Dorsal bed nucleus of stria terminalis in depressed and nondepressed temporal lobe epilepsy patients.


Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
10 2022
Historique:
revised: 25 07 2022
received: 24 03 2022
accepted: 25 07 2022
pubmed: 28 7 2022
medline: 14 10 2022
entrez: 27 7 2022
Statut: ppublish

Résumé

Temporal lobe epilepsy (TLE) and depression are common comorbid disorders whose underlying shared neural network has yet to be determined. Although animal studies demonstrate a role for the dorsal bed nucleus of the stria terminalis (dBNST) in both seizures and depression, and human clinical studies demonstrate a therapeutic effect of stimulating this region on treatment-resistant depression, the role of the dBNST in depressed and nondepressed TLE patients is still unclear. Here, we tested the hypothesis that this structure is morphologically abnormal in these epilepsy patients, with an increased abnormality in TLE patients with comorbid depression. In this case-controlled study, 3-T structural magnetic resonance imaging scans were obtained from TLE patients with no depression (TLEonly), TLE patients with depression (TLEdep), and healthy control (HC) subjects. TLE subjects were recruited from the Yale University Comprehensive Epilepsy Center, diagnosed with the International League Against Epilepsy 2014 Diagnostic Guidelines, and confirmed by video-electroencephalography. Diagnosis of major depressive disorder was confirmed by a trained neuropsychologist through a Mini International Neuropsychiatric Interview based on the Diagnostic and Statistical Manual of Mental Disorders, 4th edition. The dBNST was delineated manually by reliable raters using Bioimage Suite software. The number of patients and subjects included 35 TLEonly patients, 20 TLEdep patients, and 102 HC subjects. Both TLEonly and TLEdep patients had higher dBNST volumes compared to HC subjects, unilaterally in the left hemisphere in the TLEonly patients (p = .003) and bilaterally in the TLEdep patients (p < .0001). Furthermore, the TLEdep patients had a higher dBNST volume than the TLEonly patients in the right hemisphere (p = .02). Here, we demonstrate an abnormality of the dBNST in TLE patients, both without depression (left enlargement) and with depression (bilateral enlargement). Our results demonstrate this region to underlie TLE both with and without depression, implicating it as a target in treating the comorbidity between these two disorders.

Identifiants

pubmed: 35883245
doi: 10.1111/epi.17377
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

2561-2570

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH070902
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR000142
Pays : United States

Informations de copyright

© 2022 International League Against Epilepsy.

Références

Sankar R, Mazarati A. Neurobiology of depression as a comorbidity of epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Vezzani A, Delgado-Escueta AV, editors. Jasper's basic mechanisms of the epilepsies. Bethesda, MD: National Center for Biotechnology Information (Internet); 2012.
Garcia CS. Depression in temporal lobe epilepsy: a review of prevalence, clinical features, and management considerations. Epilepsy Res Treat. 2012;2012:809843.
Valente KD, Busatto Filho G. Depression and temporal lobe epilepsy represent an epiphenomenon sharing similar neural networks: clinical and brain structural evidences. Arq Neuropsiquiatr. 2013;71:183-90.
Harris EC, Barraclough B. Suicide as an outcome for mental disorders. A meta-analysis. Br J Psychiatry. 1997;170:205-28.
Nogueira MH, Yasuda CL, Coan AC, Kanner AM, Cendes F. Concurrent mood and anxiety disorders are associated with pharmacoresistant seizures in patients with MTLE. Epilepsia. 2017;58:1268-76.
Gonçalves EB, de Oliveira Cardoso TAM, Yasuda CL, Cendes F. Depressive disorders in patients with pharmaco-resistant mesial temporal lobe epilepsy. J Int Med Res. 2018;46:752-60.
Kanner AM, Ribot R, Mazarati A. Bidirectional relations among common psychiatric and neurologic comorbidities and epilepsy: do they have an impact on the course of the seizure disorder? Epilepsia Open. 2018;3:210-9.
Bosch OJ, Nair HP, Ahern TH, Neumann ID, Young LJ. The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacology. 2009;34:1406-15.
Crestani CC, Alves FH, Correa FM, Guimarães FS, Joca SR. Acute reversible inactivation of the bed nucleus of stria terminalis induces antidepressant-like effect in the rat forced swimming test. Behav Brain Funct. 2010;6:30.
Pezuk P, Aydin E, Aksoy A, Canbeyli R. Effects of BNST lesions in female rats on forced swimming and navigational learning. Brain Res. 2008;1228:199-207.
Stout SC, Mortas P, Owens MJ, Nemeroff CB, Moreau JL. Increased corticotropin-releasing factor concentrations in the bed nucleus of the stria terminalis of anhedonic rats. Eur J Pharmacol. 2000;401:39-46.
Takahashi D, Asaoka Y, Kimura K, Hara R, Arakaki S, Sakasai K, et al. Tonic suppression of the mesolimbic dopaminergic system by enhanced corticotropin-releasing factor signaling within the bed nucleus of the stria terminalis in chronic pain model rats. J Neurosci. 2019;39:8376-85.
Hasue RH, Shammah-Lagnado SJ. Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat. J Comp Neurol. 2002;454:15-33.
Freedman LJ, Cassell MD. Distribution of dopaminergic fibers in the central division of the extended amygdala of the rat. Brain Res. 1994;633:243-52.
Pomrenze MB, Tovar-Diaz J, Blasio A, Maiya R, Giovanetti SM, Lei K, et al. A corticotropin releasing factor network in the extended amygdala for anxiety. J Neurosci. 2019;39:1030-43.
Goschke T, Bolte A. Emotional modulation of control dilemmas: the role of positive affect, reward, and dopamine in cognitive stability and flexibility. Neuropsychologia. 2014;62:403-23.
Heinrichs SC, Koob GF. Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J Pharmacol Exp Ther. 2004;311:427-40.
Carboni E, Silvagni A, Rolando MT, Di Chiara G. Stimulation of in vivo dopamine transmission in the bed nucleus of stria terminalis by reinforcing drugs. J Neurosci. 2000;20:RC102.
Park J, Bucher ES, Fontillas K, Owesson-White C, Ariansen JL, Carelli RM, et al. Opposing catecholamine changes in the bed nucleus of the stria terminalis during intracranial self-stimulation and its extinction. Biol Psychiatry. 2013;74:69-76.
Eiler WJ 2nd, Seyoum R, Foster KL, Mailey C, June HL. D1 dopamine receptor regulates alcohol-motivated behaviors in the bed nucleus of the stria terminalis in alcohol-preferring (P) rats. Synapse. 2003;48:45-56.
Epping-Jordan MP, Markou A, Koob GF. The dopamine D-1 receptor antagonist SCH 23390 injected into the dorsolateral bed nucleus of the stria terminalis decreased cocaine reinforcement in the rat. Brain Res. 1998;784:105-15.
Swerdlow NR, Geyer MA, Vale WW, Koob GF. Corticotropin-releasing factor potentiates acoustic startle in rats: blockade by chlordiazepoxide. Psychopharmacology (Berl). 1986;88:147-52.
Sahuque LL, Kullberg EF, McGeehan AJ, Kinder JR, Hicks MP, Blanton MG, et al. Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: role of CRF receptor subtypes. Psychopharmacology (Berl). 2006;186:122-32.
Foradori CD, Lund TD, Nagahara AH, Koenig JI, Handa RJ. Corticotropin-releasing hormone heterogeneous nuclear RNA (hnRNA) and immunoreactivity are induced in extrahypothalamic brain sites by kainic-acid-induced seizures and are modulated by estrogen. Brain Res. 2007;1164:44-54.
Ben-Ari Y, Tremblay E, Ottersen OP, Meldrum BS. The role of epileptic activity in hippocampal and "remote" cerebral lesions induced by kainic acid. Brain Res. 1980;191:79-97.
La Salle GL. Kindling of motor seizures from the bed nucleus of the stria terminalis. Exp Neurol. 1979;66:309-18.
Samoriski GM, Piekut DT, Applegate CD. Differential spatial patterns of Fos induction following generalized clonic and generalized tonic seizures. Exp Neurol. 1997;143:255-68.
Albright B, Dhaher R, Wang H, Harb R, Lee TSW, Zaveri H, et al. Progressive neuronal activation accompanies epileptogenesis caused by hippocampal glutamine synthetase inhibition. Exp Neurol. 2017;288:122-33.
Kato N, Ishida N, Kanai H, Watanabe Y, Kuroda Y, McEwen BS. Expression of c-fos mRNA after audiogenic seizure in adult rats with neonatal hypothyroidism. Brain Res Mol Brain Res. 1996;38:85-90.
Shehab S, Coffey P, Dean P, Redgrave P. Regional expression of fos-like immunoreactivity following seizures induced by pentylenetetrazole and maximal electroshock. Exp Neurol. 1992;118:261-74.
Lish JD, Weissman MM, Adams PB, Hoven CW, Bird H. Family psychiatric screening instruments for epidemiologic studies: pilot testing and validation. Psychiatry Res. 1995;57:169-80.
Theiss JD, Ridgewell C, McHugo M, Heckers S, Blackford JU. Manual segmentation of the human bed nucleus of the stria terminalis using 3T MRI. Neuroimage. 2017;146:288-92.
J M, Maijtanik M, Paxinos G. Atlas of the human brain. 4th ed. New York, NY: Academic Press; 2015.
Lucas-Neto L, Mourato B, Neto D, Oliveira E, Martins H, Correia F, et al. The nucleus accumbens beyond the anterior commissure: implications for psychosurgery. Stereotact Funct Neurosurg. 2014;92:291-9.
Garcia-Finana M, Denby CE, Keller SS, Wieshmann UC, Roberts N. Degree of hippocampal atrophy is related to side of seizure onset in temporal lobe epilepsy. AJNR Am J Neuroradiol. 2006;27:1046-52.
Hecimovic H, Santos J, Price JL, Sheline YI, Mintun MA, Snyder AZ, et al. Severe hippocampal atrophy is not associated with depression in temporal lobe epilepsy. Epilepsy Behav. 2014;34:9-14.
Yilmazer-Hanke D, O'Loughlin E, McDermott K. Contribution of amygdala pathology to comorbid emotional disturbances in temporal lobe epilepsy. J Neurosci Res. 2016;94:486-503.
Peedicail JS, Sandy S, Singh S, Hader W, Myles T, Scott J, et al. Long term sequelae of amygdala enlargement in temporal lobe epilepsy. Seizure. 2020;74:33-40.
Tebartz van Elst L, Woermann FG, Lemieux L, Trimble MR. Amygdala enlargement in dysthymia-a volumetric study of patients with temporal lobe epilepsy. Biol Psychiatry. 1999;46:1614-23.
Heimer L, Harlan RE, Alheid GF, Garcia MM, de Olmos J. Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders. Neuroscience. 1997;76:957-1006.
Shammah-Lagnado SJ, Beltramino CA, McDonald AJ, Miselis RR, Yang M, de Olmos J, et al. Supracapsular bed nucleus of the stria terminalis contains central and medial extended amygdala elements: evidence from anterograde and retrograde tracing experiments in the rat. J Comp Neurol. 2000;422:533-55.
Alheid GF, Beltramino CA, De Olmos JS, Forbes MS, Swanson DJ, Heimer L. The neuronal organization of the supracapsular part of the stria terminalis in the rat: the dorsal component of the extended amygdala. Neuroscience. 1998;84:967-96.
Minami N, Morino M, Uda T, Komori T, Nakata Y, Arai N, et al. Surgery for amygdala enlargement with mesial temporal lobe epilepsy: pathological findings and seizure outcome. J Neurol Neurosurg Psychiatry. 2015;86:887-94.
Blomstedt P, Naesstrom M, Bodlund O. Deep brain stimulation in the bed nucleus of the stria terminalis and medial forebrain bundle in a patient with major depressive disorder and anorexia nervosa. Clin Case Rep. 2017;5:679-84.
Luyten L, Hendrickx S, Raymaekers S, Gabriëls L, Nuttin B. Electrical stimulation in the bed nucleus of the stria terminalis alleviates severe obsessive-compulsive disorder. Mol Psychiatry. 2016;21:1272-80.
Raymaekers S, Luyten L, Bervoets C, Gabriëls L, Nuttin B. Deep brain stimulation for treatment-resistant major depressive disorder: a comparison of two targets and long-term follow-up. Transl Psychiatry. 2017;7:e1251.
Fitzgerald PB, Segrave R, Richardson KE, Knox LA, Herring S, Daskalakis ZJ, et al. A pilot study of bed nucleus of the stria terminalis deep brain stimulation in treatment-resistant depression. Brain Stimul. 2018;11:921-8.

Auteurs

Roni Dhaher (R)

Department of Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA.

Richard A Bronen (RA)

Department of Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA.
Department of Radiology and Biomedical Imaging, Yale School of Medicine, New Haven, Connecticut, USA.

Linda Spencer (L)

Department of Psychiatry, Yale School of Medicine, New Haven, Connecticut, USA.

Lejla Colic (L)

Department of Psychiatry, Yale School of Medicine, New Haven, Connecticut, USA.
Department of Psychiatry and Psychotherapy, University Hospital Jena, Jena, Germany.
Center for Intervention and Research on Adaptive and Maladaptive Brain Circuits Underlying Mental Health, Jena, Germany.
Department of Psychiatry and Psychotherapy, Jena University Hospital, Jena, Germany.

Franklin Brown (F)

Department of Neurology, Yale School of Medicine, New Haven, Connecticut, USA.

Ali Mian (A)

Department of Radiology, Washington University School of Medicine, St Louis, Missouri, USA.

Mani Sandhu (M)

Department of Laboratory Medicine, Yale School of Medicine, New Haven, Connecticut, USA.

Brian Pittman (B)

Department of Psychiatry, Yale School of Medicine, New Haven, Connecticut, USA.

Dennis Spencer (D)

Department of Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA.

Hilary P Blumberg (HP)

Department of Radiology and Biomedical Imaging, Yale School of Medicine, New Haven, Connecticut, USA.
Department of Psychiatry, Yale School of Medicine, New Haven, Connecticut, USA.
Child Study Center, Yale School of Medicine, New Haven, Connecticut, USA.

Hamada Altalib (H)

Department of Neurology, Yale School of Medicine, New Haven, Connecticut, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH