The organization of functional neurocognitive networks in focal epilepsy correlates with domain-specific cognitive performance.

Christoffer Hatlestad‐Hall,Kjell Heuser,Hanna Renvall,Aksel Erichsen,Erik Taubøll,Ricardo Bruña,Annette Holth Skogan,Fernando Maestú,Camillo Marra,Ira H Haraldsen,Marte Roa Syvertsen,Anne‐Kristin Solbakk,Vebjørn Andersson

doi:10.1002/jnr.24896

Abstract

Understanding and diagnosing cognitive impairment in epilepsy remains a prominent challenge. New etiological models suggest that cognitive difficulties might not be directly linked to seizure activity, but are rather a manifestation of a broader brain pathology. Consequently, treating seizures is not sufficient to alleviate cognitive symptoms, highlighting the need for novel diagnostic tools. Here, we investigated whether the organization of three intrinsic, resting-state functional connectivity networks was correlated with domain-specific cognitive test performance. Using individualized EEG source reconstruction and graph theory, we examined the association between network small worldness and cognitive test performance in 23 patients with focal epilepsy and 17 healthy controls, who underwent a series of standardized pencil-and-paper and digital cognitive tests. We observed that the specific networks robustly correlated with test performance in distinct cognitive domains. Specifically, correlations were evident between the default mode network and memory in patients, the central-executive network and executive functioning in controls, and the salience network and social cognition in both groups. Interestingly, the correlations were evident in both groups, but in different domains, suggesting an alteration in these functional neurocognitive networks in focal epilepsy. The present findings highlight the potential clinical relevance of functional brain network dysfunction in cognitive impairment.

Highlights

Fundamental physiological processes in the human brain, such as those supporting control of movement (King et al, 2018), autonomic functions (Fan et al, 2012), and cognition (Shine et al, 2019), are sustained and regulated by complex interactions both within and between functional networks
HATLESTAD-HALL et al EEG source reconstruction and graph theory, we examined the association between network small worldness and cognitive test performance in 23 patients with focal epilepsy and 17 healthy controls, who underwent a series of standardized pencil-and- paper and digital cognitive tests
Cognitive dysfunction in focal epilepsy (FE) patients may change over time, possibly reflecting the dynamic nature of brain networks and their disturbance, and may even persist after successful seizure remission has been achieved with anti-seizure medication (ASM; Hermann et al, 2007)

Summary

Introduction

Fundamental physiological processes in the human brain, such as those supporting control of movement (King et al, 2018), autonomic functions (Fan et al, 2012), and cognition (Shine et al, 2019), are sustained and regulated by complex interactions both within and between functional networks. Concurrent with functional network changes, patients with epilepsy are often burdened with cognitive impairment (Henning et al, 2019; Lin et al, 2012). Such impairment is increasingly understood as a distinct manifestation of underlying brain network pathology, rather than being directly linked to seizure activity (Helmstaedter & Witt, 2017). This notion lines up with evidence that FE often manifests with widespread cognitive impairment extending beyond the seizure onset area's classical cognitive expression (Oyegbile et al, 2004). Cognitive dysfunction in FE patients may change over time, possibly reflecting the dynamic nature of brain networks and their disturbance, and may even persist after successful seizure remission has been achieved with anti-seizure medication (ASM; Hermann et al, 2007)

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