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EEG coherence has structure in the millimeter domain: subdural and hippocampal recordings from epileptic patients

https://doi.org/10.1016/0013-4694(95)93347-AGet rights and content
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Abstract

Subdural recordings from 8 patients and depth recordings from 3 patients via rows of electrodes with 5–10 mm spacing were searched for signs of significant local differentiation of coherence calculated between all possible pairs of loci. EEG samples of 2–4 min were taken during 4 states: alertness, stage 2–3 sleep, light surgical anesthesia permitting the patient to respond to questions and electrical seizures. Coherence was computed for all frequencies from 1 to 50 Hz or 0.3–100 Hz; for comparisons the mean coherence over each of 6 or 7 narrower bands between 2 and 70 Hz was used.

Whereas the literature supports the view that EEG coherence is usually substantial over many centimeters, the hypothesis here tested — and found to be well above stochastic expectations — is that significant structure occurs in the millimeter domain for EEG recorded subdurally or within the brain.

In both the subdural surface samples and those from temporal lobe depth electrode arrays coherence declines with distance between electrodes of the pair, on the average quite severely in millimeters. This is nearly the same for all frequency bands. For middle bands like 8–13 and 13–20 Hz, mean coherence typically declines most steeply in the first 10 mm, from values indistinguishable from 1.0 at < 0.5 mm distance to 0.5 at 5–10 mm and to 0.25 in another 10–20 mm in the subdural surface data. Temporal lobe depth estimates decline about half as fast; coherence ≥ 0.5 extends for 9–20 mm and ≥ 0.25 for another 20–35 mm. Low frequency bands (1–5, 5–8 Hz) usually fall slightly more slowly than high frequency bands (20–35, 35–50 Hz) but the difference is small and variance large. The steepness of decline with distance in humans is significantly but only slightly smaller than that we reported earlier for the rabbit and rat, averaging less than one half.

Local coherence, for individual pairs of loci, shows differentiation in the millimeter range, i.e., nearest neighbor pairs may be locally well above or below average and this is sustained over minutes. Local highs and lows tend to be similar for widely different frequency bands. Coherence varies quite independently of power, although they are sometimes correlated.

Regional differentiation is statistically significant in average coherence among pairs of loci on temporal vs. frontal cortex or lateral frontal vs. subfrontal strips in the same patient, but such differences are usually small. We could not test how consistent they are over hours or between patients. Differences between left and right hemispheres, whether symmetrical pairs or pooled from two or more lobes on each side, can be quite large; in our patients the right side is usually higher, especially in the waking state.

Brain state has a large influence. Slow wave sleep usually shows slightly more coherence at each distance, in all bands, compared to the waking EEG, but not consistently. Coherence at a given distance or its rate of decline with distance is a more direct measure of synchrony than naked-eye “synchronization,” which is dominated by the power spectrum. Among the range of EEG states classified as seizures, coherence varies widely but it averages higher by 0.05-0.2 than in pre-ictal states, usually in all frequencies when computed over the whole seizure but much more in the higher bands during the height of the electrical paroxysm.

The findings point to still finer structure and more variance with closer spacing of electrodes. They could not predict the known large scale coherence between scalp electrodes, but are not in conflict with them. Scalp recording blurs the finer spatial structure, but reveals macrostructure missed by subdural and depth recording with limited numbers of channels. The strong tendency for correlated fluctuations across frequency bands is contrary to expectation from the common model of independent oscillators.

Keywords

Sleep
Seizure
Depth recording
Hippocampus
Cooperativity

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