presented evidence. We conclude that a remarkably close relationship exists between the evidence accumulation process (i.e. CPP) and subjective perceptual experience, suggesting that neural decision processes and components of conscious experience are tightly linked.

Prismatic Adaptation Modulates Oscillatory EEG Correlates of Motor Preparation but Not Visual Attention in Healthy Participants.

Prismatic adaption (PA) has been proposed as a tool to induce neural plasticity and is used to help neglect rehabilitation. It leads to a recalibration of visuomotor coordination during pointing as well as to aftereffects on a number of sensorimotor and attention tasks, but whether these effects originate at a motor or attentional level remains a matter of debate. Our aim was to further characterize PA aftereffects by using an approach that allows distinguishing between effects on attentional and motor processes. We recorded EEG in healthy human participants (9 females and 7 males) while performing a new double step, anticipatory attention/motor preparation paradigm before and after adaptation to rightward-shifting prisms, with neutral lenses as a control. We then examined PA aftereffects through changes in known oscillatory EEG signatures of spatial attention orienting and motor preparation in the alpha and beta frequency bands. Our results were twofold. First, we found PA to rightward-shifting prisms to selectively affect EEG signatures of motor but not attentional processes. More specifically, PA modulated preparatory motor EEG activity over central electrodes in the right hemisphere, contralateral to the PA-induced, compensatory leftward shift in pointing movements. No effects were found on EEG signatures of spatial attention orienting over occipitoparietal sites. Second, we found the PA effect on preparatory motor EEG activity to dominate in the beta frequency band. We conclude that changes to intentional visuomotor, rather than attentional visuospatial, processes underlie the PA aftereffect of rightward-deviating prisms in healthy participants.SIGNIFICANCE STATEMENT Prismatic adaptation (PA) has been proposed as a tool to induce neural plasticity in both healthy participants and patients, due to its aftereffect impacting on a number of visuospatial and visuomotor functions. However, the neural mechanisms underlying PA aftereffects are poorly understood as only little neuroimaging evidence is available. Here, we examined, for the first time, the origin of PA aftereffects studying oscillatory brain activity. Our results show a selective modulation of preparatory motor activity following PA in healthy participants but no effect on attention-related activity. This provides novel insight into the PA aftereffect in the healthy brain and may help to inform interventions in neglect patients.

Prestimulus EEG Power Predicts Conscious Awareness But Not Objective Visual Performance.

Prestimulus oscillatory neural activity has been linked to perceptual outcomes during performance of psychophysical detection and discrimination tasks. Specifically, the power and phase of low frequency oscillations have been found to predict whether an upcoming weak visual target will be detected or not. However, the mechanisms by which baseline oscillatory activity influences perception remain unclear. Recent studies suggest that the frequently reported negative relationship between α power and stimulus detection may be explained by changes in detection criterion (i.e., increased target present responses regardless of whether the target was present/absent) driven by the state of neural excitability, rather than changes in visual sensitivity (i.e., more veridical percepts). Here, we recorded EEG while human participants performed a luminance discrimination task on perithreshold stimuli in combination with single-trial ratings of perceptual awareness. Our aim was to investigate whether the power and/or phase of prestimulus oscillatory activity predict discrimination accuracy and/or perceptual awareness on a trial-by-trial basis. Prestimulus power (3-28 Hz) was inversely related to perceptual awareness ratings (i.e., higher ratings in states of low prestimulus power/high excitability) but did not predict discrimination accuracy. In contrast, prestimulus oscillatory phase did not predict awareness ratings or accuracy in any frequency band. These results provide evidence that prestimulus α power influences the level of subjective awareness of threshold visual stimuli but does not influence visual sensitivity when a decision has to be made regarding stimulus features. Hence, we find a clear dissociation between the influence of ongoing neural activity on conscious awareness and objective performance.

Role of the Cerebellum in Adaptation to Delayed Action Effects.

Actions are typically associated with sensory consequences. For example, knocking at a door results in predictable sounds. These self-initiated sensory stimuli are known to elicit smaller cortical responses compared to passively presented stimuli, e.g., early auditory evoked magnetic fields known as M100 and M200 components are attenuated. Current models implicate the cerebellum in the prediction of the sensory consequences of our actions. However, causal evidence is largely missing. In this study, we introduced a constant delay (of 100 ms) between actions and action-associated sounds, and we recorded magnetoencephalography (MEG) data as participants adapted to the delay. We found an increase in the attenuation of the M100 component over time for self-generated sounds, which indicates cortical adaptation to the introduced delay. In contrast, no change in M200 attenuation was found. Interestingly, disrupting cerebellar activity via transcranial magnetic stimulation (TMS) abolished the adaptation of M100 attenuation, while the M200 attenuation reverses to an M200 enhancement. Our results provide causal evidence for the involvement of the cerebellum in adapting to delayed action effects, and thus in the prediction of the sensory consequences of our actions.

Inconsistent Effects of Parietal α-tACS on Pseudoneglect across Two Experiments: A Failed Internal Replication.

Transcranial electrical stimulation (tES) is being investigated as an experimental and clinical interventional technique in human participants. While promising, important limitations have been identified, including weak effect sizes and high inter- and intra-individual variability of outcomes. Here, we compared two "inhibitory" tES-techniques with supposedly different mechanisms of action as to their effects on performance in a visuospatial attention task, and report on a direct replication attempt. In two experiments, 2 × 20 healthy participants underwent tES in three separate sessions testing different protocols (10 min stimulation each) with a montage targeting right parietal cortex (right parietal-left frontal, electrode-sizes: 3cm × 3cm-7 cm × 5 cm), while performing a perceptual line bisection (landmark) task. The tES-protocols were compared as to their ability to modulate pseudoneglect (thought to be under right hemispheric control). In experiment 1, sham-tES was compared to transcranial alternating current stimulation at alpha frequency (10 Hz; α-tACS) (expected to entrain "inhibitory" alpha oscillations) and to cathodal transcranial direct current stimulation (c-tDCS) (shown to suppress neuronal spiking activity). In experiment 2, we attempted to replicate the findings of experiment 1, and establish frequency-specificity by adding a 45 Hz-tACS condition to α-tACS and sham. In experiment 1, right parietal α-tACS led to the expected changes in spatial attention bias, namely a rightward shift in subjective midpoint estimation (relative to sham). However, this was not confirmed in experiment 2 and in the complete sample. Right parietal c-tDCS and 45 Hz-tACS had no effect. These results highlight the importance of replication studies, adequate statistical power and optimizing tES-interventions for establishing the robustness and reliability of electrical stimulation effects, and best practice.

Subthalamic stimulation and levodopa modulate cortical reactivity in Parkinson's patients.

BACKGROUND: The effects of deep brain stimulation of the subthalamic nucleus (DBS-STN) and L-dopa (LD) on cortical activity in Parkinson's disease (PD) are poorly understood. OBJECTIVES: By combining transcranial magnetic stimulation (TMS) and electroencephalography (EEG) we explored the effects of STN-DBS, either alone or in combination with L-Dopa (LD), on TMS-evoked cortical activity in a sample of implanted PD patients. METHODS: PD patients were tested in three clinical conditions: i) LD therapy with STN-DBS turned on (ON/ON condition); ii) without LD therapy with STN-DBS turned on (OFF/ON condition); iii) without LD therapy with STN-DBS turned off (OFF/OFF condition). TMS pulses were delivered over left M1 while simultaneously acquiring EEG. Eight age-matched healthy volunteers (HC) were tested as a control group. RESULTS: STN-DBS enhanced early global TMS-evoked activity (∼45-80ms) and high-alpha TMS-evoked oscillations (11-13 Hz) as compared to OFF/OFF condition, independently from concomitant LD therapy. LD intake (ON/ON condition) produced a further increase of late TMS-evoked activity (∼80-130ms) and beta TMS-evoked oscillations (13-30 Hz), as compared to OFF/OFF and OFF/ON conditions, that normalized reactivity as compared to HC range of values. CONCLUSIONS: Our data reveal that bilateral STN-DBS and LD therapy induce a modulation of specific cortical components and specific ranges of frequency. These findings demonstrate that STN-DBS and LD therapy may have synergistic effects on motor cortical activity.