Distinct limbic connectivity in left and right benign mesial temporal lobe epilepsy: Evidence from a resting state functional MRI study.

drug sensitive limbic connectivity mesial temporal epilepsy neuropsychological data resting state—fMRI

Journal

Frontiers in neurology
ISSN: 1664-2295
Titre abrégé: Front Neurol
Pays: Switzerland
ID NLM: 101546899

Informations de publication

Date de publication:
2022
Historique:
received: 14 05 2022
accepted: 12 09 2022
entrez: 17 10 2022
pubmed: 18 10 2022
medline: 18 10 2022
Statut: epublish

Résumé

Functional connectivity (FC) studies showed that pharmaco-resistant mesial temporal lobe epilepsy (MTLE) affects not only the limbic system, but also several extra-limbic regions, including areas belonging to resting state networks. Less is known about FC in subjects with benign MTLE (i.e., sensitive to antiseizure medication, bMTLE). We evaluated FC of hippocampus and amygdala in subjects with bMTLE, distinguished based on the epileptic focus lateralization. We enrolled 19 patients (10 with left and 9 with right bMTLE) and 10 age-matched healthy subjects. Connectivity was investigated at rest by using a seed-based regression analyses approach with four regions of interest (left and right hippocampus, left and right amygdala). Patients were also tested with a neuropsychological battery and their scores were correlated with fMRI data. Our study documented an asymmetrical disruption of FC in bMTLE, in relation to the side of the focus. Right subjects only exhibited limited altered connections, while left subjects-who performed worse in verbal memory tests-showed a wide bilateral hypoconnectivity of hippocampus and amygdala with areas belonging to language and memory network. The strength of FC between left limbic areas and language and memory network correlated with better performances in verbal memory tests. Moreover, we observed an increased FC with areas of default mode network, more pronounced in left subjects, a possible attempt to compensate cognitive deficit but without effectiveness.We believe that these findings could help to better characterize bMTLE, in which a dysfunction of limbic connectivity is detectable despite well-controlled epilepsy.

Sections du résumé

Background UNASSIGNED
Functional connectivity (FC) studies showed that pharmaco-resistant mesial temporal lobe epilepsy (MTLE) affects not only the limbic system, but also several extra-limbic regions, including areas belonging to resting state networks. Less is known about FC in subjects with benign MTLE (i.e., sensitive to antiseizure medication, bMTLE).
Aim and methods UNASSIGNED
We evaluated FC of hippocampus and amygdala in subjects with bMTLE, distinguished based on the epileptic focus lateralization. We enrolled 19 patients (10 with left and 9 with right bMTLE) and 10 age-matched healthy subjects. Connectivity was investigated at rest by using a seed-based regression analyses approach with four regions of interest (left and right hippocampus, left and right amygdala). Patients were also tested with a neuropsychological battery and their scores were correlated with fMRI data.
Results and conclusions UNASSIGNED
Our study documented an asymmetrical disruption of FC in bMTLE, in relation to the side of the focus. Right subjects only exhibited limited altered connections, while left subjects-who performed worse in verbal memory tests-showed a wide bilateral hypoconnectivity of hippocampus and amygdala with areas belonging to language and memory network. The strength of FC between left limbic areas and language and memory network correlated with better performances in verbal memory tests. Moreover, we observed an increased FC with areas of default mode network, more pronounced in left subjects, a possible attempt to compensate cognitive deficit but without effectiveness.We believe that these findings could help to better characterize bMTLE, in which a dysfunction of limbic connectivity is detectable despite well-controlled epilepsy.

Identifiants

pubmed: 36247782
doi: 10.3389/fneur.2022.943660
pmc: PMC9558280
doi:

Types de publication

Journal Article

Langues

eng

Pagination

943660

Informations de copyright

Copyright © 2022 Pizzanelli, Pesaresi, Milano, Cecchi, Fontanelli, Giannoni, Giorgi, Cosottini and Bonanni.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Seizure. 2020 Jan 21;76:32-38
pubmed: 31986443
Neurology. 1992 Oct;42(10):1911-7
pubmed: 1407572
Nat Rev Neurosci. 2003 Jan;4(1):37-48
pubmed: 12511860
Brain. 2012 Aug;135(Pt 8):2350-7
pubmed: 22669081
PLoS One. 2012;7(10):e46791
pubmed: 23071638
Brain Topogr. 2013 Apr;26(2):355-62
pubmed: 23400553
Neurosci Biobehav Rev. 2022 Feb;133:104489
pubmed: 34929226
Eur Neurol. 1996;36(6):378-84
pubmed: 8954307
J Neural Transm (Vienna). 2018 Mar;125(3):531-545
pubmed: 28766041
Hum Brain Mapp. 2016 Sep;37(9):3137-52
pubmed: 27133613
Epilepsy Behav. 2010 Mar;17(3):344-53
pubmed: 20153261
Epilepsy Behav. 2019 Jan;90:238-246
pubmed: 30538081
Neuroimage Clin. 2021;31:102702
pubmed: 34090125
Trends Neurosci. 1995 May;18(5):210-1
pubmed: 7610490
Epilepsy Curr. 2008 May-Jun;8(3):68-72
pubmed: 18488058
Ital J Neurol Sci. 1996 Aug;17(4):305-9
pubmed: 8915764
Epileptic Disord. 2002 Dec;4 Suppl 3:S61-72
pubmed: 12495876
Neuroimage. 2014 Oct 15;100:135-44
pubmed: 24814212
BMC Neurosci. 2010 Jun 02;11:66
pubmed: 20525202
Epilepsia. 2014 Aug;55(8):1197-204
pubmed: 24962348
J Clin Neurosci. 2006 Nov;13(9):885-97
pubmed: 17049865
Neuroimage. 2009 Jan 1;44(1):83-98
pubmed: 18501637
Ann Neurol. 2006 Feb;59(2):335-43
pubmed: 16404743
Epilepsy Behav. 2021 Apr;117:107834
pubmed: 33610102
J Comp Neurol. 1999 Jun 14;408(4):449-60
pubmed: 10340497
Brain Behav. 2022 Mar;12(3):e2484
pubmed: 35166072
Arch Neurol. 1997 Apr;54(4):369-76
pubmed: 9109737
Brain. 2009 Oct;132(Pt 10):2822-30
pubmed: 19635728
Epilepsia. 2012 Jun;53(6):1013-23
pubmed: 22578020
J Neurol Neurosurg Psychiatry. 1999 Jul;67(1):44-50
pubmed: 10369821
IEEE Trans Med Imaging. 2001 Jan;20(1):45-57
pubmed: 11293691
Neurology. 1992 Feb;42(2):371-7
pubmed: 1736168
Neurology. 2007 Dec 11;69(24):2256-65
pubmed: 18071146
Neurol Sci. 2002 Mar;22(6):443-7
pubmed: 11976975
Hum Brain Mapp. 2002 Nov;17(3):143-55
pubmed: 12391568
Epilepsy Behav. 2016 Nov;64(Pt B):322-328
pubmed: 27765519
Epilepsy Res Treat. 2012;2012:630853
pubmed: 22957234
Cortex. 1992 Sep;28(3):423-33
pubmed: 1382918
Neuroimage. 2001 Dec;14(6):1370-86
pubmed: 11707093
Epilepsia. 2016 Oct;57(10):1546-1557
pubmed: 27554793
Brain Res. 2010 Apr 6;1323:152-60
pubmed: 20132802
Neuroimage. 2004;23 Suppl 1:S208-19
pubmed: 15501092
Epilepsia. 1990 Mar-Apr;31(2):145-55
pubmed: 2108014
Neuroimage. 2002 Oct;17(2):825-41
pubmed: 12377157
Epilepsy Res. 2019 Jan;149:37-43
pubmed: 30472489
Epilepsia. 2014 May;55(5):674-682
pubmed: 24650167
Neuroimage. 2011 Apr 15;55(4):1423-34
pubmed: 21277375
Nat Rev Neurol. 2011 Apr;7(4):237-40
pubmed: 21263461
Nat Rev Neurol. 2011 Mar;7(3):154-64
pubmed: 21304484
Neuroimage. 2003 Oct;20(2):1052-63
pubmed: 14568475
Rev Neurol (Paris). 2001 Sep;157(8-9 Pt 1):797-806
pubmed: 11677400
Cold Spring Harb Perspect Med. 2012 Dec 01;2(12):a009621
pubmed: 23071379
Epilepsia. 2010 Jun;51(6):1069-77
pubmed: 19889013
Neuroimage Clin. 2016 Dec 18;14:28-36
pubmed: 28123951
Epilepsy Behav. 2018 Aug;85:222-226
pubmed: 30032811

Auteurs

Chiara Pizzanelli (C)

Department of Clinical and Experimental Medicine, Neurology Unit, University of Pisa, Pisa, Italy.

Ilaria Pesaresi (I)

Neuroradiology Unit, Pisa University Hospital, Pisa, Italy.

Chiara Milano (C)

Department of Clinical and Experimental Medicine, Neurology Unit, University of Pisa, Pisa, Italy.

Paolo Cecchi (P)

Department of Translational Research and New Technologies in Medicine and Surgery, Neuroradiology Unit, University of Pisa, Pisa, Italy.

Lorenzo Fontanelli (L)

Department of Clinical and Experimental Medicine, Neurology Unit, University of Pisa, Pisa, Italy.

Sara Giannoni (S)

Department of Clinical and Experimental Medicine, Neurology Unit, University of Pisa, Pisa, Italy.

Filippo Sean Giorgi (FS)

Department of Translational Research and New Technologies in Medicine and Surgery, Human Anatomy, University of Pisa, Pisa, Italy.

Mirco Cosottini (M)

Neuroradiology Unit, Pisa University Hospital, Pisa, Italy.
Department of Translational Research and New Technologies in Medicine and Surgery, Neuroradiology Unit, University of Pisa, Pisa, Italy.

Enrica Bonanni (E)

Department of Clinical and Experimental Medicine, Neurology Unit, University of Pisa, Pisa, Italy.

Classifications MeSH