Network oscillations modulate interictal epileptiform spike rate during human memory

Abstract

Eleven patients being evaluated with intracranial electroencephalography for medically resistant temporal lobe epilepsy participated in a visual recognition memory task. Interictal epileptiform spikes were manually marked and their rate of occurrence compared between baseline and three 2 s periods spanning a 6 s viewing period. During successful, but not unsuccessful, encoding of the images there was a significant reduction in interictal epileptiform spike rate in the amygdala, hippocampus, and temporal cortex. During the earliest encoding period (0-2000 ms after image presentation) in these trials there was a widespread decrease in the power of theta, alpha and beta band local field potential oscillations that coincided with emergent focal gamma frequency activity. Interictal epileptiform spike rate correlated with spectral band power changes and broadband (4-150 Hz) desynchronization, which predicted significant reduction in interictal epileptiform spike rate. Spike-triggered averaging of the field potential power spectrum detected a burst of low frequency synchronization 200 ms before the interictal epileptiform spikes that arose during this period of encoding. We conclude that interictal epileptiform spikes are modulated by the patterns of network oscillatory activity that accompany human memory offering a new mechanistic insight into the interplay of cognitive processing, local field potential dynamics and interictal epileptiform spike generation.

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

“…Network oscillations, like the spike-preceding gamma, may help elucidate the neuronal processes underlying epileptiform activities, as demonstrated in a recent study using a rat model of epilepsy. 5 The relationship between network activity and IEDs has recently been applied to study the effect of cognitively induced oscillations on IED suppression, 9 opening a possibility for treating interictal pathophysiology. Further research will show whether the gamma-IEDs, physiological HFOs associated with normal function, 10 and seizures share common network processes and thus drive new treatments and therapeutic strategies.…”

Pathological and physiological high-frequency oscillations in focal human epilepsy

“…Patients were aware that they might be asked to recall the images 24 h later. Details of the protocol have been described previously (Matsumoto et al 2013).…”

Intracranial recordings and human memory

“…In humans, direct intra-MTL depth recordings and/or cortical surface recordings have shown that presentation of a subsequently remembered stimulus resets theta activity or alters theta power in the hippocampus, rhinal cortex, and/or amygdala [10,12-14,19,20], as well as temporal, frontal, and/or parietal-occipital association cortices [21-24]. Shifts in other frequency bands tend to co-occur with these shifts in theta.…”

“…Shifts in other frequency bands tend to co-occur with these shifts in theta. Specifically, theta and alpha phase resets in temporal, parietal, and occipital cortices [21]; theta, alpha, and beta phase resets [12] or power decreases [20] in the MTL; and right cortical theta power increases in the midst of widespread gamma increases [25] have been linked to SM. Employing SUA measurements, Rutishauser et al [19] reported that theta phase resets are tightly coupled with local spiking activity – i.e., theta phase-SUA coupling (see [26]).…”

“…[22]). Importantly, ECoG studies demonstrate that low- and high-frequency activity often share an inverse relationship [5,20,24,25,38,39,40]. Likewise, while measures of high-frequency amplitude show overlap with the BOLD measures of fMRI, low-frequency activity is anatomically dissociated with BOLD measures [41].…”