Modulating brain oscillations to drive brain function

Do neuronal oscillations play a causal role in brain function? In a study in this issue of PLOS Biology, Helfrich and colleagues address this long-standing question by attempting to drive brain oscillations using transcranial electrical current stimulation. Remarkably, they were able to manipulate visual perception by forcing brain oscillations of the left and right visual hemispheres into synchrony using oscillatory currents over both hemispheres. Under this condition, human observers more often perceived an inherently ambiguous visual stimulus in one of its perceptual instantiations. These findings shed light on the mechanisms underlying neuronal computation. They show that it is the neuronal oscillations that drive the visual experience, not the experience driving the oscillations. And they indicate that synchronized oscillatory activity groups brain areas into functional networks. This points to new ways for controlled experimental and possibly also clinical interventions for the study and modulation of brain oscillations and associated functions

Alpha power increase after transcranial alternating current stimulation at alpha frequency (α-tacs) reflects plastic changes rather than entrainment

Background: Periodic stimulation of occipital areas using transcranial alternating current stimulation (tACS) at alpha (α) frequency (8–12 Hz) enhances electroencephalographic (EEG) α-oscillation long after tACS-offset. Two mechanisms have been suggested to underlie these changes in oscillatory EEG activity: tACS-induced entrainment of brain oscillations and/or tACS-induced changes in oscillatory circuits by spike-timing dependent plasticity.<p></p> Objective: We tested to what extent plasticity can account for tACS-aftereffects when controlling for entrainment “echoes.” To this end, we used a novel, intermittent tACS protocol and investigated the strength of the aftereffect as a function of phase continuity between successive tACS episodes, as well as the match between stimulation frequency and endogenous α-frequency.<p></p> Methods: 12 healthy participants were stimulated at around individual α-frequency for 15–20 min in four sessions using intermittent tACS or sham. Successive tACS events were either phase-continuous or phase-discontinuous, and either 3 or 8 s long. EEG α-phase and power changes were compared after and between episodes of α-tACS across conditions and against sham.<p></p> Results: α-aftereffects were successfully replicated after intermittent stimulation using 8-s but not 3-s trains. These aftereffects did not reveal any of the characteristics of entrainment echoes in that they were independent of tACS phase-continuity and showed neither prolonged phase alignment nor frequency synchronization to the exact stimulation frequency.<p></p> Conclusion: Our results indicate that plasticity mechanisms are sufficient to explain α-aftereffects in response to α-tACS, and inform models of tACS-induced plasticity in oscillatory circuits. Modifying brain oscillations with tACS holds promise for clinical applications in disorders involving abnormal neural synchrony

Behavioural evidence for separate mechanisms of audiovisual temporal binding as a function of leading sensory modality

The ability to integrate auditory and visual information is critical for effective perception and interaction with the environment, and is thought to be abnormal in some clinical populations. Several studies have investigated the time window over which audiovisual events are integrated, also called the temporal binding window, and revealed asymmetries depending on the order of audiovisual input (i.e. the leading sense). When judging audiovisual simultaneity, the binding window appears narrower and non-malleable for auditory-leading stimulus pairs and wider and trainable for visual-leading pairs. Here we specifically examined the level of independence of binding mechanisms when auditory-before-visual vs. visual-before-auditory input is bound. Three groups of healthy participants practiced audiovisual simultaneity detection with feedback, selectively training on auditory-leading stimulus pairs (group 1), visual-leading stimulus pairs (group 2) or both (group 3). Subsequently, we tested for learning transfer (crossover) from trained stimulus pairs to non-trained pairs with opposite audiovisual input. Our data confirmed the known asymmetry in size and trainability for auditory–visual vs. visual–auditory binding windows. More importantly, practicing one type of audiovisual integration (e.g. auditory–visual) did not affect the other type (e.g. visual–auditory), even if trainable by within-condition practice. Together, these results provide crucial evidence that audiovisual temporal binding for auditory-leading vs. visual-leading stimulus pairs are independent, possibly tapping into different circuits for audiovisual integration due to engagement of different multisensory sampling mechanisms depending on leading sense. Our results have implications for informing the study of multisensory interactions in healthy participants and clinical populations with dysfunctional multisensory integration

Being first matters: topographical representational similarity analysis of ERP signals reveals separate networks for audiovisual temporal binding depending on the leading sense

In multisensory integration, processing in one sensory modality is enhanced by complementary information from other modalities. Inter-sensory timing is crucial in this process as only inputs reaching the brain within a restricted temporal window are perceptually bound. Previous research in the audiovisual field has investigated various features of the temporal binding window (TBW), revealing asymmetries in its size and plasticity depending on the leading input (auditory-visual, AV; visual-auditory, VA). We here tested whether separate neuronal mechanisms underlie this AV-VA dichotomy in humans. We recorded high-density EEG while participants performed an audiovisual simultaneity judgment task including various AV/VA asynchronies and unisensory control conditions (visual-only, auditory-only) and tested whether AV and VA processing generate different patterns of brain activity. After isolating the multisensory components of AV/VA event-related potentials (ERPs) from the sum of their unisensory constituents, we run a time-resolved topographical representational similarity analysis (tRSA) comparing AV and VA ERP maps. Spatial cross-correlation matrices were built from real data to index the similarity between AV- and VA-maps at each time point (500ms window post-stimulus) and then correlated with two alternative similarity model matrices: AVmaps=VAmaps vs. AVmaps≠VAmaps. The tRSA results favored the AVmaps≠VAmaps model across all time points, suggesting that audiovisual temporal binding (indexed by synchrony perception) engages different neural pathways depending on the leading sense. The existence of such dual route supports recent theoretical accounts proposing that multiple binding mechanisms are implemented in the brain to accommodate different information parsing strategies in auditory and visual sensory systems

Lasting EEG/MEG aftereffects on human brain oscillations after rhythmic transcranial brain stimulation: Level of control over oscillatory network activity

A number of rhythmic protocols have emerged for non-invasive brain stimulation (NIBS) in humans, including transcranial alternating current stimulation (tACS), oscillatory transcranial direct current stimulation (otDCS) and repetitive (also called rhythmic) transcranial magnetic stimulation (rTMS). With these techniques, it is possible to match the frequency of the externally applied electromagnetic fields to the intrinsic frequency of oscillatory neural population activity ("frequency-tuning"). Mounting evidence suggests that by this means tACS, otDCS, and rTMS can entrain brain oscillations and promote associated functions in a frequency-specific manner, in particular during (i.e. online to) stimulation. Here, we focus instead on the changes in oscillatory brain activity that persist after the end of stimulation. Understanding such aftereffects in healthy participants is an important step for developing these techniques into potentially useful clinical tools for the treatment of specific patient groups. Reviewing the electrophysiological evidence in healthy participants, we find aftereffects on brain oscillations to be a common outcome following tACS/otDCS and rTMS. However, we did not find a consistent, predictable pattern of aftereffects across studies, which is in contrast to the relative homogeneity of reported online effects. This indicates that aftereffects are partially dissociated from online, frequency-specific (entrainment) effects during tACS/otDCS and rTMS. We outline possible accounts and future directions for a better understanding of the link between online entrainment and offline aftereffects, which will be key for developing more targeted interventions into oscillatory brain activity

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

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 visuo-motor coordination during pointing as well as to after-effects 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 characterise PA after-effects by using an approach that allows distinguishing between effects on attentional and motor processes. We recorded electroencephalography (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 after-effects 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 occipito-parietal 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 visuo-motor rather than attentional visuo-spatial processes underlie the PA after-effect of rightward deviating prisms in healthy participants

Noninvasive brain stimulation techniques can modulate cognitive processing

Recent methods that allow a noninvasive modulation of brain activity are able to modulate human cognitive behavior. Among these methods are transcranial electric stimulation and transcranial magnetic stimulation that both come in multiple variants. A property of both types of brain stimulation is that they modulate brain activity and in turn modulate cognitive behavior. Here, we describe the methods with their assumed neural mechanisms for readers from the economic and social sciences and little prior knowledge of these techniques. Our emphasis is on available protocols and experimental parameters to choose from when designing a study. We also review a selection of recent studies that have successfully applied them in the respective field. We provide short pointers to limitations that need to be considered and refer to the relevant papers where appropriate

Predictive entrainment of natural speech through two fronto-motor top-down channels

Natural communication between interlocutors is enabled by the ability to predict upcoming speech in a given context. Previously we showed that these predictions rely on a fronto-motor top-down control of low-frequency oscillations in auditory-temporal brain areas that track intelligible speech. However, a comprehensive spatio-temporal characterisation of this effect is still missing. Here, we applied transfer entropy to source-localised MEG data during continuous speech perception. First, at low frequencies (1–4 Hz, brain delta phase to speech delta phase), predictive effects start in left fronto-motor regions and progress to right temporal regions. Second, at higher frequencies (14–18 Hz, brain beta power to speech delta phase), predictive patterns show a transition from left inferior frontal gyrus via left precentral gyrus to left primary auditory areas. Our results suggest a progression of prediction processes from higher-order to early sensory areas in at least two different frequency channels

Visual cortex responses reflect temporal structure of continuous quasi-rhythmic sensory stimulation

Neural processing of dynamic continuous visual input, and cognitive influences thereon, are frequently studied in paradigms employing strictly rhythmic stimulation. However, the temporal structure of natural stimuli is hardly ever fully rhythmic but possesses certain spectral bandwidths (e.g. lip movements in speech, gestures). Examining periodic brain responses elicited by strictly rhythmic stimulation might thus represent ideal, yet isolated cases. Here, we tested how the visual system reflects quasi-rhythmic stimulation with frequencies continuously varying within ranges of classical theta (4–7Hz), alpha (8–13Hz) and beta bands (14–20Hz) using EEG. Our findings substantiate a systematic and sustained neural phase-locking to stimulation in all three frequency ranges. Further, we found that allocation of spatial attention enhances EEG-stimulus locking to theta- and alpha-band stimulation. Our results bridge recent findings regarding phase locking (“entrainment”) to quasi-rhythmic visual input and “frequency-tagging” experiments employing strictly rhythmic stimulation. We propose that sustained EEG-stimulus locking can be considered as a continuous neural signature of processing dynamic sensory input in early visual cortices. Accordingly, EEG-stimulus locking serves to trace the temporal evolution of rhythmic as well as quasi-rhythmic visual input and is subject to attentional bias