Whole-brain functional correlates of memory formation in mesial temporal lobe epilepsy

Doll, Anna; Wegrzyn, Martin; Benzait, Anissa; Mertens, Markus; Woermann, Friedrich G.; Labudda, Kirsten; Bien, Christian G.; Kißler, Johanna

doi:10.1016/j.nicl.2021.102723

Cited by 7 publications

(13 citation statements)

References 59 publications

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“…Hence, reduced mTL activation might be more common in patients with known structural lesions. It might also be driven by rFLE patients and the face encoding task as previous studies indicated that the right FL and mTL are typically more activated than the left during face encoding 17,33,8 . Further, inspection of t‐values in controls indicated that both right anterior mTL and right FL activation were stronger during face than during scene or word encoding.…”

Section: Discussionmentioning

confidence: 89%

“…We preprocessed MRI data using fMRIPrep 1.4.1rc4 23 . For further details on anatomical and functional MRI data acquisition and preprocessing ref 17 …”

Section: Methodsmentioning

confidence: 99%

“…Further, we examine the association between memory performance and both structural changes and functional activation in the mTL. Therefore, we applied a memory fMRI-paradigm of learning scenes, faces and words, that we previously used to elicit robust activations throughout the brain including the mTL, 17 in a group of FLE patients with predominantly structural etiology undergoing presurgical evaluation. changes in brain activation during learning.…”

Section: Introductionmentioning

confidence: 99%

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MRI evidence for material‐specific encoding deficits and mesial–temporal alterations in presurgical frontal lobe epilepsy patients

Doll,

Wegrzyn,

Woermann

et al. 2024

Epilepsia Open

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ObjectiveNeuroimaging studies reveal frontal lobe (FL) contributions to memory encoding. Accordingly, memory impairments are documented in frontal lobe epilepsy (FLE). Still, little is known about the structural or functional correlates of such impairments. Particularly, material specificity of functional changes in cerebral activity during memory encoding in FLE is unclear.MethodsWe compared 24 FLE patients (15 right‐sided) undergoing presurgical evaluation with 30 healthy controls on a memory fMRI‐paradigm of learning scenes, faces, and words followed by an out‐of‐scanner recognition task as well as regarding their mesial temporal lobe (mTL) volumes. We also addressed effects of FLE lateralization and performance level (normal vs. low).ResultsFLE patients had poorer memory performance and larger left hippocampal volumes than controls. Volume increase seemed, however, irrelevant or even dysfunctional for memory performance. Further, functional changes in FLE patients were right‐sided for scenes and faces and bilateral for words. In detail, during face encoding, FLE patients had, regardless of their performance level, decreased mTL activation, while during scene and word encoding only low performing FLE patients had decreased mTL along with decreased FL activation. Intact verbal memory performance was associated with higher right frontal activation in FLE patients but not in controls.SignificancePharmacoresistant FLE has a distinct functional and structural impact on the mTL. Effects vary with the encoded material and patients' performance levels. Thus, in addition to the direct effect of the FL, memory impairment in FLE is presumably to a large part due to functional mTL changes triggered by disrupted FL networks.Plain Language SummaryFrontal lobe epilepsy (FLE) patients may suffer from memory impairment. Therefore, we asked patients to perform a memory task while their brain was scanned by MRI in order to investigate possible changes in brain activation during learning. FLE patients showed changes in brain activation during learning and also structural changes in the mesial temporal lobe, which is a brain region especially relevant for learning but not the origin of the seizures in FLE. We conclude that FLE leads to widespread changes that contribute to FLE patients’ memory impairment.

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Section: Discussionmentioning

confidence: 89%

“…We preprocessed MRI data using fMRIPrep 1.4.1rc4 23 . For further details on anatomical and functional MRI data acquisition and preprocessing ref 17 …”

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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MRI evidence for material‐specific encoding deficits and mesial–temporal alterations in presurgical frontal lobe epilepsy patients

Doll,

Wegrzyn,

Woermann

et al. 2024

Epilepsia Open

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“…Using a face-name association task in a different study, we, too, observed reduced right hemisphere activity in RTLE patients alongside reduced activity within the left superior and inferior frontal gyrus in LTLE patients. 43 Doll et al 44 investigated the functional correlates of verbal and nonverbal memory encoding and subsequent memory formation in a group of 31 LTLE and 25 RTLE patients compared to healthy controls. During scene encoding, they reported PMN activation across groups, but the activation did not predict subsequent memory.…”

Section: Differences In Activation Patterns Between Groupsmentioning

confidence: 99%

Investigating the effect of hippocampal sclerosis on parietal memory network

Ethofer,

Milian,

Erb

et al. 2023

Epilepsia Open

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ObjectiveWe aimed to investigate differences in episodic memory networks between patients with temporal lobe epilepsy (TLE) due to hippocampal sclerosis and healthy controls, especially with regards to the parietal memory network (PMN), as well as their relation to neuropsychological memory performance after mesial temporal resection.Methods28 healthy subjects as well as 21 patients with TLE (12 left, 9 right) were investigated using a spatial memory fMRI paradigm, which has been shown to activate the PMN. Regions of interest (ROI) were defined based on the results of the second‐level analyses and activations within the predefined ROIs were compared across groups and correlated with postoperative verbal and nonverbal memory scores.ResultsHealthy subjects showed activations within regions belonging to the dorsal visual stream and the PMN as well as the bilateral parahippocampal place area, the bilateral frontal eye field, and the bilateral middle frontal gyrus. Comparison between groups revealed that TLE patients activated significantly less in the left middle occipital gyrus and the right precuneus. The activation pattern in left TLE patients showed further reductions, mainly in areas belonging to the dorsal visual stream and the PMN within the left hemisphere. Activations within the left superior parietal lobulus, bilateral inferior parietal lobulus, bilateral middle temporal gyrus, left precuneus, left frontal eye field, and left middle frontal gyrus correlated significantly with postoperative verbal memory scores, and activations within the left superior parietal lobulus, left inferior parietal lobulus, left middle temporal gyrus, and left precuneus correlated significantly with higher performance in postoperative nonverbal memory scores.SignificanceThe PMN is involved in episodic memory encoding. Higher activations in areas belonging to the PMN and the dorsal visual stream, especially within the left hemisphere, before amygdalohippocampectomy may result in higher postoperative memory scores.Plain language summaryThis study aims to investigate the effects of epilepsy due to hippocampal sclerosis, i.e. scarring in the temporal lobe, on memory networks in the brain. We discovered that especially patients with left‐sided hippocampal sclerosis show reduced brain activations in visual areas and memory networks within the left hemisphere of the brain during orientation in space. Importantly, higher activations within these areas may result in better memory after epilepsy surgery.

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“…It is encouraging that great progress has been made in identifying and characterizing epileptic networks across various patient subgroups and analysis methodologies. [1][2][3][4][5][6][7] These findings have implications for medical and surgical management of epilepsy but are typically retrospective and not validated across diverse datasets. Thus, it is time to address the systemic barriers that prevent the advancement of these promising findings and ultimate adoption into clinical care.…”

Section: Introductionmentioning

confidence: 99%

Integrating Network Neuroscience Into Epilepsy Care: Progress, Barriers, and Next Steps

et al. 2022

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Drug resistant epilepsy is a disorder involving widespread brain network alterations. Recently, many groups have reported neuroimaging and electrophysiology network analysis techniques to aid medical management, support presurgical planning, and understand postsurgical seizure persistence. While these approaches may supplement standard tests to improve care, they are not yet used clinically or influencing medical or surgical decisions. When will this change? Which approaches have shown the most promise? What are the barriers to translating them into clinical use? How do we facilitate this transition? In this review, we will discuss progress, barriers, and next steps regarding the integration of brain network analysis into the medical and presurgical pipeline.

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Whole-brain functional correlates of memory formation in mesial temporal lobe epilepsy

Cited by 7 publications

References 59 publications

MRI evidence for material‐specific encoding deficits and mesial–temporal alterations in presurgical frontal lobe epilepsy patients

MRI evidence for material‐specific encoding deficits and mesial–temporal alterations in presurgical frontal lobe epilepsy patients

Investigating the effect of hippocampal sclerosis on parietal memory network

Integrating Network Neuroscience Into Epilepsy Care: Progress, Barriers, and Next Steps

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