Alterations in neural oscillations related to working memory deficit in temporal lobe epilepsy

Pan, Liping; Guo, Dandan; Wang, Jiajing; Hao, Yuhan; Zhang, Lulin; Qin, Xiao; Song, Yijun

doi:10.1016/j.yebeh.2021.108063

Cited by 6 publications

(8 citation statements)

References 67 publications

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“…This dominance of the right hemisphere might be in accordance with fMRI studies, which demonstrated that increasing memory load was associated with right hemisphere dominance [56]. Previous scalp EEG studies have also suggested potential roles of parietal, frontal, and temporal areas in memory tasks [57][58][59], and we enhanced the significance and credibility of these scalp EEG findings by setting intracranial activations as the criterion.…”

Section: Region Participation In the Working Memory Tasksupporting

confidence: 87%

Phase-amplitude coupling between low-frequency scalp EEG and high-frequency intracranial EEG during working memory task

Sheng

et al. 2022

J. Neural Eng.

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Objective. Revealing the relationship between simultaneous scalp electroencephalography (EEG) and intracranial electroencephalography (iEEG) is of great importance for both neuroscientific research and translational applications. However, whether prominent iEEG features in the high-gamma band can be reflected by scalp EEG is largely unknown. To address this, we investigated the phase-amplitude coupling (PAC) phenomenon between the low-frequency band of scalp EEG and the high-gamma band of iEEG. Approach. We analyzed a simultaneous iEEG and scalp EEG dataset acquired under a verbal working memory paradigm from nine epilepsy subjects. The PAC values between pairs of scalp EEG channel and identified iEEG channel were explored. After identifying the frequency combinations and electrode locations that generated the most significant PAC values, we compared the PAC values of different task periods (encoding, maintenance, and retrieval) and memory loads. Main results. We demonstrated that the amplitude of high-gamma activities in the entorhinal cortex, hippocampus, and amygdala was correlated to the delta or theta phase at scalp locations such as Cz and Pz. In particular, the frequency bin that generated the maximum PAC value centered at 3.16–3.84 Hz for the phase and 50–85 Hz for the amplitude. Moreover, our results showed that PAC values for the retrieval period were significantly higher than those of the encoding and maintenance periods, and the PAC was also influenced by the memory load. Significance. This is the first human simultaneous iEEG and scalp EEG study demonstrating that the amplitude of iEEG high-gamma components is associated with the phase of low-frequency components in scalp EEG. These findings enhance our understanding of multiscale neural interactions during working memory, and meanwhile, provide a new perspective to estimate intracranial high-frequency features with non-invasive neural recordings.

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Section: Region Participation In the Working Memory Tasksupporting

confidence: 87%

Phase-amplitude coupling between low-frequency scalp EEG and high-frequency intracranial EEG during working memory task

Sheng

et al. 2022

J. Neural Eng.

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“…An asterisk (*), serving as a fixation point, was shown for 0.5 s; four pictures from a memory set were then sequentially presented for 1 s each, separated by an interval of 0.013 s. This was followed by a 3-s maintenance phase, after which a probe image was shown to the subject. Then there was 2 s for the subject to decide whether the probe image was presented among the initial four images from the memory set (Pan et al, 2021 ).…”

Section: Methodsmentioning

confidence: 99%

“…Higher-level cognition is impaired in cases of WM deficits, affecting normal functioning in daily activities. WM processes, including the encoding, maintenance, and retrieval phases, are well-known to be associated with distributed network properties and interactions across multiple brain regions (Soreq et al, 2019 ), and alterations in neural oscillations can occur during any phase of WM but are most prominent during the encoding phase in patients with temporal lobe epilepsy (TLE; Pan et al, 2021 ). The aim of the current study was to investigate alterations in the neural networks of patients with TLE during WM encoding.…”

Section: Introductionmentioning

confidence: 99%

Alterations in Neural Networks During Working Memory Encoding Related to Cognitive Impairment in Temporal Lobe Epilepsy

Pan

Bao

et al. 2022

Front. Hum. Neurosci.

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Objective: The aim of the current study was to investigate the alterations in the neural networks of patients with temporal lobe epilepsy (TLE) during working memory (WM) encoding.Methods: Patients with TLE (n = 52) and healthy volunteers (n = 35) completed a WM task, during which 34-channel electroencephalogram signals were recorded. The neural networks during WM encoding were calculated in TLE patients with (TLE-WM) and without (TLE-N) WM deficits.Results: Functional connectivity strength decreased, and the theta network was altered in the TLE-WM group, although no significant differences in clinical features were observed between the TLE-N and TLE-WM groups.Conclusions: Not all patients with TLE present with cognitive impairments and alterations in the theta network were identified in TLE patients with functional cognitive deficits.Significance: The theta network may represent a sensitive measure of cognitive impairment and could predict cognitive outcomes among patients with TLE.

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“…Theta activity is responsible for integrating top‐down and bottom‐up information processing and the allocation of cognitive resources 16 . We previously demonstrated that the power of the theta frequency band was significantly higher than that of other frequency bands during a WM task and was higher in the frontal region than in other brain regions 17 . Frontal theta power was found to be significantly lower in temporal lobe epilepsy (TLE) patients with WM impairment than in normal subjects during the WM encoding, maintenance, and retrieval phases; moreover, reduced frontal theta power during the encoding phase was associated with longer reaction times (RTs) 17 .…”

Section: Introductionmentioning

confidence: 99%

“… 16 We previously demonstrated that the power of the theta frequency band was significantly higher than that of other frequency bands during a WM task and was higher in the frontal region than in other brain regions. 17 Frontal theta power was found to be significantly lower in temporal lobe epilepsy (TLE) patients with WM impairment than in normal subjects during the WM encoding, maintenance, and retrieval phases; moreover, reduced frontal theta power during the encoding phase was associated with longer reaction times (RTs). 17 VNS increased N1 amplitude and frontal alpha asymmetry during WM tasks and decreased error rates in patients with refractory epilepsy.…”

Section: Introductionmentioning

confidence: 99%

Transcutaneous auricular vagus nerve stimulation improves working memory in temporal lobe epilepsy: A randomized double‐blind study

Pan

Wang

et al. 2023

CNS Neurosci Ther

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AimsThis study investigated the impact of transcutaneous auricular vagus nerve stimulation (taVNS) on working memory (WM) in refractory temporal lobe epilepsy (rTLE) and the underlying mechanisms.MethodsIn this randomized double‐blind study, 28 rTLE patients were subjected to an active or sham taVNS (a/s‐taVNS) protocol for 20 weeks (a‐taVNS group, n = 19; s‐ta VNS group, n = 9). Patients performed visual WM tasks during stimulation and neural oscillations were simultaneously recorded by 19‐channel electroencephalography.ResultsCompared with the baseline state, reaction time was significantly shorter after 20 weeks of taVNS in the a‐taVNS group (p = 0.010), whereas no difference was observed in the s‐taVNS group (p > 0.05). The power spectral density (PSD) of the theta frequency band in the Fz channel decreased significantly after a‐taVNS during WM‐encoding (p = 0.020), maintenance (p = 0.038), and retrieval (p = 0.039) phases, but not in the s‐taVNS group (all p > 0.05).ConclusionNeural oscillations during WM were altered by taVNS and WM performance was improved. Alterations in frontal midline theta oscillations may be a marker for the effect of taVNS on cognitive regulation.

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Alterations in neural oscillations related to working memory deficit in temporal lobe epilepsy

Cited by 6 publications

References 67 publications

Phase-amplitude coupling between low-frequency scalp EEG and high-frequency intracranial EEG during working memory task

Phase-amplitude coupling between low-frequency scalp EEG and high-frequency intracranial EEG during working memory task

Alterations in Neural Networks During Working Memory Encoding Related to Cognitive Impairment in Temporal Lobe Epilepsy

Transcutaneous auricular vagus nerve stimulation improves working memory in temporal lobe epilepsy: A randomized double‐blind study

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