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. 2013 Oct 18:7:140.
doi: 10.3389/fncom.2013.00140. eCollection 2013.

Single-unit activities during epileptic discharges in the human hippocampal formation

Catalina Alvarado-Rojas  1 , Katia Lehongre, Juliana Bagdasaryan, Anatol Bragin, Richard Staba, Jerome Engel Jr, Vincent Navarro, Michel Le Van Quyen
Affiliations

Single-unit activities during epileptic discharges in the human hippocampal formation

Catalina Alvarado-Rojas et al. Front Comput Neurosci. .

Abstract

Between seizures the brain of patients with epilepsy generates pathological patterns of synchronous activity, designated as interictal epileptiform discharges (ID). Using microelectrodes in the hippocampal formations of 8 patients with drug-resistant temporal lobe epilepsy, we studied ID by simultaneously analyzing action potentials from individual neurons and the local field potentials (LFPs) generated by the surrounding neuronal network. We found that ~30% of the units increased their firing rate during ID and 40% showed a decrease during the post-ID period. Surprisingly, 30% of units showed either an increase or decrease in firing rates several hundred of milliseconds before the ID. In 4 patients, this pre-ID neuronal firing was correlated with field high-frequency oscillations at 40-120 Hz. Finally, we observed that only a very small subset of cells showed significant coincident firing before or during ID. Taken together, we suggested that, in contrast to traditional views, ID are generated by a sparse neuronal network and followed a heterogeneous synchronization process initiated over several hundreds of milliseconds before the paroxysmal discharges.

Keywords: interictal epileptiform discharges; microelectrode recordings; multiunit activity; spike synchronization; temporal lobe epilepsy.

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Figures

Figure 1
Figure 1
(A) Macro- and micro-electrodes superimposed on a magnetic resonance imaging scan. Nine microwires (40 μm diameter) extend beyond the tip of each macro-electrode and record the hippocampal formation. (B) Interictal discharges (ID) recorded with microelectrode local field potentials from adjacent electrodes in the hippocampus of a patient. (C) Example of wide-band recording of an ID event with the corresponding extracted single unit activities. (D) Raster plot and peri-event histogram (bin size, 10 ms) of the single unit activity shown above. Note the strong changes in the firing rate and instantaneous frequency (red) during the ID.
Figure 2
Figure 2
(A–C) Peri-ID firing changes of single units defined as the ratio of changes in discharge probability between the baseline and pre-ID, ID or post-ID. (D) Examples of two units (Top: raw data; Bottom: Raster plots and peri-event histograms) recorded in different patients and showing significant decrease (a) or increase (b) during the pre-ID period (see arrows).
Figure 3
Figure 3
(A,B) Time-frequency representations of the LFP around the ID for two patients showing pre-ID changes in neuronal firing. Note the increase in LFP high-frequency oscillations between 40 and 120 Hz preceding the ID and closely correlated with the decrease (A) or increase (B) in neuronal firing (see arrows).
Figure 4
Figure 4
Top: Cross-correlograms between pairs of units during ID in two patients (A,B). The blue lines are the significance levels computed from 1000 jittered spike trains. In both cases, the center peak exceeds the significance level (arrows) and the pairs of units are considered to be significantly correlated. Bottom: Unit synchronizations (red circles) were defined as coincidences between the two units (green and blue points) occurring over a 5-ms interval. Note the significant increase in coincidences during ID (A) and the pre-ID period (B), over the statistical threshold defined by a random jitter of the original data.
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