Quantitative cellular pathology of the amygdala in temporal lobe epilepsy and correlation with magnetic resonance imaging volumetry, tissue microstructure, and sudden unexpected death in epilepsy risk factors

Author:

Lam Hou Wang1,Patodia Smriti1,Zeicu Claudia1ORCID,Lim Yau Mun2,Mrzyglod Alicja1,Scott Catherine13,Oliveira Joana13ORCID,De Tisi Jane1,Legouhy Antoine4,Zhang Hui4,Koepp Matthias1ORCID,Diehl Beate13ORCID,Thom Maria12ORCID

Affiliation:

1. Department of Clinical and Experimental Epilepsy University College London (UCL) Queen Square Institute of Neurology London UK

2. Division of Neuropathology, UCL Queen Square Institute of Neurology and National Hospital for Neurology and Neurosurgery University College Hospitals NHS Foundation Trust London UK

3. Department of Clinical Neurophysiology, National Hospital for Neurology and Neurosurgery University College Hospitals NHS Foundation Trust London UK

4. Centre for Medical Image Computing, Department of Computer Science University College London London UK

Abstract

AbstractObjectiveAmygdala enlargement can occur in temporal lobe epilepsy, and increased amygdala volume is also reported in sudden unexpected death in epilepsy (SUDEP). Apnea can be induced by amygdala stimulation, and postconvulsive central apnea (PCCA) and generalized seizures are both known SUDEP risk factors. Neurite orientation dispersion and density imaging (NODDI) has recently provided additional information on altered amygdala microstructure in SUDEP. In a series of 24 surgical temporal lobe epilepsy cases, our aim was to quantify amygdala cellular pathology parameters that could predict enlargement, NODDI changes, and ictal respiratory dysfunction.MethodsUsing whole slide scanning automated quantitative image analysis methods, parallel evaluation of myelin, axons, dendrites, oligodendroglia, microglia, astroglia, neurons, serotonergic networks, mTOR‐pathway activation (pS6) and phosphorylated tau (pTau; AT8, AT100, PHF) in amygdala, periamygdala cortex, and white matter regions of interest were compared with preoperative magnetic resonance imaging data on amygdala size, and in 13 cases with NODDI and evidence of ictal‐associated apnea.ResultsWe observed significantly higher glial labeling (Iba1, glial fibrillary acidic protein, Olig2) in amygdala regions compared to cortex and a strong positive correlation between Olig2 and Iba1 in the amygdala. Larger amygdala volumes correlated with lower microtubule‐associated protein (MAP2), whereas higher NODDI orientation dispersion index correlated with lower Olig2 cell densities. In the three cases with recorded PCCA, higher MAP2 and pS6‐235 expression was noted than in those without. pTau did not correlate with SUDEP risk factors, including seizure frequency.SignificanceHistological quantitation of amygdala microstructure can shed light on enlargement and diffusion imaging alterations in epilepsy to explore possible mechanisms of amygdala dysfunction, including mTOR pathway activation, that in turn may increase the risk for SUDEP.

Funder

Wellcome Trust

Publisher

Wiley

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