Understanding the effects of cortical gyrification in tACS: insights from experiments and computational models

Abstract

The alpha rhythm is often associated with relaxed wakefulness or idling and is altered by various factors. Abnormalities in the alpha rhythm have been linked to several neurological and psychiatric disorders, including Alzheimer's disease. Transcranial alternating current stimulation (tACS) has been proposed as a potential tool to restore a disrupted alpha rhythm in the brain by stimulating at the individual alpha frequency (IAF), although some research has produced contradictory results. In this study, we applied an IAF-tACS protocol over parieto-occipital areas to a sample of healthy subjects and measured its effects over the power spectra. Additionally, we used computational models to get a deeper understanding of the results observed in the experiment. Both experimental and numerical results showed an increase in alpha power of 8.02% with respect to the sham condition in a widespread set of regions in the cortex, excluding some expected parietal regions. This result could be partially explained by taking into account the orientation of the electric field with respect to the columnar structures of the cortex, showing that the gyrification in parietal regions could generate effects in opposite directions (hyper-/depolarization) at the same time in specific brain regions. Additionally, we used a network model of spiking neuronal populations to explore the effects that these opposite polarities could have on neural activity, and we found that the best predictor of alpha power was the average of the normal components of the electric field. To sum up, our study sheds light on the mechanisms underlying tACS brain activity modulation, using both empirical and computational approaches. Non-invasive brain stimulation techniques hold promise for treating brain disorders, but further research is needed to fully understand and control their effects on brain dynamics and cognition. Our findings contribute to this growing body of research and provide a foundation for future studies aimed at optimizing the use of non-invasive brain stimulation in clinical settings.

Individual alpha frequency tACS reduces functional connectivity across the default mode network

“…Aligned with the previous explanation for the FC reductions, tACS could introduce non-uniform phase distributions in the cortex, favouring a decoupling of phases and envelopes, but still entrain the activity of the neuronal populations in the same stimulation frequency. This would consequently increase the activity within the frequency range, increasing power 18,20 but reducing FC as shown previously.…”

“…Lastly, we aimed to study the relationship between the FC ratios and simultaneous alterations in relative power given the previously suggested capacity of tACS to alter power 18 . To do this, we performed a Pearson's correlation between the FC ratio of those DMN links that showed significant differences in the stim-sham comparison after FDR correction, and the ratio of IAF ± 2 relative power of the regions that make up the link (e.g.…”

“…We performed an ad-hoc theoretical analysis to investigate the potential effects of cortical morphology over FC modulation. Given our current stimulation protocol and cortical folding, the neurons of certain regions may receive the stimulation in antiphase, as the electric field direction may result anti-parallel to some cortical columns (i.e., hyperpolarizing) and parallel to others 18 (see Figure 7). To evaluate the effect of this phase disparities over FC, we simulated two MEG signals through filtered white noise and calculated their initial connectivity through PLV and AEC.…”

“…In order to understand further these results, we studied the potential interaction of cortical morphology with the stimulation protocol. Given the brain cortical folding, the neurons of certain regions may receive the stimulation in anti-phase, as the electric field direction may result antiparallel to some cortical columns (i.e., hyper-polarizing effect) and parallel to others 18 (see Figure 7). Therefore, we performed a theoretical experiment by introducing phase disparities in two simulated MEG signals and measuring the resulting FC.…”

“…the synchronization of an oscillatory system to an external driver) at the frequency of stimulation 14 . The anatomical and functional complexity of the brain makes the results of neuromodulation highly dependent on the protocol employed 15 , but it has been observed that entrainment is more likely to occur if the stimulation frequency matches the frequency of the ongoing oscillation 16 and if the anatomy of the target region is taken into account 17,18 .…”