We studied the effects of frontal theta electrical stimulation on multitasking performance, as well as changes in neurophysiological measures associated with tACS effects. The results showed that repeated runs of theta-tACS generates positive effects on multitasking performance accompanied by an offline increase in posterior beta power. Additionally, changes in frontal oscillations positively correlated with changes in multitasking performance. These results suggest that applying frontal theta stimulation increases power in multiple frequencies of brain oscillations related to improved multitasking performance.

tACS effects on multitasking performance and neurophysiological measurements

The present results indicated that low frequency oscillating (i.e. theta) currents introduced extracranially to the brain modulated higher frequency oscillations (i.e. beta oscillations) in brain regions close to and distant from the stimulation sites. This finding corroborates several previous reports. With intracranial recordings, Ozen et al., (2010) demonstrated that weak slow oscillatory stimulation could affect neurons in widespread cortical areas, including regions distant from the site of stimulation. Notably, a larger fraction of neurons were affected as the stimulation intensity increased [43]. It has been proposed that depending on the intensity of the stimulation, neurons distant from the stimulation site can be activated directly via emphatic coupling or indirectly through synaptic connections [44, 45]. A relatively high current density (318.5 μA/cm2) was applied in the present study in comparison to other tACS studies that do not exhibit effects in distant regions or other frequency bands (14.2 μA/cm2~28.6 μA/cm2) [27, 29, 46]. The stimulation electrodes were centered at F3 and F4 of the 10–20 system to be over bilateral dorsolateral prefrontal cortex (DLPFC) [47]. Since there are abundant structural and functional connections between frontal, parietal and visual cortex to direct top-down modulation of sensory activity that mediate bottom-up information processes [48, 49], the distant neurophysiological effects generated by tACS might be a result of the potentiation of these long-range associative connections.

In contrast to previous studies [29, 50, 51], our results suggest that tACS can affect power in a frequency (i.e. beta) other than the stimulating frequency (i.e. theta). Similar cross-frequency modulation has been reported in several other studies [30–32, 52]. Notably, a recent study showed that by applying theta-tACS over parietal regions, alpha power decreases in multiple regions across the whole brain [31]. Indeed, with a repetitive stimulation protocol (five 5-min stimulation runs with 1-min interval in between) and a high current density (517 μA/cm2), Kirov et al., (2009) found a pronounced and widespread power enhancement in theta and beta oscillations after transcranial slow oscillation stimulation at 0.75 Hz. The exact cellular mechanism involved in such a cross-frequency modulation is elusive. However, the similarity between the current findings and the effects observed by Kirov et al., (2009) likewise suggests that repeated runs of oscillatory stimulation with short inter-run-intervals (1-min) and high current density (larger than 300 μA/cm2) may result in general functional neuroplastic effects. Neuroplastic changes have been proposed to be responsible for the after-effects of tACS [28, 53], although an online tACS-induced neural entrainment may be a prerequisite for such plasticity [54]. Ali et al., (2013) demonstrated that periodic perturbation (i.e. 3-Hz stimulation) effectively increased the power of higher harmonics of the resonant frequency (i.e. 6 Hz). Furthermore, the range of the affected frequencies broadened as the stimulation intensity increased [30]. Since the current density of the present study is relatively high, the cross-frequency modulation might be a consequence of network entrainment. An important question for future research is to address the frequency specificity and intensity required to yield the observed effects.

To successfully perform a multitasking challenge, several domains of cognitive control abilities are required, such as sustained attention [55], task switching [56], selective attention [57], and inhibitory control [58]. Given that multitasking is a higher-order cognitive process that involves the integration of processes from many domains of cognitive control abilities, a multi-frequency network may exist to support cognitive subcomponents that contribute to the successful multitasking behavior. The interregional cross-frequency modulation induced by tACS may be the result of enhancing multiple cognitive functions subserving multitasking behavior. Therefore, instead of affecting endogenous brain oscillations in a specific frequency manner, tACS may have generated an overall positive effect on multiple active cognitive networks, which may explain the positive correlations between the improvement of multitasking performance and the enhancement of frontal theta, alpha, and beta power.

Another important open question is what do posterior beta power changes represent in this context. Increased beta activity outside motor-related regions is associated with anticipatory attention processes [38, 39], or maintenance of the current cognitive state [40]. In other words, beta activity is associated with the continuation of the sensorimotor cognitive set by helping endogenous top-down influences manage the effect of impending external events [40]. In the current context, increased beta power may serve to maintain sensorimotor representations of the driving task so that attention may be allocated to the appearance of an impending sign for discrimination without changing concurrent driving performance. The result of the pre-stimulus analysis shows that tACS resulted in an anticipatory change in posterior beta power, which supports the hypothesis that tACS optimized the maintenance of sensorimotor representations that contributes to successful multitasking behavior.

Interestingly, the application of theta tACS over bilateral PFC failed to significantly increase endogenous theta rhythms. One explanation is suggested by studies that have indicated stimulation effects are most efficient when the externally applied frequency is at the intrinsic frequency [29]. However, this possibility seems unlikely in the present study according to our analyses based on baseline peak theta band. As effects of transcranial electrical stimulation on electrophysiological activity critically depend upon the prevailing brain-state [27, 59] and because young adults demonstrate relatively high theta power during multitasking [7], a more plausible explanation to account for this finding is that during multitasking, endogenous theta power has reached a maximal level and cannot be further enhanced (i.e. ceiling effect). Since the effects of non-invasive brain stimulation may be graded across different populations from healthy young adults to physiological aging and pathological conditions [60], it is possible that the effect can be only observed in older adults, clinical populations or younger adults with room to improve. Indeed, this interpretation receives some support from the correlations that show participants who were able to increase theta power exhibited the greatest performance improvements.

Regarding the interpretation of the present results, it is important to note that the lack of a frequency control condition means we offer no direct evidence that the observed behavioral and neurophysiological effects are specifically dependent upon theta-tACS. Similarly, without a control site for stimulation, it is unclear whether these effects are specific to PFC stimulation or whether similar effects may be observed by stimulating other cortical regions. This will be the focus of future research.