Abstract
BackgroundTheta-band neuronal oscillations in the prefrontal cortex are associated with several cognitive functions. Oscillatory phase is an important correlate of excitability and phase synchrony mediates information transfer between neuronal populations oscillating at that frequency. The ability to extract and exploit the prefrontal theta rhythm in real time in humans would facilitate insight into neurophysiological mechanisms of cognitive processes involving the prefrontal cortex, and development of brain-state-dependent stimulation for therapeutic applications.ObjectivesWe investigate individual source-space beamforming-based estimation of the prefrontal theta oscillation as a method to target specific phases of the ongoing theta oscillations in the human dorsomedial prefrontal cortex (DMPFC) with real-time EEG-triggered transcranial magnetic stimulation (TMS). Different spatial filters for extracting the prefrontal theta oscillation from EEG signals are compared and additional signal quality criteria are assessed to take into account the dynamics of this cortical oscillation.MethodsTwenty two healthy participants were recruited for anatomical MRI scans and EEG recordings with 18 composing the final analysis. We calculated individual spatial filters based on EEG beamforming in source space. The extracted EEG signal was then used to simulate real-time phase-detection and quantify the accuracy as compared to post-hoc phase estimates. Different spatial filters and triggering parameters were compared. Finally, we validated the feasibility of this approach by actual real-time triggering of TMS pulses at different phases of the prefrontal theta oscillation.ResultsHigher phase-detection accuracy was achieved using individualized source-based spatial filters, as compared to an average or standard Laplacian filter, and also by detecting and avoiding periods of low theta amplitude and periods containing a phase reset. Using optimized parameters, prefrontal theta-phase synchronized TMS of DMPFC was achieved with an accuracy of ±55°.ConclusionThis study demonstrates the feasibility of triggering TMS pulses during different phases of the ongoing prefrontal theta oscillation in real time. This method is relevant for brain state-dependent stimulation in human studies of cognition. It will also enable new personalized therapeutic repetitive TMS protocols for more effective treatment of neuropsychiatric disorders.
Highlights
Synchronous oscillatory activity between neuronal populations allows information exchange and the strengthening of connections through neuroplasticity (Harris et al, 2003; Buzsaki and Draguhn, 2004)
The hippocampal theta oscillation has been found to be significantly phase-locked to the neuronal firing of large populations of neurons in the medial prefrontal cortex (Siapas et al, 2005), with different phases corresponding to different states of excitability
We propose here adaptations to the real-time phase detection method presented previously (Zrenner et al, 2018), in order to account for the characteristics of the prefrontal theta oscillation, and thereby enable real-time EEG-triggered transcranial magnetic stimulation (TMS) targeting of specific phases of the theta oscillation
Summary
Synchronous oscillatory activity between neuronal populations allows information exchange and the strengthening of connections through neuroplasticity (Harris et al, 2003; Buzsaki and Draguhn, 2004) These neuronal oscillations are ubiquitous in the functioning brain cortex and can be observed with the aid of several tools, including non-invasive recordings such as electroencephalography (EEG) and magnetoencephalography. Neuronal spiking has been observed predominantly in specific theta-phases depending on the brain region (Klausberger et al, 2004; Fujisawa and Buzsaki, 2011), with stimulation applied in different phases of theta oscillation yielding differential profiles of neuroplasticity (Pavlides et al, 1988; Holscher et al, 1997; Hyman et al, 2003). The ability to extract and exploit the prefrontal theta rhythm in real time in humans would facilitate insight into neurophysiological mechanisms of cognitive processes involving the prefrontal cortex, and development of brain-statedependent stimulation for therapeutic applications
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