High-density EEG during electroconvulsive therapy-induced seizures and other brain states: scalp potentials are global and highly multipolar

Introduction

Electroconvulsive therapy (ECT) drives the brain into a brief period of intense activity, allowing dynamical patterns to emerge in a safe and controlled environment. This makes the induced seizure a rare experimental window through which large-scale principles of brain organization are more accessible than in ordinary resting or task states. Despite the clinical importance and scientific opportunities that ECT provides, few studies have examined ECT seizures using multi-channel EEG[1,2], with emphasis on studying waveform evolution and statistical relations rather than explicitly spatial. Spatial organization of the seizure over the whole scalp remains largely undescribed.

Methods

We recruited 33 depressed patients (17 male, 16 female, median age 38 years, 31 unipolar, 2 bipolar depressed), who received ECT for clinical reasons (n=32 bifrontal stimulation, n=3 right unilateral stimulation, restimulation in 2 cases). High-density EEG (60-channels, 1000 Hz) was measured in five different states: prior to anesthesia (resting state, eyes open/closed), immediately before stimulation (during anesthesia), during the seizure, and throughout the subsequent postictal period. ECT was done under anaesthesia (propofol/etomidate, and add-on remifentanil), and muscle relaxation (succinylcholine). EEGs were high-pass filtered @ 0.125Hz and notch filters applied. Quantitative definitions based on global field power were used to locate segments corresponding to the 5 states. Electrode quality control used instantaneous time-derivative methods. At each timepoint, we fit spherical harmonic modes to measurements, contrasting them with fits to random shapes with the same number of degrees of freedom in order to measure statistical significance. Perturbative electro-quasistatics is used to estimate source depth[3].

Results

Scalp EEG is well-described by a compact set of spatial patterns. At most moments in time, the seizure voltage map assumes the shape of two spheres, touching edge-to-edge, with opposite voltage polarities, with a preferential alignment along the anterior-posterior axis. Fits to the multipole pattern set are strong (Rˆ2=[0.60-96]) and highly significant (dipole confidence level z>9.3, quadrupole z>3.8). Across the entire cohort, across the course of all seizures, the pattern is dominated by the ℓ=1 dipole (edge-to-edge spheres shape), followed by the ℓ=2 quadrupole, along with higher-order modes. In some patients we successfully resolved global structure up to ℓ=6, corresponding to variance as low as ∼0.1µV. Contrasting the relative strengths of dipole to quadrupole modes during and outside of the ictal stage, we argue that the source center-of-mass is deeper ictally than pre-ictally in 29/35 seizures.Bifrontally vs. unilaterally-evoked seizures show no significant differences in spatial patterns nor orientations.

Conclusions

In both seizure and non-seizure states, a significant component of scalp EEG consists of global spatial spherical harmonic patterns whose relative time-varying amplitudes change as sources change. The source center-of-mass is on average deeper during the ictal phase for most seizures. Spherical harmonic fitting provides a physically interpretable spatial spectrum which complements conventional temporal spectral analysis with a compact spatial description, and provides a route to probe depth and structure of brain activity in and out of seizures using scalp EEG.

References

References:

1. R. Brumback, R. Staton, 1982, The electroencephalographic pattern during electroconvulsive therapy. Clinical Electroencephalography, 13(3):148–153,
2. R. Hogan, E. Trammel, N. Farber, M. Avidan, and B. Julian A. Palanca., 2019 Central- positive complexes: A novel characterization of ictal markers induced during electroconvulsive therapy. The Journal ofECT, 35(4):e39–e45
3. J. Jackson, Classical Electrodynamics 3rd Edition, 1999, Wiley