Spatiotemporal dynamics between interictal epileptiform discharges and ripples during associative memory processing

Abstract

We describe the spatiotemporal course of cortical high-gamma activity (HGA), hippocampal ripple activity and interictal epileptiform discharges (IEDs) during an associative memory task in 15 epilepsy patients undergoing invasive electroencephalography (iEEG). Successful encoding trials were significantly greater HGA in hippocampus and frontal regions. Successful recall trials manifested sustained HGA in occipital pole and hippocampus compared to failed responses. Hippocampal ripple rates were greater during successful encoding and retrieval trials. IEDs during encoding were associated with decreased odds of remembering in hippocampus (−19%), temporal pole (−18%) or middle temporal gyrus (−15%). Hippocampal IEDs during retrieval predicted 33% decreased odds of remembering. Odds of remembering were further reduced if IEDs occurred during the 500-2000 ms window of encoding or retrieval. Hippocampal IEDs were followed by a transient decrease in ripple rate. We hypothesize that IEDs impair associative memory in a regionally and temporally specific manner by decreasing physiologic hippocampal ripples necessary for effective encoding and recall. Because dynamic memory impairment arises from pathological IED events competing with physiological ripples, IEDs represent a promising therapeutic target for memory remediation in patients with epilepsy.

Hippocampal ripples linked to recognition memory judgments in children

“…Specifically, our findings highlight the early development of cognitive specificity in ripple activation, which shows notable selectivity towards explicit memory judgments in young children. This reinforces the notion that awake hippocampal ripples are closely tied to mnemonic processes that are consciously accessible and reportable (Henin et al, 2021;Kunz et al, 2022;Norman et al, 2019Norman et al, , 2021Vaz et al, 2019), as opposed to the more automatic, sensory-driven components, that contribute to the sense of familiarity in a more implicit manner (Eichenbaum et al, 2007). parents before surgery.…”

“…They have been extensively linked to declarative memory retrieval in humans (Dickey et al, 2022;Henin et al, 2021;Khuvis et al, 2021;Kunz et al, 2022;Norman et al, 2019Norman et al, , 2021Sakon and Kahana, 2022), and have been shown to support memory-guided decision making (Fernández-Ruiz et al, 2019;Jadhav et al, 2012;Shin et al, 2019) and offline memory consolidation (Maingret et al, 2016;Rothschild et al, 2017;van de Ven et al, 2016) in animal models.…”

Temporal lobe interictal spikes disrupt encoding and retrieval of verbal memory: A subregion analysis

“…41,42 However, our results are in contrast with other studies that have reported no effect of IS in the MTL on memory encoding, 5,21,22 although one recent study also reported impairment. 13 Likely, our methods account for the discrepancy between those studies and ours. The verbal free task used here may be more in detecting a TCI/TMI during the encoding period than other tasks.…”

“…7,8 Furthermore, this is in accordance with a recent study that found a selective temporal impairment during stimulus presentation using an associative memory task. 13 However, another study reported that IS occurring before or during the presentation of a cognitive stimulus decrease memory performance. 40 More research that takes into consideration IS timing and performance might provide further insights.…”

“…11 Multiple mechanisms have been proposed by which IS may cause cognitive impairments. 5,12,13 Various reports have described location-specific effects of IS. In verbal episodic memory tasks, left-sided IS disrupt memory encoding 14,15 ; conversely, during spatial or visual tasks, right-sided IS produce TCI/TMI.…”