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Stephani, T.

Publications and source records attributed to Stephani, T..

13 recordsLinked to original sources

Somatosensory high frequency oscillations across the human central nervous system

Information transmission in the central nervous system (CNS) relies on the propagation of action potentials (neuronal spikes), traditionally thought to be inaccessible with electroencephalography (EEG). Converging evidence from human and animal recordings however demonstrates that high frequency oscillations (HFOs) in EEG recordings represent neuronal population spiking, complementing standard low-frequency EEG recordings in cortex. Here, we developed an approach to simultaneously record HFOs to somatosensory stimulation across the entire human CNS noninvasively: from spinal over subcortical to cortical stages. Our approach provides a detailed temporal and spectral characterization of HFOs at each CNS level, delineating how they evolve across the somatosensory processing hierarchy. Critically, we show that low and high frequency electrophysiological responses represent at least partly independent processing channels across the CNS. We thus demonstrate the feasibility of studying the full spectrum of neuronal information processing across the CNS, offering a multi-level window into human neurophysiology in health and disease.

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Evaluating noise correction approaches for non-invasive electrophysiology of the human spinal cord

The spinal cord is a vital component of the central nervous system for the processing of sensorimotor information transmitted between the body and the brain. Electrospinography (ESG) is the most accessible non-invasive technique for recording spinal signals in humans, but the vast and detrimental impact of physiological noise (mostly of cardiac nature) has prevented widespread adoption. Here, we aim to address this issue by examining various denoising algorithms for cardiac artefact reduction - including principal component analysis-based techniques (PCA), independent component analysis-based approaches (ICA) and signal space projection (SSP). We observed that in situations where large numbers of spinal electrodes are used, SSP offers the best results in terms of balancing the removal of harmful noise and preserving neural information of interest. In cases where only a small number of electrodes are available, an approach based on PCA is deemed helpful. Approaches based on ICA were found to be unsuitable for cardiac artefact removal in ESG, due to a suboptimal balance of artefact removal and signal preservation. Finally, we also approached this issue from a signal-enhancement perspective and observed that in cases where extensive electrode arrays are used in the context of task-based designs, a spatial filtering technique based on canonical correlation analysis (CCA) reveals clear evoked spinal potentials even with single-trial resolution. Taken together, there are several appropriate algorithms for physiological noise removal in ESG, rendering this an accessible and easy-to-use technique for non-invasive assessments of human spinal cord function.

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Excitability modulations of somatosensory perception do not depend on feedforward neuronal population spikes

Neural states shape perception at earliest cortical processing levels. Previous work in humans showed a relationship between initial cortical excitation, as indicated by the N20 component of the somatosensory evoked potential (SEP), pre-stimulus alpha oscillations, and the perceived intensity in a somatosensory discrimination paradigm. Here we address the follow-up question whether these excitability dynamics reflect changes in feedforward or feedback signals. We leveraged high-frequency oscillations (HFO) as a metric for neuronal population spiking activity of the first excitatory feedforward volley in the somatosensory cortex, non-invasively extracted from electroencephalography (EEG) data of 32 male human participants. Using Bayesian statistics, we found evidence against the involvement of HFO in moment-to-moment variability of perceived stimulus intensity, in contrast to previously observed pre-stimulus alpha and N20 effects. Given that the N20 component presumably reflects backpropagating membrane potentials towards the apical dendrites, we argue that top-down feedback processes (e.g., related to alpha oscillations) may thus rely on modulations at distal dendritic sites of involved pyramidal cells rather than on output firing changes at their basal compartments.

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Pre-stimulus beta power encodes explicit and implicit perceptual biases in distinct cortical areas

Perception is biased by expectations and previous actions. Pre-stimulus brain oscillations are a potential candidate for implementing biases in the brain. In two EEG studies (43 and 39 participants) on somatosensory near-threshold detection, we investigated the pre-stimulus neural correlates of an (implicit) previous choice bias and an explicit bias. The explicit bias was introduced by informing participants about stimulus probability on a single-trial level (volatile context) or block-wise (stable context). Behavioural analysis confirmed adjustments in the decision criterion and confidence ratings according to the cued probabilities and previous choice-induced biases. Pre-stimulus beta power with distinct sources in sensory and higher-order cortical areas predicted explicit and implicit biases, respectively, on a single subject level and partially mediated the impact of previous choice and stimulus probability on the detection response. We suggest pre-stimulus beta oscillations in distinct brain areas as a neural correlate of explicit and implicit biases in somatosensory perception.

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Sensorimotor brain-computer interface performance depends on signal-to-noise ratio but not connectivity of the mu rhythm in a multiverse analysis of longitudinal data

ObjectiveServing as a channel for communication with locked-in patients or control of prostheses, sensorimotor brain-computer interfaces (BCIs) decode imaginary movements from the recorded activity of the users brain. However, many individuals remain unable to control the BCI, and the underlying mechanisms are unclear. The users BCI performance was previously shown to correlate with the resting-state signal-to-noise ratio (SNR) of the mu rhythm and the phase synchronization (PS) of the mu rhythm between sensorimotor areas. Yet, these predictors of performance were primarily evaluated in a single BCI session, while the longitudinal aspect remains rather uninvestigated. In addition, different analysis pipelines were used to estimate PS in source space, potentially hindering the reproducibility of the results. ApproachTo systematically address these issues, we performed an extensive validation of the relationship between pre-stimulus SNR, PS, and session-wise BCI performance using a publicly available dataset of 62 human participants performing up to 11 sessions of BCI training. We performed the analysis in sensor space using the surface Laplacian and in source space by combining 24 processing pipelines in a multiverse analysis. This way, we could investigate how robust the observed effects were to the selection of the pipeline. Main resultsOur results show that SNR had both between- and within-subject effects on BCI performance for the majority of the pipelines. In contrast, the effect of PS on BCI performance was less robust to the selection of the pipeline and became non-significant after controlling for SNR. SignificanceTaken together, our results demonstrate that changes in neuronal connectivity within the sensorimotor system are not critical for learning to control a BCI, and interventions that increase the SNR of the mu rhythm might lead to improvements in the users BCI performance.

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Non-invasive multi-channel electrophysiology of the human spinal cord - assessing somatosensory processing from periphery to cortex

The spinal cord is of fundamental importance for integrative processing in brain-body communication, yet routine non-invasive recordings in humans are hindered by vast methodological challenges. Here we overcome these challenges by developing an easy-to-use electrophysiological approach based on high-density multi-channel spinal recordings combined with multivariate spatial-filtering analyses. These advances enable a spatiotemporal characterization of spinal cord responses and demonstrate a sensitivity that permits assessing even single-trial responses. To furthermore enable the study of integrative processing along the neural processing hierarchy in somatosensation, we expand this approach by simultaneous peripheral, spinal and cortical recordings and provide direct evidence that bottom-up integrative processing occurs already within the spinal cord and thus after the first synaptic relay in the central nervous system. Finally, we demonstrate the versatility of this approach by providing non-invasive recordings of nociceptive spinal cord responses during heat-pain stimulation. Beyond establishing a new window on human spinal cord function at millisecond timescale, this work provides the foundation to study brain-body communication in its entirety in health and disease.

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Cortical response variability is driven by local excitability changes with somatotopic organization

Identical sensory stimuli can lead to different neural responses depending on the instantaneous brain state. Specifically, neural excitability in sensory areas may shape the brains response already from earliest cortical processing onwards. However, whether these dynamics affect a given sensory domain globally or occur on a spatially local level is largely unknown. We studied this in the somatosensory domain of 38 human participants with EEG, presenting stimuli to the median and tibial nerves alternatingly, and testing the co-variation of initial cortical responses in hand and foot areas, as well as their relation to pre-stimulus oscillatory states. We found that amplitude fluctuations of initial cortical responses to hand and foot stimulation - the N20 and P40 components of the somatosensory evoked potential (SEP), respectively - were not related, indicating local excitability changes in primary sensory regions. In addition, effects of pre-stimulus alpha (8-13 Hz) and beta (18-23 Hz) band amplitude on hand-related responses showed a robust somatotopic organization, thus further strengthening the notion of local excitability fluctuations. However, for foot-related responses, the spatial specificity of pre-stimulus effects was less consistent across frequency bands, with beta appearing to be more foot-specific than alpha. Connectivity analyses in source space suggested this to be due to a somatosensory alpha rhythm that is primarily driven by activity in hand regions while beta frequencies may operate in a more hand-region-independent manner. Altogether, our findings suggest spatially distinct excitability dynamics within the primary somatosensory cortex, yet with the caveat that frequency-specific processes in one sub-region may not readily generalize to other sub-regions.

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Harmoni: a Method for Eliminating Spurious Interactions due to the Harmonic Components in Neuronal Data

Cross-frequency synchronization (CFS) has been proposed as a mechanism for integrating spatially and spectrally distributed information in the brain. However, investigating CFS in Magneto- and Electroencephalography (MEG/EEG) is hampered by the presence of spurious neuronal interactions due to the non-sinusoidal waveshape of brain oscillations. Such waveshape gives rise to the presence of oscillatory harmonics mimicking genuine neuronal oscillations. Until recently, however, there has been no methodology for removing these harmonics from neuronal data. In order to address this long-standing challenge, we introduce a novel method (called HARMOnic miNImization - Harmoni) that removes the signal components which can be harmonics of a non-sinusoidal signal. Harmonis working principle is based on the presence of CFS between harmonic components and the fundamental component of a non-sinusoidal signal. We extensively tested Harmoni in realistic EEG simulations. The simulated couplings between the source signals represented genuine and spurious CFS and within-frequency phase synchronization. Using diverse evaluation criteria, including ROC analyses, we showed that the within- and cross-frequency spurious interactions are suppressed significantly, while the genuine activities are not affected. Additionally, we applied Harmoni to real resting-state EEG data revealing intricate remote connectivity patterns which are usually masked by the spurious connections. Given the ubiquity of non-sinusoidal neuronal oscillations in electrophysiological recordings, Harmoni is expected to facilitate novel insights into genuine neuronal interactions in various research fields, and can also serve as a steppingstone towards the development of further signal processing methods aiming at refining within- and cross-frequency synchronization in electrophysiological recordings.

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Alterations in rhythmic and non-rhythmic resting-state EEG activity and their link to cognition in older age

While many structural and biochemical changes in the brain have been previously associated with aging, the findings concerning electrophysiological signatures, reflecting functional properties of neuronal networks, remain rather controversial. To try resolve this issue, we took advantage of a large population study (N=1703) and comprehensively investigated the association of multiple EEG biomarkers (power of alpha and theta oscillations, individual alpha peak frequency (IAF), the slope of 1/f power spectral decay), aging, and aging and cognitive performance. Cognitive performance was captured with three factors representing processing speed, episodic memory, and interference resolution. Our results show that not only did IAF decline with age but it was also associated with interference resolution over multiple cortical areas. To a weaker extent, 1/f slope of the PSD showed age-related reductions, mostly in frontal brain regions. Finally, alpha power was negatively associated with the speed of processing in the right frontal lobe, despite the absence of age-related alterations. Our results thus demonstrate that multiple electrophysiological features, as well as their interplay, should be considered when investigating the association between age, neuronal activity, and cognitive performance.

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Respiration, heartbeat, and conscious tactile perception

Previous studies have shown that timing of sensory stimulation during the cardiac cycle interacts with perception. Given the natural coupling of respiration and cardiac activity, we investigated here their joint effects on tactile perception. Forty-one healthy female and male human participants reported conscious perception of finger near-threshold electrical pulses (33% null trials) and decision confidence while electrocardiography, respiratory activity, and finger photoplethysmography were recorded. Participants adapted their respiratory cycle to expected stimulus onsets to preferentially occur during late inspiration / early expiration. This closely matched heart rate variation (sinus arrhythmia) across the respiratory cycle such that most frequent stimulation onsets occurred during the period of highest heart rate probably indicating highest alertness and cortical excitability. Tactile detection rate was highest during the first quadrant after expiration onset. Inter-individually, stronger respiratory phase-locking to the task was associated with higher detection rates. Regarding the cardiac cycle, we confirmed previous findings that tactile detection rate was higher during diastole than systole and newly specified its minimum at 250 - 300 ms after the R-peak corresponding to the pulse wave arrival in the finger. Expectation of stimulation induced a transient heart deceleration which was more pronounced for unconfident decision ratings. Inter-individually, stronger post-stimulus modulations of heart rate were linked to higher detection rates. In summary, we demonstrate how tuning to the respiratory cycle and integration of respiratory-cardiac signals are used to optimize performance of a tactile detection task. Significance statementMechanistic studies on perception and cognition tend to focus on the brain neglecting contributions of the body. Here, we investigated how respiration and heartbeat influence tactile perception: Respiration phase-locking to expected stimulus onsets corresponds to highest heart rate (and presumably alertness/cortical excitability) and correlates with detection performance. Tactile detection varies across the heart cycle with a minimum when the pulse reaches the finger and a maximum in diastole. Taken together with our previous finding of unchanged early ERPs across the cardiac cycle we conclude that these effects are not a peripheral physiological artifact but a result of cognitive processes that model our bodys internal state, make predictions to guide behavior, and might also tune respiration to serve the task.

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Opposing signatures of neural excitability and sensory input in initial cortical responses differentially predict intensity perception

Perception of sensory information is determined by stimulus features (e.g., intensity) and instantaneous neural states (e.g., excitability). Commonly, it is assumed that both are reflected similarly in evoked brain potentials, that is, higher evoked activity leads to a stronger percept of a stimulus. We tested this assumption in a somatosensory discrimination task in humans, simultaneously assessing (i) single-trial excitatory post-synaptic currents inferred from short-latency somatosensory evoked potentials (SEP), (ii) pre-stimulus alpha oscillations (8-13 Hz), and (iii) peripheral nerve measures. Fluctuations of neural excitability shaped the perceived stimulus intensity already during the very first cortical response (at [~]20 ms) yet demonstrating opposite neural signatures as compared to the effect of presented stimulus intensity. We reconcile this discrepancy via a common framework based on modulations of electro-chemical membrane gradients linking neural states and responses, which calls for reconsidering conventional interpretations of brain potential magnitudes in stimulus intensity encoding.

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Power-Law Dynamics in Cortical Excitability as probed by Early Somatosensory Evoked Responses

Brain responses vary considerably from moment to moment, even to identical sensory stimuli. This has been attributed to changes in instantaneous neuronal states determining the systems excitability. Yet the spatio-temporal organization of these dynamics remains poorly understood. Here we test whether variability in stimulus-evoked activity can be interpreted within the framework of criticality, which postulates dynamics of neural systems to be tuned towards the phase transition between stability and instability as is reflected in scale-free fluctuations in spontaneous neural activity. Using a novel non-invasive approach in 33 male participants, we tracked instantaneous cortical excitability by inferring the magnitude of excitatory post-synaptic currents from the N20 component of the somatosensory evoked potential. Fluctuations of cortical excitability demonstrated long-range temporal dependencies decaying according to a power law across trials - a hallmark of systems at critical states. As these dynamics covaried with changes in pre-stimulus oscillatory activity in the alpha band (8-13 Hz), we establish a mechanistic link between ongoing and evoked activity through cortical excitability and argue that the co-emergence of common temporal power laws may indeed originate from neural networks poised close to a critical state. In contrast, no signatures of criticality were found in subcortical or peripheral nerve activity. Thus, criticality may represent a parsimonious organizing principle of variability in stimulus-related brain processes on a cortical level, possibly reflecting a delicate equilibrium between robustness and flexibility of neural responses to external stimuli. Significance StatementVariability of neural responses in primary sensory areas is puzzling, as it is detrimental to the exact mapping between stimulus features and neural activity. However, such variability can be beneficial for information processing in neural networks if it is of a specific nature, namely if dynamics are poised at a so-called critical state characterized by a scale-free spatio-temporal structure. Here, we demonstrate the existence of a link between signatures of criticality in ongoing and evoked activity through cortical excitability, which fills the long-standing gap between two major directions of research on neural variability: The impact of instantaneous brain states on stimulus processing on the one hand and the scale-free organization of spatio-temporal network dynamics of spontaneous activity on the other.

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Eye contact in active and passive viewing: event-related brain potential evidence from a combined eye tracking and EEG study

Eye contact is a salient social cue which is assumed to influence early brain processes involved in face perception. The N170 component in the event-related potential (ERP) has frequently been reported to be larger to faces with an averted rather than direct gaze towards the observer. In most studies, however, this effect has been investigated in comparatively artificial, passive settings where participants were instructed to fixate their gaze while observing occasional gaze changes in stimulus faces. Yet, it is unclear whether similar mechanisms are in place during naturalistic gaze interactions involving the continuous interplay of directed and averted gaze between the communication partners. To fill this gap, we compared passive viewing of gaze change sequences with an active condition where participants own gaze continuously interacted with the gaze of a stimulus face; while recording ERPs and monitoring gaze with eye tracking. In addition, we investigated the relevance of emotional facial expressions for gaze processing. For both passive viewing and active interaction, N170 amplitudes were larger when the gaze of stimulus faces was averted rather than directed at the participants. Furthermore, eye contact decreased P300 amplitudes in both conditions. Emotional facial expression influenced N170 amplitudes but did not elicit an early posterior negativity nor did it interact with gaze direction. We conclude that comparable mechanisms of gaze perception are in place in gaze interaction as compared to passive viewing, encouraging the further study of the eye contact effect in naturalistic settings.

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