Microangiopathy in temporal lobe epilepsy with diffusion MRI alterations and cognitive decline.
Cognitive decline
Diffusion MRI
Fixel-based analysis
Microangiopathy
Temporal lobe epilepsy
White matter
Journal
Acta neuropathologica
ISSN: 1432-0533
Titre abrégé: Acta Neuropathol
Pays: Germany
ID NLM: 0412041
Informations de publication
Date de publication:
08 Oct 2024
08 Oct 2024
Historique:
received:
01
08
2024
accepted:
28
09
2024
revised:
23
09
2024
medline:
8
10
2024
pubmed:
8
10
2024
entrez:
8
10
2024
Statut:
epublish
Résumé
White matter microvascular alterations in temporal lobe epilepsy (TLE) may be relevant to acquired neurodegenerative processes and cognitive impairments associated with this condition. We quantified microvascular changes, myelin, axonal, glial and extracellular-matrix labelling in the gyral core and deep temporal lobe white matter regions in surgical resections from 44 TLE patients with or without hippocampal sclerosis. We compared this pathology data with in vivo pre-operative MRI diffusion measurements in co-registered regions and neuropsychological measures of cognitive impairment and decline. In resections, increased arteriolosclerosis was observed in TLE compared to non-epilepsy controls (greater sclerotic index, p < 0.001), independent of age. Microvascular changes included increased vascular densities in some regions but uniformly reduced mean vascular size (quantified with collagen-4, p < 0.05-0.0001), and increased pericyte coverage of small vessels and capillaries particularly in deep white matter (quantified with platelet-derived growth factor receptorβ and smooth muscle actin, p < 0.01) which was more marked the longer the duration of epilepsy (p < 0.05). We noted increased glial numbers (Olig2, Iba1) but reduced myelin (MAG, PLP) in TLE compared to controls, particularly prominent in deep white matter. Gene expression analysis showed a greater reduction of myelination genes in HS than non-HS cases and with age and correlation with diffusion MRI alterations. Glial densities and vascular size were increased with increased MRI diffusivity and vascular density with white matter abnormality quantified using fixel-based analysis. Increased perivascular space was associated with reduced fractional anisotropy as well as age-accelerated cognitive decline prior to surgery (p < 0.05). In summary, likely acquired microangiopathic changes in TLE, including vascular sclerosis, increased pericyte coverage and reduced small vessel size, may indicate a functional alteration in contractility of small vessels and haemodynamics that could impact on tissue perfusion. These morphological features correlate with white matter diffusion MRI alterations and might explain cognitive decline in TLE.
Identifiants
pubmed: 39377933
doi: 10.1007/s00401-024-02809-8
pii: 10.1007/s00401-024-02809-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
49Subventions
Organisme : Wellcome Trust
ID : 221934/Z/20/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 221934/Z/20/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 221934/Z/20/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 221934/Z/20/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 221934/Z/20/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 221934/Z/20/Z
Pays : United Kingdom
Informations de copyright
© 2024. The Author(s).
Références
Alarcon-Martinez L, Yemisci M, Dalkara T (2021) Pericyte morphology and function. Histol Histopathol 36:633–643. https://doi.org/10.14670/HH-18-314
doi: 10.14670/HH-18-314
pubmed: 33595091
Alonso-Nanclares L, DeFelipe J (2014) Alterations of the microvascular network in the sclerotic hippocampus of patients with temporal lobe epilepsy. Epilepsy Behav 38:48–52. https://doi.org/10.1016/j.yebeh.2013.12.009
doi: 10.1016/j.yebeh.2013.12.009
pubmed: 24406303
Arango-Lievano M, Boussadia B, De Terdonck LDT, Gault C, Fontanaud P, Lafont C et al (2018) Topographic reorganization of cerebrovascular mural cells under seizure conditions. Cell Rep 23:1045–1059. https://doi.org/10.1016/j.celrep.2018.03.110
doi: 10.1016/j.celrep.2018.03.110
pubmed: 29694884
Bankhead P, Loughrey MB, Fernandez JA, Dombrowski Y, McArt DG, Dunne PD et al (2017) QuPath: open source software for digital pathology image analysis. Sci Rep 7:16878. https://doi.org/10.1038/s41598-017-17204-5
doi: 10.1038/s41598-017-17204-5
pubmed: 29203879
pmcid: 5715110
Baxendale S, Thompson P (2020) The association of cognitive phenotypes with postoperative outcomes after epilepsy surgery in patients with temporal lobe epilepsy. Epilepsy Behav 112:107386. https://doi.org/10.1016/j.yebeh.2020.107386
doi: 10.1016/j.yebeh.2020.107386
pubmed: 32911298
Bell B, Lin JJ, Seidenberg M, Hermann B (2011) The neurobiology of cognitive disorders in temporal lobe epilepsy. Nat Rev Neurol 7:154–164. https://doi.org/10.1038/nrneurol.2011.3
doi: 10.1038/nrneurol.2011.3
pubmed: 21304484
Blevins BL, Vinters HV, Love S, Wilcock DM, Grinberg LT, Schneider JA et al (2021) Brain arteriolosclerosis. Acta Neuropathol 141:1–24. https://doi.org/10.1007/s00401-020-02235-6
doi: 10.1007/s00401-020-02235-6
pubmed: 33098484
Bonduelle T, Hartlieb T, Baldassari S, Sim NS, Kim SH, Kang HC et al (2021) Frequent SLC35A2 brain mosaicism in mild malformation of cortical development with oligodendroglial hyperplasia in epilepsy (MOGHE). Acta Neuropathol Commun 9:3. https://doi.org/10.1186/s40478-020-01085-3
doi: 10.1186/s40478-020-01085-3
pubmed: 33407896
pmcid: 7788938
Concha L, Livy DJ, Beaulieu C, Wheatley BM, Gross DW (2010) In vivo diffusion tensor imaging and histopathology of the fimbria-fornix in temporal lobe epilepsy. J Neurosci 30:996–1002. https://doi.org/10.1523/JNEUROSCI.1619-09.2010
doi: 10.1523/JNEUROSCI.1619-09.2010
pubmed: 20089908
pmcid: 6633109
Craggs LJ, Hagel C, Kuhlenbaeumer G, Borjesson-Hanson A, Andersen O, Viitanen M et al (2013) Quantitative vascular pathology and phenotyping familial and sporadic cerebral small vessel diseases. Brain Pathol 23:547–557. https://doi.org/10.1111/bpa.12041
doi: 10.1111/bpa.12041
pubmed: 23387519
pmcid: 8029230
Deleo F, Thom M, Concha L, Bernasconi A, Bernhardt BC, Bernasconi N (2018) Histological and MRI markers of white matter damage in focal epilepsy. Epilepsy Res 140:29–38. https://doi.org/10.1016/j.eplepsyres.2017.11.010
doi: 10.1016/j.eplepsyres.2017.11.010
pubmed: 29227798
Demerath T, Donkels C, Reisert M, Heers M, Rau A, Schroter N et al (2022) Gray-White matter blurring of the temporal pole associated with hippocampal sclerosis: a microstructural study involving 3 T MRI and ultrastructural histopathology. Cereb Cortex 32:1882–1893. https://doi.org/10.1093/cercor/bhab320
doi: 10.1093/cercor/bhab320
pubmed: 34515307
Dhollander T, Clemente A, Singh M, Boonstra F, Civier O, Duque JD et al (2021) Fixel-based analysis of diffusion MRI: methods, applications challenges and opportunities. Neuroimage 241:118417. https://doi.org/10.1016/j.neuroimage.2021.118417
doi: 10.1016/j.neuroimage.2021.118417
pubmed: 34298083
Ding R, Hase Y, Ameen-Ali KE, Ndung’u M, Stevenson W, Barsby J et al (2020) Loss of capillary pericytes and the blood-brain barrier in white matter in poststroke and vascular dementias and Alzheimer’s disease. Brain Pathol 30:1087–1101. https://doi.org/10.1111/bpa.12888
doi: 10.1111/bpa.12888
pubmed: 32705757
pmcid: 8018063
Doerrfuss JI, Hebel JM, Holtkamp M (2023) Epileptogenicity of white matter lesions in cerebral small vessel disease: a systematic review and meta-analysis. J Neurol 270:4890–4902. https://doi.org/10.1007/s00415-023-11828-6
doi: 10.1007/s00415-023-11828-6
pubmed: 37341807
pmcid: 10511556
Donkels C, Pfeifer D, Janz P, Huber S, Nakagawa J, Prinz M et al (2017) Whole transcriptome screening reveals myelination deficits in dysplastic human temporal neocortex. Cereb Cortex 27(2):1558–1572. https://doi.org/10.1093/cercor/bhv346
doi: 10.1093/cercor/bhv346
pubmed: 26796214
Drenthen GS, Backes WH, Aldenkamp AP, Vermeulen RJ, Klinkenberg S, Jansen JFA (2020) On the merits of non-invasive myelin imaging in epilepsy, a literature review. J Neurosci Methods 338:108687. https://doi.org/10.1016/j.jneumeth.2020.108687
doi: 10.1016/j.jneumeth.2020.108687
pubmed: 32173402
Fang C, Magaki SD, Kim RC, Kalaria RN, Vinters HV, Fisher M (2023) Arteriolar neuropathology in cerebral microvascular disease. Neuropathol Appl Neurobiol 49:e12875. https://doi.org/10.1111/nan.12875
doi: 10.1111/nan.12875
pubmed: 36564356
pmcid: 10350910
Fischl B (2012) FreeSurfer. Neuroimage 62:774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021
doi: 10.1016/j.neuroimage.2012.01.021
pubmed: 22248573
Garbelli R, de Bock F, Medici V, Rousset MC, Villani F, Boussadia B et al (2015) PDGFRbeta(+) cells in human and experimental neuro-vascular dysplasia and seizures. Neuroscience 306:18–27. https://doi.org/10.1016/j.neuroscience.2015.07.090
doi: 10.1016/j.neuroscience.2015.07.090
pubmed: 26283024
Garbelli R, Milesi G, Medici V, Villani F, Didato G, Deleo F et al (2012) Blurring in patients with temporal lobe epilepsy: clinical, high-field imaging and ultrastructural study. Brain 135:2337–2349. https://doi.org/10.1093/brain/aws149
doi: 10.1093/brain/aws149
pubmed: 22734123
Gonzales AL, Klug NR, Moshkforoush A, Lee JC, Lee FK, Shui B et al (2020) Contractile pericytes determine the direction of blood flow at capillary junctions. Proc Natl Acad Sci U S A 117:27022–27033. https://doi.org/10.1073/pnas.1922755117
doi: 10.1073/pnas.1922755117
pubmed: 33051294
pmcid: 7604512
Gordon BA (2020) Neurofilaments in disease: what do we know? Curr Opin Neurobiol 61:105–115
doi: 10.1016/j.conb.2020.02.001
pubmed: 32151970
pmcid: 7198337
Gruber VE, Lang J, Endmayr V, Diehm R, Pimpel B, Glatter S et al (2021) Impaired myelin production due to an intrinsic failure of oligodendrocytes in mTORpathies. Neuropathol Appl Neurobiol 47:812–825. https://doi.org/10.1111/nan.12744
doi: 10.1111/nan.12744
pubmed: 34173252
pmcid: 8518586
Hatton SN, Huynh KH, Bonilha L, Abela E, Alhusaini S, Altmann A et al (2020) White matter abnormalities across different epilepsy syndromes in adults: an ENIGMA-Epilepsy study. Brain. https://doi.org/10.1093/brain/awaa200
doi: 10.1093/brain/awaa200
pubmed: 32814957
pmcid: 7567169
Hatton SN, Huynh KH, Bonilha L, Abela E, Alhusaini S, Altmann A et al (2020) White matter abnormalities across different epilepsy syndromes in adults: an ENIGMA-Epilepsy study. Brain 143:2454–2473. https://doi.org/10.1093/brain/awaa200
doi: 10.1093/brain/awaa200
pubmed: 32814957
pmcid: 7567169
Hildebrandt M, Amann K, Schroder R, Pieper T, Kolodziejczyk D, Holthausen H et al (2008) White matter angiopathy is common in pediatric patients with intractable focal epilepsies. Epilepsia 49:804–815. https://doi.org/10.1111/j.1528-1167.2007.01514.x
doi: 10.1111/j.1528-1167.2007.01514.x
pubmed: 18266747
Hirunpattarasilp C, Attwell D, Freitas F (2019) The role of pericytes in brain disorders: from the periphery to the brain. J Neurochem 150:648–665. https://doi.org/10.1111/jnc.14725
doi: 10.1111/jnc.14725
pubmed: 31106417
Jayakumar AR, Apeksha A, Norenberg MD (2017) Role of matricellular proteins in disorders of the central nervous system. Neurochem Res 42(3):858–875
doi: 10.1007/s11064-016-2088-5
pubmed: 27878658
Kalaria RN (2018) The pathology and pathophysiology of vascular dementia. Neuropharmacology 134:226–239. https://doi.org/10.1016/j.neuropharm.2017.12.030
doi: 10.1016/j.neuropharm.2017.12.030
pubmed: 29273521
Kasper BS, Paulus W (2004) Perivascular clustering in temporal lobe epilepsy: oligodendroglial cells of unknown function. Acta Neuropathol 108:471–475. https://doi.org/10.1007/s00401-004-0914-3
doi: 10.1007/s00401-004-0914-3
pubmed: 15480711
Keren-Aviram G, Dachet F, Bagla S, Balan K, Loeb JA, Dratz EA (2018) Proteomic analysis of human epileptic neocortex predicts vascular and glial changes in epileptic regions. PLoS ONE 13:e0195639. https://doi.org/10.1371/journal.pone.0195639
doi: 10.1371/journal.pone.0195639
pubmed: 29634780
pmcid: 5892923
Kim HW, Hong J, Jeon JC (2020) Cerebral small vessel disease and alzheimer’s disease: a review. Front Neurol 11:927. https://doi.org/10.3389/fneur.2020.00927
doi: 10.3389/fneur.2020.00927
pubmed: 32982937
pmcid: 7477392
Klement W, Blaquiere M, Zub E, deBock F, Boux F, Barbier E et al (2019) A pericyte-glia scarring develops at the leaky capillaries in the hippocampus during seizure activity. Epilepsia 60:1399–1411. https://doi.org/10.1111/epi.16019
doi: 10.1111/epi.16019
pubmed: 31135065
Knowles JK, Batra A, Xu H, Monje M (2022) Adaptive and maladaptive myelination in health and disease. Nat Rev Neurol 18:735–746. https://doi.org/10.1038/s41582-022-00737-3
doi: 10.1038/s41582-022-00737-3
pubmed: 36376595
Knowles JK, Xu H, Soane C, Batra A, Saucedo T, Frost E et al (2022) Maladaptive myelination promotes generalized epilepsy progression. Nat Neurosci 25:596–606. https://doi.org/10.1038/s41593-022-01052-2
doi: 10.1038/s41593-022-01052-2
pubmed: 35501379
pmcid: 9076538
Leal-Campanario R, Alarcon-Martinez L, Rieiro H, Martinez-Conde S, Alarcon-Martinez T, Zhao X et al (2017) Abnormal capillary vasodynamics contribute to ictal neurodegeneration in epilepsy. Sci Rep 7:43276. https://doi.org/10.1038/srep43276
doi: 10.1038/srep43276
pubmed: 28240297
pmcid: 5327474
Li Y, Liu P, Lin Q, Zhou D, An D (2023) Postoperative seizure and memory outcome of temporal lobe epilepsy with hippocampal sclerosis: a systematic review. Epilepsia 64:2845–2860. https://doi.org/10.1111/epi.17757
doi: 10.1111/epi.17757
pubmed: 37611927
Liu M, Bernhardt BC, Hong SJ, Caldairou B, Bernasconi A, Bernasconi N (2016) The superficial white matter in temporal lobe epilepsy: a key link between structural and functional network disruptions. Brain 139:2431–2440. https://doi.org/10.1093/brain/aww167
doi: 10.1093/brain/aww167
pubmed: 27357350
pmcid: 4995361
Liwnicz BH, Leach JL, Yeh HS, Privitera M (1990) Pericyte degeneration and thickening of basement membranes of cerebral microvessels in complex partial seizures: electron microscopic study of surgically removed tissue. Neurosurgery 26:409–420. https://doi.org/10.1097/00006123-199003000-00006
doi: 10.1097/00006123-199003000-00006
pubmed: 2320209
Lockwood-Estrin G, Thom M, Focke NK, Symms MR, Martinian L, Sisodiya SM et al (2012) Correlating 3T MRI and histopathology in patients undergoing epilepsy surgery. J Neurosci Methods 205:182–189. https://doi.org/10.1016/j.jneumeth.2011.12.014
doi: 10.1016/j.jneumeth.2011.12.014
pubmed: 22227441
Marchi N, Lerner-Natoli M (2013) Cerebrovascular remodeling and epilepsy. Neuroscientist 19:304–312. https://doi.org/10.1177/1073858412462747
doi: 10.1177/1073858412462747
pubmed: 23072899
Milesi S, Boussadia B, Plaud C, Catteau M, Rousset MC, De Bock F et al (2014) Redistribution of PDGFRbeta cells and NG2DsRed pericytes at the cerebrovasculature after status epilepticus. Neurobiol Dis 71:151–158. https://doi.org/10.1016/j.nbd.2014.07.010
doi: 10.1016/j.nbd.2014.07.010
pubmed: 25088711
Miners JS, Palmer JC, Love S (2016) Pathophysiology of hypoperfusion of the precuneus in early alzheimer’s disease. Brain Pathol 26:533–541. https://doi.org/10.1111/bpa.12331
doi: 10.1111/bpa.12331
pubmed: 26452729
Mito R, Pedersen M, Pardoe H, Parker D, Smith RE, Cameron J et al (2024) Exploring individual fixel-based white matter abnormalities in epilepsy. Brain Commun 6:fcad352. https://doi.org/10.1093/braincomms/fcad352
doi: 10.1093/braincomms/fcad352
pubmed: 38187877
O’Brien JT, Thomas A (2015) Vascular dementia. Lancet 386:1698–1706. https://doi.org/10.1016/S0140-6736(15)00463-8
doi: 10.1016/S0140-6736(15)00463-8
pubmed: 26595643
Ohi K, Sumiyoshi C, Fujino H, Yasuda Y, Yamamori H, Fujimoto M et al (2017) A brief assessment of intelligence decline in schizophrenia as represented by the difference between current and premorbid intellectual quotient. Front Psychiatry 8:293. https://doi.org/10.3389/fpsyt.2017.00293
doi: 10.3389/fpsyt.2017.00293
pubmed: 29312019
pmcid: 5743746
Olesen JB, Abildstrom SZ, Erdal J, Gislason GH, Weeke P, Andersson C et al (2011) Effects of epilepsy and selected antiepileptic drugs on risk of myocardial infarction, stroke, and death in patients with or without previous stroke: a nationwide cohort study. Pharmacoepidemiol Drug Saf 20:964–971. https://doi.org/10.1002/pds.2186
doi: 10.1002/pds.2186
pubmed: 21766386
Ozdogmus O, Cavdar S, Ersoy Y, Ercan F, Uzun I (2009) A preliminary study, using electron and light-microscopic methods, of axon numbers in the fornix in autopsies of patients with temporal lobe epilepsy. Anat Sci Int 84:2–6. https://doi.org/10.1007/s12565-008-0001-2
doi: 10.1007/s12565-008-0001-2
pubmed: 19214658
Pachitariu M, Stringer C (2022) Cellpose 2.0: how to train your own model. Nat Methods 19:1634–1641. https://doi.org/10.1038/s41592-022-01663-4
doi: 10.1038/s41592-022-01663-4
pubmed: 36344832
pmcid: 9718665
Prager O, Kamintsky L, Hasam-Henderson LA, Schoknecht K, Wuntke V, Papageorgiou I et al (2019) Seizure-induced microvascular injury is associated with impaired neurovascular coupling and blood-brain barrier dysfunction. Epilepsia 60:322–336. https://doi.org/10.1111/epi.14631
doi: 10.1111/epi.14631
pubmed: 30609012
Raffelt DA, Smith RE, Ridgway GR, Tournier JD, Vaughan DN, Rose S et al (2015) Connectivity-based fixel enhancement: Whole-brain statistical analysis of diffusion MRI measures in the presence of crossing fibres. Neuroimage 117:40–55. https://doi.org/10.1016/j.neuroimage.2015.05.039
doi: 10.1016/j.neuroimage.2015.05.039
pubmed: 26004503
Raffelt DA, Tournier JD, Smith RE, Vaughan DN, Jackson G, Ridgway GR et al (2017) Investigating white matter fibre density and morphology using fixel-based analysis. Neuroimage 144:58–73. https://doi.org/10.1016/j.neuroimage.2016.09.029
doi: 10.1016/j.neuroimage.2016.09.029
pubmed: 27639350
Reeves C, Pradim-Jardim A, Sisodiya SM, Thom M, Liu JYW (2019) Spatiotemporal dynamics of PDGFRbeta expression in pericytes and glial scar formation in penetrating brain injuries in adults. Neuropathol Appl Neurobiol 45:609–627. https://doi.org/10.1111/nan.12539
doi: 10.1111/nan.12539
pubmed: 30636077
pmcid: 6767497
Reiss Y, Bauer S, David B, Devraj K, Fidan E, Hattingen E et al (2023) The neurovasculature as a target in temporal lobe epilepsy. Brain Pathol 33:e13147. https://doi.org/10.1111/bpa.13147
doi: 10.1111/bpa.13147
pubmed: 36599709
pmcid: 10041171
Reiter JT, Schulte F, Bauer T, David B, Endler C, Isaak A et al (2024) Evidence for interictal blood-brain barrier dysfunction in people with epilepsy. Epilepsia 65:1462–1474. https://doi.org/10.1111/epi.17929
doi: 10.1111/epi.17929
pubmed: 38436479
Reyes A, Kaestner E, Bahrami N, Balachandra A, Hegde M, Paul BM et al (2019) Cognitive phenotypes in temporal lobe epilepsy are associated with distinct patterns of white matter network abnormalities. Neurology 92:e1957–e1968. https://doi.org/10.1212/WNL.0000000000007370
doi: 10.1212/WNL.0000000000007370
pubmed: 30918094
pmcid: 6511080
Riba M, Del Valle J, Molina-Porcel L, Pelegri C, Vilaplana J (2022) Wasteosomes (Corpora amylacea) as a hallmark of chronic glymphatic insufficiency. Proc Natl Acad Sci U S A 119:e2211326119. https://doi.org/10.1073/pnas.2211326119
doi: 10.1073/pnas.2211326119
pubmed: 36409907
pmcid: 9860256
Rigau V, Morin M, Rousset MC, de Bock F, Lebrun A, Coubes P et al (2007) Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 130:1942–1956. https://doi.org/10.1093/brain/awm118
doi: 10.1093/brain/awm118
pubmed: 17533168
Rogers MA, Fantauzzo KA (2020) The emerging complexity of PDGFRs: activation, internalization and signal attenuation. Biochem Soc Trans 48:1167–1176. https://doi.org/10.1042/BST20200004
doi: 10.1042/BST20200004
pubmed: 32369556
pmcid: 7722362
Ruber T, David B, Luchters G, Nass RD, Friedman A, Surges R et al (2018) Evidence for peri-ictal blood-brain barrier dysfunction in patients with epilepsy. Brain 141:2952–2965. https://doi.org/10.1093/brain/awy242
doi: 10.1093/brain/awy242
pubmed: 30239618
Sakuma S, Halliday WC, Nomura R, Ochi A, Otsubo H (2014) Increased population of oligodendroglia-like cells in pediatric intractable epilepsy. Neurosci Lett 566:188–193. https://doi.org/10.1016/j.neulet.2014.03.002
doi: 10.1016/j.neulet.2014.03.002
pubmed: 24631559
Shepherd C, Liu J, Goc J, Martinian L, Jacques TS, Sisodiya SM et al (2013) A quantitative study of white matter hypomyelination and oligodendroglial maturation in focal cortical dysplasia type II. Epilepsia 54:898–908. https://doi.org/10.1111/epi.12143
doi: 10.1111/epi.12143
pubmed: 23551043
pmcid: 4165267
Smyth LCD, Highet B, Jansson D, Wu J, Rustenhoven J, Aalderink M et al (2022) Characterisation of PDGF-BB:PDGFRbeta signalling pathways in human brain pericytes: evidence of disruption in Alzheimer’s disease. Commun Biol 5:235. https://doi.org/10.1038/s42003-022-03180-8
doi: 10.1038/s42003-022-03180-8
pubmed: 35301433
pmcid: 8931009
Smyth LCD, Rustenhoven J, Scotter EL, Schweder P, Faull RLM, Park TIH et al (2018) Markers for human brain pericytes and smooth muscle cells. J Chem Neuroanat 92:48–60. https://doi.org/10.1016/j.jchemneu.2018.06.001
doi: 10.1016/j.jchemneu.2018.06.001
pubmed: 29885791
Stefanits H, Czech T, Pataraia E, Baumgartner C, Derhaschnig N, Slana A et al (2012) Prominent oligodendroglial response in surgical specimens of patients with temporal lobe epilepsy. Clin Neuropathol 31:409–417. https://doi.org/10.5414/np300536
doi: 10.5414/np300536
pubmed: 23083461
Stringer C, Wang T, Michaelos M, Pachitariu M (2021) Cellpose: a generalist algorithm for cellular segmentation. Nat Methods 18:100–106. https://doi.org/10.1038/s41592-020-01018-x
doi: 10.1038/s41592-020-01018-x
pubmed: 33318659
Swissa E, Serlin Y, Vazana U, Prager O, Friedman A (2019) Blood-brain barrier dysfunction in status epileptics: mechanisms and role in epileptogenesis. Epilepsy Behav 101:106285. https://doi.org/10.1016/j.yebeh.2019.04.038
doi: 10.1016/j.yebeh.2019.04.038
pubmed: 31711869
Szklarczyk D, Kirsch R, Koutrouli M, Nastou K, Mehryary F, Hachilif R et al (2023) The STRING database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res 51:D638–D646. https://doi.org/10.1093/nar/gkac1000
doi: 10.1093/nar/gkac1000
pubmed: 36370105
Tai XY, Koepp M, Duncan JS, Fox N, Thompson P, Baxendale S et al (2016) Hyperphosphorylated tau in patients with refractory epilepsy correlates with cognitive decline: a study of temporal lobe resections. Brain 139:2441–2455. https://doi.org/10.1093/brain/aww187
doi: 10.1093/brain/aww187
pubmed: 27497924
pmcid: 5926008
Uemura MT, Maki T, Ihara M, Lee VMY, Trojanowski JQ (2020) Brain microvascular pericytes in vascular cognitive impairment and dementia. Front Aging Neurosci 12:80. https://doi.org/10.3389/fnagi.2020.00080
doi: 10.3389/fnagi.2020.00080
pubmed: 32317958
pmcid: 7171590
Urquia-Osorio H, Pimentel-Silva LR, Rezende TJR, Almendares-Bonilla E, Yasuda CL, Concha L et al (2022) Superficial and deep white matter diffusion abnormalities in focal epilepsies. Epilepsia 63:2312–2324. https://doi.org/10.1111/epi.17333
doi: 10.1111/epi.17333
pubmed: 35707885
van Lanen RH, Melchers S, Hoogland G, Schijns OE, Zandvoort MAV, Haeren RH et al (2021) Microvascular changes associated with epilepsy: a narrative review. J Cereb Blood Flow Metab 41:2492–2509. https://doi.org/10.1177/0271678X211010388
doi: 10.1177/0271678X211010388
pubmed: 33866850
pmcid: 8504411
Vazquez-Liebanas E, Nahar K, Bertuzzi G, Keller A, Betsholtz C, Mae MA (2022) Adult-induced genetic ablation distinguishes PDGFB roles in blood-brain barrier maintenance and development. J Cereb Blood Flow Metab 42:264–279. https://doi.org/10.1177/0271678X211056395
doi: 10.1177/0271678X211056395
pubmed: 34689641
Veersema TJ, de Neef A, van Scheppingen J, Ferrier CH, van Eijsden P, Gosselaar PH et al (2019) Changes in vascular density in resected tissue of 97 patients with mild malformation of cortical development, focal cortical dysplasia or TSC-related cortical tubers. Int J Dev Neurosci 79:96–104. https://doi.org/10.1016/j.ijdevneu.2019.11.003
doi: 10.1016/j.ijdevneu.2019.11.003
pubmed: 31770571
Verghese JP, Terry A, de Natale ER, Politis M (2022) Research evidence of the role of the glymphatic system and its potential pharmacological modulation in neurodegenerative diseases. J Clin Med. https://doi.org/10.3390/jcm11236964
doi: 10.3390/jcm11236964
pubmed: 36498538
pmcid: 9735716
Vos SB, Winston GP, Goodkin O, Pemberton HG, Barkhof F, Prados F et al (2020) Hippocampal profiling: Localized magnetic resonance imaging volumetry and T2 relaxometry for hippocampal sclerosis. Epilepsia 61:297–309. https://doi.org/10.1111/epi.16416
doi: 10.1111/epi.16416
pubmed: 31872873
Wang Y, Zuo H, Li W, Wu X, Zhou F, Chen X et al (2024) Cerebral small vessel disease increases risk for epilepsy: a Mendelian randomization study. Neurol Sci 45:2171–2180. https://doi.org/10.1007/s10072-023-07221-w
doi: 10.1007/s10072-023-07221-w
pubmed: 38012465
Wardlaw JM, Benveniste H, Nedergaard M, Zlokovic BV, Mestre H, Lee H et al (2020) Perivascular spaces in the brain: anatomy, physiology and pathology. Nat Rev Neurol 16:137–153. https://doi.org/10.1038/s41582-020-0312-z
doi: 10.1038/s41582-020-0312-z
pubmed: 32094487
Wieser HG, Blume WT, Fish D, Goldensohn E, Hufnagel A, King D et al (2001) ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia 42:282–286
doi: 10.1046/j.1528-1157.2001.4220282.x
pubmed: 11240604
Winston GP, Vos SB, Caldairou B, Hong SJ, Czech M, Wood TC et al (2020) Microstructural imaging in temporal lobe epilepsy: diffusion imaging changes relate to reduced neurite density. Neuroimage Clin 26:102231. https://doi.org/10.1016/j.nicl.2020.102231
doi: 10.1016/j.nicl.2020.102231
pubmed: 32146320
pmcid: 7063236
Witt JA, Coras R, Schramm J, Becker AJ, Elger CE, Blumcke I et al (2015) Relevance of hippocampal integrity for memory outcome after surgical treatment of mesial temporal lobe epilepsy. J Neurol 262:2214–2224. https://doi.org/10.1007/s00415-015-7831-3
doi: 10.1007/s00415-015-7831-3
pubmed: 26138541
Xie K, Royer J, Lariviere S, Rodriguez-Cruces R, Frassle S, Cabalo DG et al (2023) Atypical connectome topography and signal flow in temporal lobe epilepsy. bioRxiv. https://doi.org/10.1101/2023.05.23.541934
doi: 10.1101/2023.05.23.541934
pubmed: 38234827
pmcid: 10793399
Yuan A, Rao MV, Veeranna, Nixon RA (2017) Neurofilaments and neurofilament proteins in health and disease. Cold Spring Harb Perspect Biol 9(4):a018309
doi: 10.1101/cshperspect.a018309
pubmed: 28373358
pmcid: 5378049
Zambach SA, Cai C, Helms HCC, Hald BO, Dong Y, Fordsmann JC et al (2021) Precapillary sphincters and pericytes at first-order capillaries as key regulators for brain capillary perfusion. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.2023749118
doi: 10.1073/pnas.2023749118
pubmed: 34155102
pmcid: 8255959
Zhao X, Zhou Y, Li Y, Huang S, Zhu H, Zhou Z et al (2023) The asymmetry of glymphatic system dysfunction in patients with temporal lobe epilepsy: a DTI-ALPS study. J Neuroradiol. https://doi.org/10.1016/j.neurad.2023.05.009
doi: 10.1016/j.neurad.2023.05.009
pubmed: 37844660