Non-invasive Brain Stimulation: A Paradigm Shift in Understanding Brain Oscillations

Johannes Vosskuhl, Daniel Strüber, Christoph S Herrmann, Johannes Vosskuhl, Daniel Strüber, Christoph S Herrmann

Abstract

Cognitive neuroscience set out to understand the neural mechanisms underlying cognition. One central question is how oscillatory brain activity relates to cognitive processes. Up to now, most of the evidence supporting this relationship was correlative in nature. This situation changed dramatically with the recent development of non-invasive brain stimulation (NIBS) techniques, which open up new vistas for neuroscience by allowing researchers for the first time to validate their correlational theories by manipulating brain functioning directly. In this review, we focus on transcranial alternating current stimulation (tACS), an electrical brain stimulation method that applies sinusoidal currents to the intact scalp of human individuals to directly interfere with ongoing brain oscillations. We outline how tACS can impact human brain oscillations by employing different levels of observation from non-invasive tACS application in healthy volunteers and intracranial recordings in patients to animal studies demonstrating the effectiveness of alternating electric fields on neurons in vitro and in vivo. These findings likely translate to humans as comparable effects can be observed in human and animal studies. Neural entrainment and plasticity are suggested to mediate the behavioral effects of tACS. Furthermore, we focus on mechanistic theories about the relationship between certain cognitive functions and specific parameters of brain oscillaitons such as its amplitude, frequency, phase and phase coherence. For each of these parameters we present the current state of testing its functional relevance by means of tACS. Recent developments in the field of tACS are outlined which include the stimulation with physiologically inspired non-sinusoidal waveforms, stimulation protocols which allow for the observation of online-effects, and closed loop applications of tACS.

Keywords: brain oscillations; causality; mechanisms of tACS; non-invasive brain stimulation; transcranial alternating current stimulation.

Figures

Figure 1
Figure 1
Different forms of non-invasive brain stimulation (NIBS). The left panel depicts a sketch of the respective application. The inlays show the voltage between the electrodes over time. The gray areas depict simplified electric field distributions in which the target area should be located. The right panel represents the stimulation signal (green) relative to EEG (black) from a potential target area. (A) Transcranial direct current stimulation (tDCS) via externally attached electrodes. (B) Transcranial alternating current stimulation (tACS). (C) Transcranial random noise stimulation (tRNS). (D) (Repetetive) transcranial magnetic stimulation (TMS).
Figure 2
Figure 2
Explanatory levels of brain stimulation with alternating currents. Black rectangles (A) and needles (B–D) depict the stimulation electrodes. Gray areas illustrate the electric fields between the electrodes. (A) Stimulation of the human brain. Most restricted in the insights into the neural dynamics and stimulation parameters but most relevant for the observation of cognitive effects. Most often, non-invasive but also invasive recordings and stimulation have been used. (B) Invasive stimulation of animals allows for more precise and controlled stimulation and accurate recordings. Only limited observation of cognitive effects of stimulation is possible. (C) Stimulation of brain slices or cell assemblies. Highly controlled stimulation and recording are possible. Network effects of stimulation can be observed but no behavior. (D) Stimulation of a single neuron. Observations of the effect of alternating currents on different parts of the neuron down to the single iron channel or synapse are possible.
Figure 3
Figure 3
Arnold Tongue. The horizontal axis represents the stimulation frequency with smaller () stimulation frequencies relative to the endogenous frequency. The vertical axis shows the stimulation intensity. The inlays depict the relationship between the endogenous (e.g., EEG, black) and stimulation signal (red). Note how the stimulation signal increases in amplitude from bottom to top and how its frequency relates to the EEG signal. During stimulation, the endogenous oscillation couples in phase and frequency to the stimulation signal (entrainment) in cases inside of the Arnold Tongue (dark gray area) and stays unmodulated out of the Arnold Tongue (light gray area). When the stimulation frequency is identical with the endogenous frequency, even low stimulation intensities lead to a coupling of the two oscillations (central, lower inlay). The same intensity does not lead to entrainment, when the stimulation frequency is not matched to the endogenous frequency (lower left and right inlays). If, however, the intensity is increased, these non-matched frequencies do lead to entrainment (upper left and right inlays).
Figure 4
Figure 4
Different tACS designs and their effects on EEG measures. The left panel shows the electrode montage, simplified electric fields between electrodes (gray) and inlays with the stimulation signal (red) relative to the EEG (black). (A) External current is applied at the natural frequency. As a result in the frequency spectrum, the amplitude of the natural frequency (black) increases due to entrainment (green). (B) Alternating currents is applied at a frequency slightly above the natural frequency. The effect is a shift of the natural frequency to the tACS frequency. (C) Current is applied at the natural frequency. The phase of the natural frequency synchronizes to the phase of tACS and is more regular during stimulation. (D) When three electrodes are used, one can be connected to one pole and the other two to the other pole of the stimulation device. Thereby, the phase underneath the coupled electrodes is the same and areas underneath will synchronize their endogenous phases to the tACS.

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