Brief CommunicationEffects of hippocampal interictal discharge timing, duration, and spatial extent on list learning
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.
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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.
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Cited by (4)
Advances in human intracranial electroencephalography research, guidelines and good practices
2022, NeuroImageCitation Excerpt :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.