Transcranial alternating current stimulation enhances individual alpha activity in human EEG

Abstract

Non-invasive electrical stimulation of the human cortex by means of transcranial direct current stimulation (tDCS) has been instrumental in a number of important discoveries in the field of human cortical function and has become a well-established method for evaluating brain function in healthy human participants. Recently, transcranial alternating current stimulation (tACS) has been introduced to directly modulate the ongoing rhythmic brain activity by the application of oscillatory currents on the human scalp. Until now the efficiency of tACS in modulating rhythmic brain activity has been indicated only by inference from perceptual and behavioural consequences of electrical stimulation. No direct electrophysiological evidence of tACS has been reported. We delivered tACS over the occipital cortex of 10 healthy participants to entrain the neuronal oscillatory activity in their individual alpha frequency range and compared results with those from a separate group of participants receiving sham stimulation. The tACS but not the sham stimulation elevated the endogenous alpha power in parieto-central electrodes of the electroencephalogram. Additionally, in a network of spiking neurons, we simulated how tACS can be affected even after the end of stimulation. The results show that spike-timing-dependent plasticity (STDP) selectively modulates synapses depending on the resonance frequencies of the neural circuits that they belong to. Thus, tACS influences STDP which in turn results in aftereffects upon neural activity.The present findings are the first direct electrophysiological evidence of an interaction of tACS and ongoing oscillatory activity in the human cortex. The data demonstrate the ability of tACS to specifically modulate oscillatory brain activity and show its potential both at fostering knowledge on the functional significance of brain oscillations and for therapeutic application.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Stimulation details and results.

A: Location of stimulation and EEG electrodes: The tACS electrodes were placed bilaterally over the occipital cortex (PO9, PO10, international 10/10 system); EEG is measured from parieto-occipital midline electrodes CPz, Pz, and POz. B: Timeline of experimental events: The experiment started with the determination of the individual alpha frequency during a 1-minute period in which the participants were in a relaxed state with eyes closed followed by an evaluation of an individual phosphene threshold. Subsequently, the participants performed a simple detection task for 16 minutes. During this period, EEG recording was stopped after 3 minutes (Pre-measure) and a 10 minute stimulation (either tACS or Sham) was given, followed by a further 3 minute EEG recording (Post-measure). C: Group averaged EEG activity: Average FFT power spectra for the 3 minute intervals preceding (pre, dotted line) and following (post, solid line) the stimulation condition separately for the tACS-group (left) and the Sham-group (right). D: mean individual alpha amplitude for tACS and sham group: There is an increase in individual alpha power from pre- to post-stimulus measurement in the subjects that received tACS (solid line), but not for the subjects that received sham-stimulation (dotted line). No tACS related alpha modulation can be observed in the upper and lower frequency band. Data are normalized to the pre-stimulation alpha power. Asterisks indicate statistical significance. Data are the means ±s.e.m.

Figure 2. Network simulation of tACS.

A: Spike timing dependent plasticity: synaptic weights are increased if a post-synaptic potential follows a pre-synaptic spike (long-term potentiation, LTP) and decreased if a post-synaptic potential occurs prior to a pre-synaptic spike (long-term depression, LTD). B: Schematic illustration of the network: A driving neuron establishes a recurrent loop with each neuron of a hidden layer. The total synaptic delay, Δt, (i.e., the sum of both delays of the loop) varied between 20 and 160 ms. The driving neuron was stimulated with a spike train of 10 Hz repetition rate. C: Synaptic weights of the back-projection as a function of the total synaptic delay of the recurrent loops: Grey dots display synaptic weights at the start of the simulation, black dots represent synaptic weights after the end of simulation. External stimulation of the driving neuron at 10 Hz resulted in increased weights for recurrent loops with a total delay between 60 and 100 ms, and dramatically reduced synaptic weights for loops with total delays outside this interval. Note, that the highest synaptic weights are observed at 100 ms, i.e., for loops with a resonance frequency near the stimulation frequency.