Elsevier

Epilepsy & Behavior

Volume 123, October 2021, 108209
Epilepsy & Behavior

Brief Communication
Effects of hippocampal interictal discharge timing, duration, and spatial extent on list learning

https://doi.org/10.1016/j.yebeh.2021.108209Get rights and content

Abstract

Interictal epileptiform discharges (IEDs) can impair memory. The properties of IEDs most detrimental to memory, however, are undefined. We studied the impact of temporal and spatial characteristics of IEDs on list learning. Subjects completed a memory task during intracranial EEG recordings including hippocampal depth and temporal neocortical subdural electrodes. Subjects viewed a series of objects, and after a distracting task, recalled the objects from the list. The impacts of IED presence, duration, and propagation to neocortex during encoding of individual stimuli were assessed. The effects of IED total number and duration during maintenance and recall periods on delayed recall performance were also determined. The influence of IEDs during recall was further investigated by comparing the likelihood of IEDs preceding correctly recalled items vs. periods of no verbal response. Across 6 subjects, we analyzed 28 hippocampal and 139 lateral temporal contacts. Recall performance was poor, with a median of 17.2% correct responses (range 10.4–21.9%). Interictal epileptiform discharges during encoding, maintenance, and recall did not significantly impact task performance, and there was no significant difference between the likelihood of IEDs during correct recall vs. periods of no response. No significant effects of discharge duration during encoding, maintenance, or recall were observed. Interictal epileptiform discharges with spread to lateral temporal cortex during encoding did not adversely impact recall. A post hoc analysis refining model assumptions indicated a negative impact of IED count during the maintenance period, but otherwise confirmed the above results. Our findings suggest no major effect of hippocampal IEDs on list learning, but study limitations, such as baseline hippocampal dysfunction, should be considered. The impact of IEDs during the maintenance period may be a focus of future research.

Introduction

Interictal epileptiform discharges (IEDs) are electrophysiological abnormalities on EEG in individuals with epilepsy or a propensity for epilepsy. Interictal epileptiform discharges can disrupt cognitive task performance in animal models and humans, with memory processes particularly vulnerable to IED effects in the temporal lobes [1]. In humans, IEDs impaired verbal and non-verbal working [2], short-term [3], and long-term [4] memory and correlated with accelerated rates of long-term forgetting [4], [5].

Studies of IED timing in relation to memory performance suggest no effect of hippocampal or mesial temporal IEDs during encoding, but a negative impact during maintenance [6] and retrieval [6], [7], [8]. A reduced mesial temporal IED rate from baseline during encoding of images correctly recognized after a 24-h delay may suggest a negative effect of greater IED burden on encoding, although the study was not designed to address this issue [9]. Whether specific IED characteristics, such as duration or spatial extent, determine effects on encoding is unclear.

In this study, patients with intractable focal-onset epilepsy completed a list learning task during iEEG monitoring with hippocampal depth and neocortical subdural electrodes. The properties of hippocampal IEDs during encoding were characterized and their relationships to delayed free recall performance were determined, with the hypothesis that IEDs with longer duration or greater spatial extent were more likely to impair memory. The effects of discharges during maintenance and recall periods were also assessed, with the expectation that a greater burden of IEDs would correlate with impaired performance.

Section snippets

Subjects

Subjects were six adults with medically refractory focal-onset seizures, admitted to New York University Langone Health for iEEG implantation for epilepsy surgery evaluation (Table 1). Participants had hippocampal IEDs and suspected temporal lobe seizures, with implanted mesial depth and neocortical subdural temporal electrodes. The local institutional review board approved the study, and written informed consent was obtained from each subject.

Intracranial EEG (iEEG) recordings

A total of 31 hippocampal and 142 lateral temporal

Task performance

EEG was recorded over 1120 trials (objects) of the list learning task. Median percent correct recall was 17.2% (range 10.4–21.9%) (Table 2).

Presence of IEDs during encoding

No statistically significant relationship was evident between the presence or absence of hippocampal IEDs during encoding and percentage of items correctly recalled (p > 0.1).

Spatial extent

No statistically significant relationship between spatial extent of discharges during encoding and free recall performance was evident (p > 0.1). The majority of hippocampal IEDs had

Discussion

The primary analysis failed to support that hippocampal IEDs disrupt list learning. No significant effects of hippocampal IED presence, duration, or propagation to lateral temporal cortex were seen during list encoding. Further, there was no relationship between performance and IED number or duration during maintenance or recall periods, although a post hoc analysis suggested a possible negative impact of greater IED counts during maintenance. Our findings contrast with earlier work indicating

Funding

This work was supported by a United States (U.S.) Department of Veterans Affairs Clinical Sciences R&D (CSRD) Service Career Development Award (IK2 CX-001255) (BLM) and the National Institutes of Mental Health (F32 MH106266) (LL).

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors wish to thank Adeen Flinker, PhD, for his guidance regarding data analysis and Daniel Maksumov, BS, for administrative assistance.

References (18)

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    Temporal approaches typically extract different iEEG measurements that are then convolved with a hemodynamic response function to predict the BOLD signal (Haufe et al., 2018; Mukamel et al., 2005). Initial spatial comparisons showed overlap between the sEEG high frequency and fMRI signal changes (Lachaux et al., 2007a; Nir et al., 2007). More complex relationships between these signals were revealed later (Hermes et al., 2012), where ECoG high frequency power increases and low frequency power decreases explain complementary variance in BOLD increases (see also (Haufe et al., 2018; Hermes et al., 2017)).

1

Present address: Department of Psychology, Syracuse University, 430 Huntington Hall, Syracuse, NY 13244, United States.

2

Present address: Department of Psychology, Columbia University, 1190 Amsterdam Ave., New York, NY 10027, United States.

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