Episodic memory network connectivity in temporal lobe epilepsy

Marine Fleury; Sarah Buck; Lawrence P Binding; Lorenzo Caciagli; Sjoerd B Vos; Gavin P Winston; Pamela J Thompson; Matthias J Koepp; John S Duncan; Meneka K Sidhu

doi:10.1111/epi.17370

Episodic memory network connectivity in temporal lobe epilepsy

Epilepsia. 2022 Oct;63(10):2597-2622. doi: 10.1111/epi.17370. Epub 2022 Aug 2.

Authors

Marine Fleury^{1

2}, Sarah Buck^{1

2}, Lawrence P Binding^{1

2

3}, Lorenzo Caciagli^{1

2

4}, Sjoerd B Vos^{1

2

5}, Gavin P Winston^{1

2

6}, Pamela J Thompson^{1

2}, Matthias J Koepp^{1

2}, John S Duncan^{1

2}, Meneka K Sidhu^{1

2}

Affiliations

¹ Department of Clinical and Experimental Epilepsy, University College London Queen Square Institute of Neurology, London, UK.
² MRI Unit, Epilepsy Society, Buckinghamshire, UK.
³ Department of Computer Science, Centre for Medical Image Computing, University College London, London, UK.
⁴ Department of Bioengineering, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
⁵ Neuroradiological Academic Unit, University College London Queen Square Institute of Neurology, University College London, London, UK.
⁶ Division of Neurology, Department of Medicine, Queen's University, Kingston, Ontario, Canada.

Abstract

Objective: Temporal lobe epilepsy (TLE) affects brain networks and is associated with impairment of episodic memory. Temporal and extratemporal reorganization of memory functions is described in functional magnetic resonance imaging (fMRI) studies. Functional reorganizations have been shown at the local activation level, but network-level alterations have been underinvestigated. We aim to investigate the functional anatomy of memory networks using memory fMRI and determine how this relates to memory function in TLE.

Methods: Ninety patients with unilateral TLE (43 left) and 29 controls performed a memory-encoding fMRI paradigm of faces and words with subsequent out-of-scanner recognition test. Subsequent memory event-related contrasts of words and faces remembered were generated. Psychophysiological interaction analysis investigated task-associated changes in functional connectivity seeding from the mesial temporal lobes (MTLs). Correlations between changes in functional connectivity and clinical memory scores, epilepsy duration, age at epilepsy onset, and seizure frequency were investigated, and between connectivity supportive of better memory and disease burden. Connectivity differences between controls and TLE, and between TLE with and without hippocampal sclerosis, were explored using these confounds as regressors of no interest.

Results: Compared to controls, TLE patients showed widespread decreased connectivity between bilateral MTLs and frontal lobes, and increased local connectivity between the anterior MTLs bilaterally. Increased intrinsic connectivity within the bilateral MTLs correlated with better out-of-scanner memory performance in both left and right TLE. Longer epilepsy duration and higher seizure frequency were associated with decreased connectivity between bilateral MTLs and left/right orbitofrontal cortex (OFC) and insula, connections supportive of memory functions. TLE due to hippocampal sclerosis was associated with greater connectivity disruption within the MTL and extratemporally.

Significance: Connectivity analyses showed that TLE is associated with temporal and extratemporal memory network reorganization. Increased bilateral functional connectivity within the MTL and connectivity to OFC and insula are efficient, and are disrupted by greater disease burden.

Keywords: connectivity; epilepsy; memory; network; psychophysiological interaction.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Epilepsy, Temporal Lobe* / pathology
Functional Laterality / physiology
Hippocampus / pathology
Humans
Magnetic Resonance Imaging / methods
Memory, Episodic*
Sclerosis / complications
Seizures

Abstract

Publication types

MeSH terms

Grants and funding