Neuroticism in temporal lobe epilepsy is associated with altered limbic-frontal lobe resting-state functional connectivity

Bonet, Charlene N. Rivera; Hwang, Gyujoon; Hermann, Bruce P.; Struck, Aaron F.; Nair, Veena A.; Mathis, Jedidiah; Allen, Linda; Almane, Dace; Arkush, Karina; Birn, Rasmus M.; Conant, Lisa L.; DeYoe, Edgar A.; Felton, Elizabeth A.; Maganti, Rama; Nencka, Andrew S.; Raghavan, Manoj; Shah, Umang; Sosa, Veronica N.; Ustine, Candida; Prabhakaran, Vivek; Binder, Jeffrey R.; Meyerand, M. Elizabeth

doi:10.1016/j.yebeh.2020.107172

Cited by 10 publications

(5 citation statements)

References 70 publications

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“…Neuroticism is a commonly recognized predictor of depression and anxiety, which are also more frequent in patients with TLE. According to [120], patients with increased neuroticism with depression and anxiety symptoms, demonstrated both unique and com mon patterns of abnormal functional connectivity of rest ing networks between the mesial temporal and frontal lobes. For example, increased neuroticism was signifi cantly associated with hyposynchrony between the right hippocampus and the Brodmann area, and this unique relationship was independent of the symptoms of depres sion and anxiety.…”

Section: Changes In Neural Network Involved In the Comorbidity Of Epilepsy And Depressionmentioning

confidence: 99%

Stress-Associated Molecular and Cellular Hippocampal Mechanisms Common for Epilepsy and Comorbid Depressive Disorders

Gulyaeva

2021

Biochemistry Moscow

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The review discusses molecular and cellular mechanisms common to the temporal lobe epileptogenesis/epilepsy and depressive disorders. Comorbid temporal lobe epilepsy and depression are associated with dysfunction of the hypothalamic-pituitary-adrenocortical axis. Excessive glucocorticoids disrupt the function and impair the structure of the hippocampus, a brain region key to learning, memory, and emotions. Selective vulnerability of the hippocampus to stress, mediated by the reception of glucocorticoid hormones secreted during stress, is the price of the high functional plasticity and pleiotropy of this limbic structure. Common molecular and cellular mechanisms include the dysfunction of glucocorticoid receptors, neurotransmitters, and neurotrophic factors, development of neuroinflammation, leading to neurodegeneration and loss of hippocampal neurons, as well as disturbances in neurogenesis in the subgranular neurogenic niche and formation of aberrant neural networks. These glucocorticoid-dependent processes underlie altered stress response and the development of chronic stress-induced comorbid pathologies, in particular, temporal lobe epilepsy and depressive disorders.

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Section: Changes In Neural Network Involved In the Comorbidity Of Epilepsy And Depressionmentioning

confidence: 99%

Stress-Associated Molecular and Cellular Hippocampal Mechanisms Common for Epilepsy and Comorbid Depressive Disorders

Gulyaeva

2021

Biochemistry Moscow

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“…Medical conditions in our patient cohort, including bipolar disorder, anxiety, migraines and hypothyroidism, may associate with abnormal FC. For example, personality traits that are predictors of depression and anxiety have been found to be more common among mesial temporal lobe epilepsy patients and have been associated with decreased frontotemporal synchronization on rs-fMRI analysis [34]. In our cohort, patients 5-7 had more underlying health concerns, had worse surgical outcomes, and had the most variable FC.…”

Section: Discussionmentioning

confidence: 92%

Preoperative functional connectivity by magnetic resonance imaging for refractory neocortical epilepsy

Lee

Hacker

Park

et al. 2023

Preprint

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Objective: Patients with refractory epilepsy experience extensive and invasive clinical testing for seizure onset zones treatable by surgical resection. However, surgical resection can fail to provide therapeutic benefit, and patients with neocortical epilepsy have the poorest therapeutic outcomes. This case series studied patients with neocortical epilepsy who were referred for surgical treatment. Prior to surgery, patients volunteered for resting-state functional magnetic resonance imaging (rs-fMRI) in addition to imaging for the clinical standard of care. This work examined the variability of functional connectivity in patients, estimated from rs-fMRI, for associations with surgical outcomes. Methods: This work examined pre-operative structural imaging, pre-operative rs-fMRI, and post-operative structural imaging from seven epilepsy patients. Review of the clinical record provided Engel classifications for surgical outcomes. A novel method assessed pre-operative rs-fMRI from patients using comparative rs-fMRI from a large cohort of healthy control subjects and estimated Gibbs distributions for functional connectivity in patients compared to healthy controls. Results: Three patients had Engel classification Ia, one patient had Engel classification IIa, and three patients had Engel classification IV. Metrics for variability of functional connectivity, including absolute differences of the functional connectivity of each patient from healthy control averages and probabilistic scores for absolute differences, were higher for patients classified as Engel IV, for whom epilepsy surgery provided no meaningful improvement. Significance: This work continues on-going efforts to use rs-fMRI to characterize abnormal functional connectivity in the brain. Preliminary evidence indicates that the topography of variant functional connectivity in epilepsy patients may be clinically relevant for identifying patients unlikely to have favorable outcomes after epilepsy surgery. Widespread topographic variations of functional connectivity also support the hypothesis that epilepsy is a disease of brain resting-state networks.

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“…Fronto-limbic involvement was also suggested by one study relating resting-state fMRI connectivity measures to measures of neuroticism, depression, and anxiety ( Doucet et al, 2013 ). The authors showed that neuroticism, a personality trait that is associated with depressive symptoms relates to atypical functional connectivity between mesiotemporal and frontal lobe regions, with connectivity alterations that were partially overlapping to those related to depression and anxiety symptoms ( Rivera Bonet et al, 2020 ). In an earlier study, the authors also reported associations between affective symptoms and reductions in gray matter volumes, again targeting both frontal and temporal neocortices, as well as mesiotemporal lobe structures such as the hippocampus and amygdala ( Rivera Bonet et al, 2019 ).…”

Section: Temporal Lobe Epilepsymentioning

confidence: 99%

Multimodal connectome biomarkers of cognitive and affective dysfunction in the common epilepsies

Rodríguez‐Cruces

Royer

Larivière

et al. 2022

Network Neuroscience

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Epilepsy is one of the most common chronic neurological conditions, traditionally defined as a disorder of recurrent seizures. Cognitive and affective dysfunctions are increasingly recognized as core disease dimensions and can affect patient wellbeing sometimes more than the seizures themselves. Connectome-based approaches hold immense promise for revealing mechanisms that contribute to dysfunction, and to identify biomarkers. Our review discusses emerging multimodal neuroimaging and connectomics studies that highlight network substrates of cognitive/affective dysfunction in the common epilepsies. We first overview work in drug-resistant epilepsy syndromes i.e., temporal lobe epilepsy related to mesiotemporal sclerosis (TLE) and extratemporal epilepsy (ETE) related to malformations of cortical development. While these are traditionally conceptualized as ‘focal’ epilepsies, many patients present with broad structural and functional anomalies. Moreover, the extent of distributed changes contributes to difficulties in multiple cognitive domains as well as affective-behavioral challenges. We will also review work in idiopathic generalized epilepsy (IGE), a class of generalized epilepsy syndromes that involve subcortico-cortical circuits. Overall, neuroimaging and network neuroscience studies point to both shared and syndrome specific connectome signatures of dysfunction across TLE, ETE, and IGE. Lastly, we point to current gaps in the literature and formulate recommendations for future research.

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Neuroticism in temporal lobe epilepsy is associated with altered limbic-frontal lobe resting-state functional connectivity

Cited by 10 publications

References 70 publications

Stress-Associated Molecular and Cellular Hippocampal Mechanisms Common for Epilepsy and Comorbid Depressive Disorders

Stress-Associated Molecular and Cellular Hippocampal Mechanisms Common for Epilepsy and Comorbid Depressive Disorders

Preoperative functional connectivity by magnetic resonance imaging for refractory neocortical epilepsy

Multimodal connectome biomarkers of cognitive and affective dysfunction in the common epilepsies

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