Chronic intracranial recordings after resection for epilepsy reveal a "running down" of epileptiform activity

Kundu, Bornali; Charlebois, Chantel M.; Anderson, Daria Nesterovich; Peters, Angela; Rolston, John D.

doi:10.1111/epi.17645

Cited by 7 publications

(4 citation statements)

References 30 publications

(52 reference statements)

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“…hypothesized that as a patient's seizure frequency decreased, the aperiodic exponent would concurrently be reduced. 36 We observed more-specific changes in aperiodic exponents, such that patient-specific circadian rhythmicity of the aperiodic exponent was associated with seizure reduction. Here, we report a novel electrographic biomarker measured during the initial months after implantation that prognosticates clinical response to RNS in patients with mesial temporal lobe epilepsy.…”

Section: Key Pointsmentioning

confidence: 71%

“…The objective of this study was to evaluate the aperiodic exponent, presumed to reflect E/I balance, as a biomarker for the clinical response to RNS. We hypothesized that as a patient's seizure frequency decreased, the aperiodic exponent would concurrently be reduced 36 . We observed more‐specific changes in aperiodic exponents, such that patient‐specific circadian rhythmicity of the aperiodic exponent was associated with seizure reduction.…”

Section: Introductionmentioning

confidence: 99%

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Circadian changes in aperiodic activity are correlated with seizure reduction in patients with mesial temporal lobe epilepsy treated with responsive neurostimulation

Charlebois,

Anderson,

Smith

et al. 2024

Epilepsia

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ObjectivesResponsive neurostimulation (RNS) is an established therapy for drug‐resistant epilepsy that delivers direct electrical brain stimulation in response to detected epileptiform activity. However, despite an overall reduction in seizure frequency, clinical outcomes are variable, and few patients become seizure‐free. The aim of this retrospective study was to evaluate aperiodic electrophysiological activity, associated with excitation/inhibition balance, as a novel electrographic biomarker of seizure reduction to aid early prognostication of the clinical response to RNS.MethodsWe identified patients with intractable mesial temporal lobe epilepsy who were implanted with the RNS System between 2015 and 2021 at the University of Utah. We parameterized the neural power spectra from intracranial RNS System recordings during the first 3 months following implantation into aperiodic and periodic components. We then correlated circadian changes in aperiodic and periodic parameters of baseline neural recordings with seizure reduction at the most recent follow‐up.ResultsSeizure reduction was correlated significantly with a patient's average change in the day/night aperiodic exponent (r = .50, p = .016, n = 23 patients) and oscillatory alpha power (r = .45, p = .042, n = 23 patients) across patients for baseline neural recordings. The aperiodic exponent reached its maximum during nighttime hours (12 a.m. to 6 a.m.) for most responders (i.e., patients with at least a 50% reduction in seizures).SignificanceThese findings suggest that circadian modulation of baseline broadband activity is a biomarker of response to RNS early during therapy. This marker has the potential to identify patients who are likely to respond to mesial temporal RNS. Furthermore, we propose that less day/night modulation of the aperiodic exponent may be related to dysfunction in excitation/inhibition balance and its interconnected role in epilepsy, sleep, and memory.

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Section: Key Pointsmentioning

confidence: 71%

Section: Introductionmentioning

confidence: 99%

Circadian changes in aperiodic activity are correlated with seizure reduction in patients with mesial temporal lobe epilepsy treated with responsive neurostimulation

Charlebois,

Anderson,

Smith

et al. 2024

Epilepsia

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“…This is in keeping with the notion of a protracted normalization of brain networks postoperatively. 68 …”

Section: Discussionmentioning

confidence: 99%

Long-term neuropsychological trajectories in children with epilepsy: does surgery halt decline?

Eriksson,

Prentice,

Piper

et al. 2024

Brain

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Neuropsychological impairments are common in children with drug-resistant epilepsy. It has been proposed that epilepsy surgery may alleviate these impairments by providing seizure freedom; however, findings from prior studies have been inconsistent. We mapped long-term neuropsychological trajectories in children before and after undergoing epilepsy surgery, to measure the impact of disease course and surgery on functioning. We performed a retrospective cohort study of 882 children who had undergone epilepsy surgery at Great Ormond Street Hospital (1990-2018). We extracted patient information and neuropsychological functioning – obtained from IQ tests (domains: Full-Scale IQ, Verbal IQ, Performance IQ, Working Memory, and Processing Speed) and tests of academic attainment (Reading, Spelling and Numeracy) – and investigated changes in functioning using regression analyses. We identified 500 children (248 females) who had undergone epilepsy surgery (median age at surgery = 11.9 years, interquartile range = [7.8,15.0]) and neuropsychology assessment. These children showed declines in all domains of neuropsychological functioning in the time leading up to surgery (all p-values ≤ 0.001; e.g., βFSIQ = -1.9, SEFSIQ = 0.3, pFSIQ < 0.001). Children lost on average one to four points per year, depending on the domain considered; 27-43% declined by 10 or more points from their first to their last preoperative assessment. At the time of presurgical evaluation, most children (46-60%) scored one or more standard deviations below the mean (<85) on the different neuropsychological domains; 37% of these met the threshold for intellectual disability (Full-Scale IQ < 70). On a group level, there was no change in performance from pre- to postoperative assessment on any of the domains (all p-values > 0.128). However, children who became seizure-free through surgery showed higher postoperative neuropsychological performance (e.g., rrb-FSIQ = 0.37, p < 0.001). These children continued to demonstrate improvements in neuropsychological functioning over the course of their long-term follow-up (e.g., βFSIQ = 0.9, SEFSIQ = 0.3, pFSIQ = 0.004). Children who had discontinued antiseizure medication (ASM) treatment at one-year follow-up showed an eight-to-13-point advantage in postoperative Working Memory, Processing Speed, and Numeracy, and greater improvements in Verbal IQ, Working Memory, Reading, and Spelling (all p-values < 0.034) over the postoperative period compared to children who were seizure-free and still receiving ASMs. In conclusion, by providing seizure freedom and the opportunity for ASM cessation, epilepsy surgery may not only halt but reverse the downward trajectory that children with drug-resistant epilepsy display in neuropsychological functioning. To halt this decline as soon as possible, or potentially prevent it from occurring in the first place, children with focal epilepsy should be considered for epilepsy surgery as early as possible after diagnosis.

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“…Recent methodological advancements offer an apt means to decompose the EEG power spectrum into rhythmic oscillations (periodic component) and non-rhythmic fluctuations (aperiodic component). It helps to dissect complex neural signals (Leroy et al, 2022), enrich our understanding of brain function (Lendner et al, 2020), identify potential biomarkers of disease (Pollak et al, 2024), and assess the effectiveness of a therapy (Kundu et al, 2023; Salvatore et al, 2023). The strength of the approach particularly stems from its reflection of the EEG signal’s two-fold nature, encompassing both its mathematical characteristics in signal analysis and its neurophysiological correlates.…”

Section: Introductionmentioning

confidence: 99%

Normative characterization of age-related periodic and aperiodic activity in resting-state clinical EEG recordings

Leroy,

Bublitz,

von Dincklage

et al. 2024

Preprint

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ObjectiveNon-invasive oscillatory brain stimulation techniques target the oscillatory activity of the brain and have several potential therapeutic applications in the clinical context. The aim of these analyses from clinical routine EEG recordings was to provide normative values of physiological age-related oscillatory (periodic) and non-rhythmic (aperiodic) activity.MethodsWe analyzed 532 EEGs of patients between 8 and 92 years of age. EEG segments were preprocessed, and the power spectrum was computed using a multitaper method. We decomposed the power spectrum into periodic (peak power, frequency, and bandwidth) and aperiodic (intercept and exponent) components. Linear regression models were used to investigate age-related changes in these parameters.ResultsWe observed significant global age-related changes in the periodic alpha (- 0.015 Hz/year) and gamma (+ 0.013 to + 0.031Hz/year) peak frequency as well as in the aperiodic exponent (- 0.003 to - 0.004 μV2/Hz/year). In the other parameters there were solely regional or no significant age-related changes.ConclusionsDecomposing the power spectrum into periodic and aperiodic components allows for the characterization of age-related changes.SignificanceThis study provides the first spectrum-wide normative characterization of age-related changes in periodic and aperiodic activity, relevant for non-invasive brain stimulation with alternating current targeting ongoing oscillatory activity.Highlights-Alpha peak frequency decreases with age, while gamma peak frequency accelerates.-Age-related changes in alpha and theta power result from a flattening of the aperiodic slope, not decreased oscillatory activity-Decomposing the EEG spectrum into periodic and aperiodic activity is essential when characterizing ongoing oscillatory activity

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Chronic intracranial recordings after resection for epilepsy reveal a "running down" of epileptiform activity

Cited by 7 publications

References 30 publications

Circadian changes in aperiodic activity are correlated with seizure reduction in patients with mesial temporal lobe epilepsy treated with responsive neurostimulation

Circadian changes in aperiodic activity are correlated with seizure reduction in patients with mesial temporal lobe epilepsy treated with responsive neurostimulation

Long-term neuropsychological trajectories in children with epilepsy: does surgery halt decline?

Normative characterization of age-related periodic and aperiodic activity in resting-state clinical EEG recordings

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