Julian Keil

Now I am Ready—Now I am not: The Influence of Pre-TMS Oscillations and Corticomuscular Coherence on Motor-Evoked Potentials

There is a growing body of research on the functional role of oscillatory brain activity. However, its relation to functional connectivity has remained largely obscure. In the sensorimotor system, movement-related changes emerge in the α (8-14 Hz) and β (15-30 Hz) range (event-related desynchronization, ERD, before and during movement; event-related synchronization, ERS, after movement offset). Some studies suggest that β-ERS may functionally inhibit new movements. According to the gating-by-inhibition framework ( Jensen and Mazaheri 2010), we expected that the ERD would go along with increased corticomuscular coupling, and vice versa. By combining transcranial magnetic stimulation (TMS) and electroencephalography, we were directly able to test this hypothesis. In a reaction time task, single TMS pulses were delivered randomly during ERD/ERS to the motor cortex. The motor-evoked potential (MEP) was then related to the β and α frequencies and corticomuscular coherence. Results indicate that MEPs are smaller when preceded by high pre-TMS β-band power and low pre-TMS α-band corticomuscular coherence (and vice versa) in a network of motor-relevant areas comprising frontal, parietal, and motor cortices. This confirms that an increase in rhythms that putatively reflect functionally inhibited states goes along with weaker coupling of the respective brain regions.

Prestimulus Beta Power and Phase Synchrony Influence the Sound-Induced Flash Illusion

We investigated the sound-induced flash illusion, an example for the influence of auditory information on visual perception. It consists of the perception of 2 visual stimuli upon the presentation of a single visual stimulus alongside 2 auditory stimuli. We used magnetoencephalography to assess the influence of prestimulus oscillatory activity on varying the perception of invariant stimuli. We compared cortical activity from trials in which subjects perceived an illusion with trials in which subjects did not perceive the illusion, keeping the stimulation fixed. Subjects perceived the illusion in approximately 50% of trials. Prior to the illusion, we found stronger beta-band power in left temporal sensors, localized to the left middle temporal gyrus. Illusory perceptions were preceded by increased beta-band phase synchrony between the left middle temporal gyrus and auditory areas as well as by decreased phase synchrony with visual areas. Alpha-band phase synchrony between visual and temporal, parietal, and frontal cortical areas as well as alpha-band phase synchrony between auditory and visual areas were modulated. This supports and extends reports on the influence of brain states prior to stimulation on subsequent perception. We suggest that prestimulus local and network activities form predispositions if sensory streams will be integrated.

Cortical Brain States and Corticospinal Synchronization Influence TMS-evoked motor potentials

Transcranial magnetic stimulation (TMS) influences cortical processes. Recent findings indicate, however, that, in turn, the efficacy of TMS depends on the state of ongoing cortical oscillations. Whereas power and phase of electromyographic (EMG) activity recorded from the hand muscles as well as neural synchrony between cortex and hand muscles are known to influence the effect of TMS, to date, no study has shown an influence of the phase of cortical oscillations during wakefulness. We applied single-pulse TMS over the motor cortex and recorded motor-evoked potentials along with the electroencephalogram (EEG) and EMG. We correlated phase and power of ongoing EEG and EMG signals with the motor-evoked potential (MEP) amplitude. We also investigated the functional connectivity between cortical and hand muscle activity (corticomuscular coherence) with the MEP amplitude. EEG and EMG power and phase in a frequency band around 18 Hz correlated with the MEP amplitude. High beta-band (∼34 Hz) corticomuscular coherence exhibited a positive linear relationship with the MEP amplitude, indicating that strong synchrony between cortex and hand muscles at the moment when TMS is applied entails large MEPs. Improving upon previous studies, we demonstrate a clear dependence of TMS-induced motor effects on the state of ongoing EEG phase and power fluctuations. We conclude that not only the sampling of incoming information but also the susceptibility of cortical communication flow depends cyclically on neural phase.

Motor intention determines sensory attenuation of brain responses to self-initiated sounds

One of the functions of the brain is to predict sensory consequences of our own actions. In auditory processing, self-initiated sounds evoke a smaller brain response than passive sound exposure of the same sound sequence. Previous work suggests that this response attenuation reflects a predictive mechanism to differentiate the sensory consequences of ones own actions from other sensory input, which seems to form the basis for the sense of agency (recognizing oneself as the agent of the movement). This study addresses the question whether attenuation of brain responses to self-initiated sounds can be explained by brain activity involved in movement planning rather than movement execution. We recorded ERPs in response to sounds initiated by button presses. In one condition, participants moved a finger to press the button voluntarily, whereas in another condition, we initiated a similar, but involuntary, finger movement by stimulating the corresponding region of the primary motor cortex with TMS. For involuntary movements, no movement intention (and no feeling of agency) could be formed; thus, no motor plans were available to the forward model. A portion of the brain response evoked by the sounds, the N1-P2 complex, was reduced in amplitude following voluntary, self-initiated movements, but not following movements initiated by motor cortex stimulation. Our findings demonstrate that movement intention and the corresponding feeling of agency determine sensory attenuation of brain responses to self-initiated sounds. The present results support the assumptions of a predictive internal forward model account operating before primary motor cortex activation.

The role of alpha oscillations for illusory perception.

Highlights • We review studies showing a crucial role of alpha oscillations for illusory perception.• Power and/or phase of alpha oscillations influence illusory perception.• Alpha oscillations influence visual, auditory and multisensory illusions.• Modulations of alpha oscillations are found before and/or during illusory perception.

GABA concentration in superior temporal sulcus predicts gamma power and perception in the sound-induced flash illusion

In everyday life we are confronted with inputs of multisensory stimuli that need to be integrated across our senses. Individuals vary considerably in how they integrate multisensory information, yet the neurochemical foundations underlying this variability are not well understood. Neural oscillations, especially in the gamma band (>30Hz) play an important role in multisensory processing. Furthermore, gamma-aminobutyric acid (GABA) neurotransmission contributes to the generation of gamma band oscillations (GBO), which can be sustained by activation of metabotropic glutamate receptors. Hence, differences in the GABA and glutamate systems might contribute to individual differences in multisensory processing. In this combined magnetic resonance spectroscopy and electroencephalography study, we examined the relationships between GABA and glutamate concentrations in the superior temporal sulcus (STS), source localized GBO, and illusion rate in the sound-induced flash illusion (SIFI). In 39 human volunteers we found robust relationships between GABA concentration, GBO power, and the SIFI perception rate (r-values=0.44 to 0.53). The correlation between GBO power and SIFI perception rate was about twofold higher when the modulating influence of the GABA level was included in the analysis as compared to when it was excluded. No significant effects were obtained for glutamate concentration. Our study suggests that the GABA level shapes individual differences in audiovisual perception through its modulating influence on GBO. GABA neurotransmission could be a promising target for treatment interventions of multisensory processing deficits in clinical populations, such as schizophrenia or autism.

The strength of alpha and beta oscillations parametrically scale with the strength of an illusory auditory percept

Studies investigating the role of oscillatory activity in sensory perception are primarily conducted in the visual domain, while the contribution of oscillatory activity to auditory perception is heavily understudied. The objective of the present study was to investigate macroscopic (EEG) oscillatory brain response patterns that contribute to an auditory (Zwicker tone, ZT) illusion. Three different analysis approaches were chosen: 1) a parametric variation of the ZT illusion intensity via three different notch widths of the ZT-inducing noise; 2) contrasts of high-versus-low-intensity ZT illusion trials, excluding physical stimuli differences; 3) a representational similarity analysis to relate source activity patterns to loudness ratings. Depending on the analysis approach, levels of alpha to beta activity (10-20Hz) reflected illusion intensity, mainly defined by reduced power levels co-occurring with stronger percepts. Consistent across all analysis approaches, source level analysis implicated auditory cortices as main generators, providing evidence that the activity level in the alpha and beta range - at least in part - contributes to the strength of the illusory auditory percept. This study corroborates the notion that alpha to beta activity in the auditory cortex is linked to functionally similar states, as has been proposed for visual, somatosensory and motor regions. Furthermore, our study provides certain theoretical implications for pathological auditory conscious perception (tinnitus).

You can't stop the music: reduced auditory alpha power and coupling between auditory and memory regions facilitate the illusory perception of music during noise.

Our brain has the capacity of providing an experience of hearing even in the absence of auditory stimulation. This can be seen as illusory conscious perception. While increasing evidence postulates that conscious perception requires specific brain states that systematically relate to specific patterns of oscillatory activity, the relationship between auditory illusions and oscillatory activity remains mostly unexplained. To investigate this we recorded brain activity with magnetoencephalography and collected intracranial data from epilepsy patients while participants listened to familiar as well as unknown music that was partly replaced by sections of pink noise. We hypothesized that participants have a stronger experience of hearing music throughout noise when the noise sections are embedded in familiar compared to unfamiliar music. This was supported by the behavioral results showing that participants rated the perception of music during noise as stronger when noise was presented in a familiar context. Time-frequency data show that the illusory perception of music is associated with a decrease in auditory alpha power pointing to increased auditory cortex excitability. Furthermore, the right auditory cortex is concurrently synchronized with the medial temporal lobe, putatively mediating memory aspects associated with the music illusion. We thus assume that neuronal activity in the highly excitable auditory cortex is shaped through extensive communication between the auditory cortex and the medial temporal lobe, thereby generating the illusion of hearing music during noise.

Early and late beta-band power reflect audiovisual perception in the McGurk illusion

The McGurk illusion is a prominent example of audiovisual speech perception and the influence that visual stimuli can have on auditory perception. In this illusion, a visual speech stimulus influences the perception of an incongruent auditory stimulus, resulting in a fused novel percept. In this high-density electroencephalography (EEG) study, we were interested in the neural signatures of the subjective percept of the McGurk illusion as a phenomenon of speech-specific multisensory integration. Therefore, we examined the role of cortical oscillations and event-related responses in the perception of congruent and incongruent audiovisual speech. We compared the cortical activity elicited by objectively congruent syllables with incongruent audiovisual stimuli. Importantly, the latter elicited a subjectively congruent percept: the McGurk illusion. We found that early event-related responses (N1) to audiovisual stimuli were reduced during the perception of the McGurk illusion compared with congruent stimuli. Most interestingly, our study showed a stronger poststimulus suppression of beta-band power (13-30 Hz) at short (0-500 ms) and long (500-800 ms) latencies during the perception of the McGurk illusion compared with congruent stimuli. Our study demonstrates that auditory perception is influenced by visual context and that the subsequent formation of a McGurk illusion requires stronger audiovisual integration even at early processing stages. Our results provide evidence that beta-band suppression at early stages reflects stronger stimulus processing in the McGurk illusion. Moreover, stronger late beta-band suppression in McGurk illusion indicates the resolution of incongruent physical audiovisual input and the formation of a coherent, illusory multisensory percept.

Distinct patterns of local oscillatory activity and functional connectivity underlie intersensory attention and temporal prediction

Intersensory attention (IA) describes our ability to attend to stimuli of one sensory modality, while disregarding other modalities. Temporal prediction (TP) describes the process of directing attention to specific moments in time. Both attention mechanisms facilitate sensory stimulus processing, yet it is not understood whether they rely on common or distinct network patterns. In this electroencephalography (EEG) study, we presented auditory cues followed by visuo-tactile stimuli. The cues indicated whether participants should detect visual or tactile targets in the visuo-tactile stimuli. TP was manipulated by presenting stimuli block-wise at fixed or variable inter-stimulus intervals. We analysed power and functional connectivity of source-projected oscillations. We computed graph theoretical measures to identify networks underlying IA and TP. Participants responded faster when stimuli were presented with fixed compared to variable inter-stimulus intervals, demonstrating a facilitating effect of TP. Distinct patterns of local delta-, alpha-, and beta-band power modulations and differential functional connectivity in the alpha- and beta-bands reflected the influence of IA and TP. An interaction between IA and TP was found in theta-band connectivity in a network comprising frontal, somatosensory and parietal areas. Our study provides insights into how IA and TP dynamically shape oscillatory power and functional connectivity to facilitate stimulus processing.