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Volume of hippocampus-amygdala transition area predicts outcomes of electroconvulsive therapy in major depressive disorder: high accuracy validated in two independent cohorts

Published online by Cambridge University Press:  23 May 2022

Jinping Xu ,
Wenfei Li ,
Tongjian Bai ,
Jiaying Li ,
Jinhuan Zhang ,
Qingmao Hu ,
Jiaojian Wang ,
Yanghua Tian  and
Kai Wang
Jinping Xu
Affiliation:
Institute of Biomedical and Health Engineering, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
Wenfei Li
Affiliation:
Affiliated Psychological Hospital of Anhui Medical University, Hefei 230022 China
Tongjian Bai
Affiliation:
Department of Neurology, The First Hospital of Anhui Medical University, Hefei, 230022, China
Jiaying Li
Affiliation:
Institute of Biomedical and Health Engineering, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
Jinhuan Zhang
Affiliation:
Institute of Biomedical and Health Engineering, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
Qingmao Hu
Affiliation:
Institute of Biomedical and Health Engineering, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China CAS Key Laboratory of Human-Machine Intelligence-Synergy Systems, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
Jiaojian Wang
Affiliation:
Key Laboratory of Biological Science and Technology, Ministry of Education, College of Bioengineering, Chongqing University, Chongqing 400030, China
Yanghua Tian*
Affiliation:
Department of Neurology, The First Hospital of Anhui Medical University, Hefei, 230022, China Department of Neurology, the Second Hospital of Anhui Medical University, Hefei 230022, China Institute of Artificial Intelligence, Hefei Comprehensive National Science Center, Hefei, 230022, China Anhui Province Key Laboratory of Cognition and Neuropsychiatric Disorders, Hefei 230022, China Anhui Medical University, School of Mental Health and Psychological Sciences, Hefei 230022, China
Kai Wang
Affiliation:
Department of Neurology, The First Hospital of Anhui Medical University, Hefei, 230022, China Institute of Artificial Intelligence, Hefei Comprehensive National Science Center, Hefei, 230022, China Anhui Province Key Laboratory of Cognition and Neuropsychiatric Disorders, Hefei 230022, China Anhui Medical University, School of Mental Health and Psychological Sciences, Hefei 230022, China Collaborative Innovation Center of Neuropsychiatric Disorders and Mental Health, Hefei 230022, China Anhui Province clinical research center for neurological disease, Hefei 230022, China
*
Authors for correspondence: Yanghua Tian, E-mail: ayfytyh@126.com; Jiaojian Wang, E-mail: jiaojianwang@uestc.edu.cn
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Abstract

Background

Although many previous studies reported structural plasticity of the hippocampus and amygdala induced by electroconvulsive therapy (ECT) in major depressive disorder (MDD), yet the exact roles of both areas for antidepressant effects are still controversial.

Methods

In the current study, segmentation of amygdala and hippocampal sub-regions was used to investigate the longitudinal changes of volume, the relationship between volume and antidepressant effects, and prediction performances for ECT in MDD patients before and after ECT using two independent datasets.

Results

As a result, MDD patients showed selectively and consistently increased volume in the left lateral nucleus, right accessory basal nucleus, bilateral basal nucleus, bilateral corticoamygdaloid transition (CAT), bilateral paralaminar nucleus of the amygdala, and bilateral hippocampus-amygdala transition area (HATA) after ECT in both datasets, whereas marginally significant increase of volume in bilateral granule cell molecular layer of the head of dentate gyrus, the bilateral head of cornu ammonis (CA) 4, and left head of CA 3. Correlation analyses revealed that increased volume of left HATA was significantly associated with antidepressant effects after ECT. Moreover, volumes of HATA in the MDD patients before ECT could be served as potential biomarkers to predict ECT remission with the highest accuracy of 86.95% and 82.92% in two datasets (The predictive models were trained on Dataset 2 and the sensitivity, specificity and accuracy of Dataset 2 were obtained from leave-one-out-cross-validation. Thus, they were not independent and very likely to be inflated).

Conclusions

These results not only suggested that ECT could selectively induce structural plasticity of the amygdala and hippocampal sub-regions associated with antidepressant effects of ECT in MDD patients, but also provided potential biomarkers (especially HATA) for effectively and timely interventions for ECT in clinical applications.

Keywords

Amygdalaelectroconvulsive therapyhippocampusmajor depressive disorderstructure MRIsupport vector machine

Information

Type
Original Article
Information
Psychological Medicine , Volume 53 , Issue 10 , July 2023 , pp. 4464 - 4473
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally in the current study.

References

Aghamohammadi-Sereshki, A., Hrybouski, S., Travis, S., Huang, Y., Olsen, F., Carter, R., … Malykhin, N. V. (2019). Amygdala subnuclei and healthy cognitive aging. Human Brain Mapping, 40(1), 34–52. doi: 10.1002/hbm.24353.CrossRefGoogle ScholarPubMed
American Psychiatric Press. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC, USA: American Psychiatric Press.Google Scholar
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., … Zilles, K. (2005). Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps. Anatomy and Embryology (Berl), 210(5–6), 343–352. doi: 10.1007/s00429-005-0025-5.CrossRefGoogle ScholarPubMed
Bai, T., Wei, Q., Xie, W., Wang, A., Wang, J., Ji, G. J., … Tian, Y. (2019). Hippocampal-subregion functional alterations associated with antidepressant effects and cognitive impairments of electroconvulsive therapy. Psychological Medicine, 49(8), 1357–1364. doi: 10.1017/S0033291718002684.CrossRefGoogle ScholarPubMed
Bouckaert, F., De Winter, F. L., Emsell, L., Dols, A., Rhebergen, D., Wampers, M., … Vandenbulcke, M. (2016). Grey matter volume increase following electroconvulsive therapy in patients with late life depression: A longitudinal MRI study. Journal of Psychiatry & Neuroscience, 41(2), 105–114. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/26395813.CrossRefGoogle ScholarPubMed
Brown, S. S. G., Rutland, J. W., Verma, G., Feldman, R. E., Alper, J., Schneider, M., … Balchandani, P. (2019). Structural MRI at 7T reveals amygdala nuclei and hippocampal subfield volumetric association with major depressive disorder symptom severity. Scientific Reports, 9(1), 10166. doi: 10.1038/s41598-019-46687-7.CrossRefGoogle ScholarPubMed
Cao, B., Luo, Q., Fu, Y., Du, L., Qiu, T., Yang, X., … Qiu, H. (2018). Predicting individual responses to the electroconvulsive therapy with hippocampal subfield volumes in major depression disorder. Scientific Reports, 8(1), 5434. doi: 10.1038/s41598-018-23685-9.CrossRefGoogle Scholar
Cao, B., Luo, Q., Fu, Y., Du, L., Qiu, T., Yang, X., … Qiu, H. (2020). Predicting individual responses to the electroconvulsive therapy with hippocampal subfield volumes in major depression disorder. Scientific Reports, 10(1), 17386. doi: 10.1038/s41598-020-73418-0.CrossRefGoogle Scholar
Christidi, F., Karavasilis, E., Rentzos, M., Velonakis, G., Zouvelou, V., Xirou, S., … Bede, P. (2019). Hippocampal pathology in amyotrophic lateral sclerosis: Selective vulnerability of subfields and their associated projections. Neurobiology of Aging, 84, 178–188. doi: 10.1016/j.neurobiolaging.2019.07.019.CrossRefGoogle ScholarPubMed
Dukart, J., Regen, F., Kherif, F., Colla, M., Bajbouj, M., Heuser, I., … Draganski, B. (2014). Electroconvulsive therapy-induced brain plasticity determines therapeutic outcome in mood disorders. Proceedings of the National Academy of Sciences, 111(3), 1156–1161. doi: 10.1073/pnas.1321399111.CrossRefGoogle ScholarPubMed
Enneking, V., Leehr, E. J., Dannlowski, U., & Redlich, R. (2020). Brain structural effects of treatments for depression and biomarkers of response: A systematic review of neuroimaging studies. Psychological Medicine, 50(2), 187–209. doi: 10.1017/S0033291719003660.CrossRefGoogle ScholarPubMed
Fudge, J. L., deCampo, D. M., & Becoats, K. T. (2012). Revisiting the hippocampal-amygdala pathway in primates: Association with immature-appearing neurons. Neuroscience, 212, 104–119. doi: 10.1016/j.neuroscience.2012.03.040.CrossRefGoogle ScholarPubMed
Fujita, A., Nakaaki, S., Segawa, K., Azuma, H., Sato, K., Arahata, K., … Furukawa, T. A. (2006). Memory, attention, and executive functions before and after sine and pulse wave electroconvulsive therapies for treatment-resistant major depression. Journal of ECT, 22(2), 107–112. doi: 10.1097/00124509-200606000-00006.CrossRefGoogle ScholarPubMed
Gabrieli, J. D. E., Ghosh, S. S., & Whitfield-Gabrieli, S. (2015). Prediction as a humanitarian and pragmatic contribution from human cognitive neuroscience. Neuron, 85(1), 11–26. doi: 10.1016/j.neuron.2014.10.047.CrossRefGoogle ScholarPubMed
Gbyl, K., Rostrup, E., Raghava, J. M., Andersen, C., Rosenberg, R., Larsson, H. B. W., & Videbech, P. (2021). Volume of hippocampal subregions and clinical improvement following electroconvulsive therapy in patients with depression. Progress in Neuro-psychopharmacology & Biological Psychiatry, 104, 110048. doi: 10.1016/j.pnpbp.2020.110048.CrossRefGoogle ScholarPubMed
Gbyl, K., & Videbech, P. (2018). Electroconvulsive therapy increases brain volume in major depression: A systematic review and meta-analysis. Acta Psychiatrica Scandinavica, 138(3), 180–195. doi: 10.1111/acps.12884.CrossRefGoogle ScholarPubMed
Group, U. E. R. (2003). Efficacy and safety of electroconvulsive therapy in depressive disorders: A systematic review and meta-analysis. Lancet (London, England), 361(9360), 799–808. doi: 10.1016/S0140-6736(03)12705-5.Google Scholar
Gryglewski, G., Baldinger-Melich, P., Seiger, R., Godbersen, G. M., Michenthaler, P., Klobl, M., … Lanzenberger, R. (2019). Structural changes in amygdala nuclei, hippocampal subfields and cortical thickness following electroconvulsive therapy in treatment-resistant depression: Longitudinal analysis. British Journal of Psychiatry, 214(3), 159–167. doi: 10.1192/bjp.2018.224.CrossRefGoogle ScholarPubMed
Hamidi, M., Drevets, W. C., & Price, J. L. (2004). Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biological Psychiatry, 55(6), 563–569. doi: 10.1016/j.biopsych.2003.11.006.CrossRefGoogle ScholarPubMed
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology Neurosurgery and Psychiatry, 23(1), 56–62. doi: 10.1136/Jnnp.23.1.56.CrossRefGoogle ScholarPubMed
Iglesias, J. E., Augustinack, J. C., Nguyen, K., Player, C. M., Player, A., Wright, M, & … Alzheimer's Disease Neuroimaging, I. (2015). A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI. Neuroimage, 115, 117–137. doi: 10.1016/j.neuroimage.2015.04.042.CrossRefGoogle ScholarPubMed
Iglesias, J. E., Van Leemput, K., Augustinack, J., Insausti, R., Fischl, B., Reuter, M., & Alzheimer's Disease Neuroimaging, I. (2016). Bayesian Longitudinal segmentation of hippocampal substructures in brain MRI using subject-specific atlases. Neuroimage, 141, 542–555. doi: 10.1016/j.neuroimage.2016.07.020.CrossRefGoogle ScholarPubMed
Jiang, R., Abbott, C. C., Jiang, T., Du, Y., Espinoza, R., Narr, K. L., … Calhoun, V. D. (2018). SMRI Biomarkers predict electroconvulsive treatment outcomes: Accuracy with independent data sets. Neuropsychopharmacology, 43(5), 1078–1087. doi: 10.1038/npp.2017.165.CrossRefGoogle ScholarPubMed
Jorgensen, A., Magnusson, P., Hanson, L. G., Kirkegaard, T., Benveniste, H., Lee, H., … Jorgensen, M. B. (2016). Regional brain volumes, diffusivity, and metabolite changes after electroconvulsive therapy for severe depression. Acta Psychiatrica Scandinavica, 133(2), 154–164. doi: 10.1111/acps.12462.CrossRefGoogle ScholarPubMed
Joshi, S. H., Espinoza, R. T., Pirnia, T., Shi, J., Wang, Y., Ayers, B., … Narr, K. L. (2016). Structural plasticity of the hippocampus and amygdala induced by electroconvulsive therapy in major depression. Biological Psychiatry, 79(4), 282–292. doi: 10.1016/j.biopsych.2015.02.029.CrossRefGoogle ScholarPubMed
Kedo, O., Zilles, K., Palomero-Gallagher, N., Schleicher, A., Mohlberg, H., Bludau, S., & Amunts, K. (2018). Receptor-driven, multimodal mapping of the human amygdala. Brain Structure and Function, 223(4), 1637–1666. doi: 10.1007/s00429-017-1577-x.Google ScholarPubMed
Khaleel, N., Roopa, R., Smitha, J. S., & Andrade, C. (2013). Electroconvulsive therapy attenuates dendritic arborization in the basolateral amygdala. Journal of ECT, 29(3), 156–157. doi: 10.1097/YCT.0b013e318282a6b1.CrossRefGoogle ScholarPubMed
Laroy, M., Emsell, L., Germann, J., Dols, A., Stek, M., Chakravarty, M. M., … Bouckaert, F. (2019). Hippocampal subfield volumetric changes following electroconvulsive therapy in patients with late-life depression. European Neuropsychopharmacology, 29, S214–S215. doi: 10.1016/j.euroneuro.2019.09.321.CrossRefGoogle Scholar
Leaver, A. M., Vasavada, M., Kubicki, A., Wade, B., Loureiro, J., Hellemann, G., … Narr, K. L. (2020). Hippocampal subregions and networks linked with antidepressant response to electroconvulsive therapy. Molological Psychiatry, 26(8), 4288–4299. doi: 10.1038/s41380-020-0666-z.Google ScholarPubMed
Maigaard, K., Hageman, I., Jorgensen, A., Jorgensen, M. B., & Wortwein, G. (2012). Electroconvulsive stimulations prevent chronic stress-induced increases in L-type calcium channel mRNAs in the hippocampus and basolateral amygdala. Neuroscience Letters, 516(1), 24–28. doi: 10.1016/j.neulet.2012.03.043.CrossRefGoogle ScholarPubMed
Mikolas, P., Tozzi, L., Doolin, K., Farrell, C., O'Keane, V., & Frodl, T. (2019). Effects of early life adversity and FKBP5 genotype on hippocampal subfields volume in major depression. Journal of Affective Disorders, 252, 152–159. doi: 10.1016/j.jad.2019.04.054.CrossRefGoogle ScholarPubMed
Morey, R. A., Clarke, E. K., Haswell, C. C., Phillips, R. D., Clausen, A. N., Mufford, M. S., … LaBar, K. S. (2020). Amygdala nuclei volume and shape in military veterans with posttraumatic stress disorder. Biological Psychiatry-Cognitive Neuroscience and Neuroimaging, 5(3), 281–290. doi: 10.1016/j.bpsc.2019.11.016.CrossRefGoogle ScholarPubMed
Myrvang, A. D., Vangberg, T. R., Stedal, K., Ro, O., Endestad, T., Rosenvinge, J. H., & Aslaksen, P. M. (2018). Hippocampal subfields in adolescent anorexia nervosa. Psychiatry Research- Neuroimaging, 282, 24–30. doi: 10.1016/j.pscychresns.2018.10.007.CrossRefGoogle ScholarPubMed
Oltedal, L., Narr, K. L., Abbott, C., Anand, A., Argyelan, M., Bartsch, H., … Dale, A. M. (2018). Volume of the human hippocampus and clinical response following electroconvulsive therapy. Biological Psychiatry, 84(8), 574–581. doi: 10.1016/j.biopsych.2018.05.017.CrossRefGoogle ScholarPubMed
Ota, M., Noda, T., Sato, N., Okazaki, M., Ishikawa, M., Hattori, K., … Kunugi, H. (2015). Effect of electroconvulsive therapy on gray matter volume in major depressive disorder. Journal of Affective Disorders, 186, 186–191. doi: 10.1016/j.jad.2015.06.051.CrossRefGoogle ScholarPubMed
Palomero-Gallagher, N., Kedo, O., Mohlberg, H., Zilles, K., & Amunts, K. (2020). Multimodal mapping and analysis of the cyto- and receptorarchitecture of the human hippocampus. Brain Structure and Function, 225(3), 881–907. doi: 10.1007/s00429-019-02022-4.CrossRefGoogle ScholarPubMed
Phillips, R. D., De Bellis, M. D., Brumback, T., Clausen, A. N., Clarke-Rubright, E. K., Haswell, C. C., & Morey, R. A. (2021). Volumetric trajectories of hippocampal subfields and amygdala nuclei influenced by adolescent alcohol use and lifetime trauma. Translational Psychiatry, 11(1), 154. doi: 10.1038/s41398-021-01275-0.CrossRefGoogle ScholarPubMed
Postel, C., Viard, A., Andre, C., Guenole, F., de Flores, R., Baleyte, J. M., … Guillery-Girard, B. (2019). Hippocampal subfields alterations in adolescents with post-traumatic stress disorder. Human Brain Mapping, 40(4), 1244–1252. doi: 10.1002/hbm.24443.CrossRefGoogle ScholarPubMed
Prasad, S., Shah, A., Bhalsing, K. S., Kumar, K. J., Saini, J., Ingalhalikar, M., & Pal, P. K. (2019). Abnormal hippocampal subfields are associated with cognitive impairment in essential tremor. Journal of Neural Transmission (Vienna), 126(5), 597–606. doi: 10.1007/s00702-019-01992-3.CrossRefGoogle ScholarPubMed
Qi, S., Abbott, C. C., Narr, K. L., Jiang, R., Upston, J., McClintock, S. M., … Calhoun, V. D. (2020). Electroconvulsive therapy treatment responsive multimodal brain networks. Human Brain Mapping, 41(7), 1775–1785. doi: 10.1002/hbm.24910.CrossRefGoogle ScholarPubMed
Redlich, R., Opel, N., Grotegerd, D., Dohm, K., Zaremba, D., Burger, C., … Dannlowski, U. (2016). Prediction of individual response to electroconvulsive therapy via machine learning on structural magnetic resonance imaging data. JAMA Psychiatry, 73(6), 557–564. doi: 10.1001/jamapsychiatry.2016.0316.CrossRefGoogle ScholarPubMed
Reuter, M., Rosas, H. D., & Fischl, B. (2010). Highly accurate inverse consistent registration: A robust approach. Neuroimage, 53(4), 1181–1196. doi: 10.1016/j.neuroimage.2010.07.020.CrossRefGoogle ScholarPubMed
Robinson, J. L., Barron, D. S., Kirby, L. A., Bottenhorn, K. L., Hill, A. C., Murphy, J. E., … Fox, P. T. (2015). Neurofunctional topography of the human hippocampus. Human Brain Mapping, 36(12), 5018–5037. doi: 10.1002/hbm.22987.CrossRefGoogle ScholarPubMed
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009). Stress, memory and the amygdala. Nature Reviews Neuroscience, 10(6), 423–433. doi: 10.1038/nrn2651.CrossRefGoogle ScholarPubMed
Rubinow, M. J., Mahajan, G., May, W., Overholser, J. C., Jurjus, G. J., Dieter, L., … Stockmeier, C. A. (2016). Basolateral amygdala volume and cell numbers in major depressive disorder: A postmortem stereological study. Brain Structure and Function, 221(1), 171–184. doi: 10.1007/s00429-014-0900-z.CrossRefGoogle ScholarPubMed
Sackeim, H. A., Prudic, J., Fuller, R., Keilp, J., Lavori, P. W., & Olfson, M. (2007). The cognitive effects of electroconvulsive therapy in community settings. Neuropsychopharmacology, 32(1), 244–254. doi: 10.1038/sj.npp.1301180.CrossRefGoogle ScholarPubMed
Sartorius, A., Demirakca, T., Bohringer, A., Clemm von Hohenberg, C., Aksay, S. S., Bumb, J. M., … Ende, G. (2016). Electroconvulsive therapy increases temporal gray matter volume and cortical thickness. European Neuropsychopharmacology, 26(3), 506–517. doi: 10.1016/j.euroneuro.2015.12.036.CrossRefGoogle ScholarPubMed
Sartorius, A., Demirakca, T., Bohringer, A., Clemm von Hohenberg, C., Aksay, S. S., Bumb, J. M., … Ende, G. (2019). Electroconvulsive therapy induced gray matter increase is not necessarily correlated with clinical data in depressed patients. Brain Stimulation, 12(2), 335–343. doi: 10.1016/j.brs.2018.11.017.CrossRefGoogle Scholar
Saygin, Z. M., Kliemann, D., Iglesias, J. E., van der Kouwe, A. J. W., Boyd, E., Reuter, M, & … Alzheimer's Disease Neuroimaging, I. (2017). High-resolution magnetic resonance imaging reveals nuclei of the human amygdala: Manual segmentation to automatic atlas. Neuroimage, 155, 370–382. doi: 10.1016/j.neuroimage.2017.04.046.CrossRefGoogle ScholarPubMed
Schmaal, L., Veltman, D. J., van Erp, T. G., Samann, P. G., Frodl, T., Jahanshad, N., … Hibar, D. P. (2016). Subcortical brain alterations in major depressive disorder: Findings from the ENIGMA major depressive disorder working group. Mological Psychiatry, 21(6), 806–812. doi: 10.1038/mp.2015.69.Google ScholarPubMed
Semkovska, M., & McLoughlin, D. M. (2010). Objective cognitive performance associated with electroconvulsive therapy for depression: A systematic review and meta-analysis. Biological Psychiatry, 68(6), 568–577. doi: 10.1016/j.biopsych.2010.06.009.CrossRefGoogle ScholarPubMed
Spaans, H. P., Sienaert, P., Bouckaert, F., van den Berg, J. F., Verwijk, E., Kho, K. H., … Kok, R. M. (2015). Speed of remission in elderly patients with depression: Electroconvulsive therapy v. medication. British Journal of Psychiatry, 206(1), 67–71. doi: 10.1192/bjp.bp.114.148213.CrossRefGoogle ScholarPubMed
Takamiya, A., Chung, J. K., Liang, K. C., Graff-Guerrero, A., Mimura, M., & Kishimoto, T. (2018). Effect of electroconvulsive therapy on hippocampal and amygdala volumes: Systematic review and meta-analysis. British Journal of Psychiatry, 212(1), 19–26. doi: 10.1192/bjp.2017.11.CrossRefGoogle ScholarPubMed
Ten Doesschate, F., van Eijndhoven, P., Tendolkar, I., van Wingen, G. A., & van Waarde, J. A. (2014). Pre-treatment amygdala volume predicts electroconvulsive therapy response. Frontiers in Psychiatry, 5, 169. doi: 10.3389/fpsyt.2014.00169.CrossRefGoogle ScholarPubMed
Tendolkar, I., van Beek, M., van Oostrom, I., Mulder, M., Janzing, J., Voshaar, R. O., & van Eijndhoven, P. (2013). Electroconvulsive therapy increases hippocampal and amygdala volume in therapy refractory depression: A longitudinal pilot study. Psychiatry Research, 214(3), 197–203. doi: 10.1016/j.pscychresns.2013.09.004.CrossRefGoogle ScholarPubMed
Tesli, N., van der Meer, D., Rokicki, J., Storvestre, G., Rosaeg, C., Jensen, A., … Haukvik, U. K. (2020). Hippocampal subfield and amygdala nuclei volumes in schizophrenia patients with a history of violence. European Archives of Psychiatry and Clinical Neuroscience, 270(6), 771–782. doi: 10.1007/s00406-020-01098-y.CrossRefGoogle ScholarPubMed
Vaculik, M. F., Noorani, A., Hung, P. S., & Hodaie, M. (2019). Selective hippocampal subfield volume reductions in classic trigeminal neuralgia. Neuroimage Clinical, 23, 101911. doi: 10.1016/j.nicl.2019.101911.CrossRefGoogle ScholarPubMed
Vasavada, M. M., Leaver, A. M., Njau, S., Joshi, S. H., Ercoli, L., Hellemann, G., … Espinoza, R. (2017). Short- and long-term cognitive outcomes in patients with major depression treated with electroconvulsive therapy. Journal of ECT, 33(4), 278–285. doi: 10.1097/YCT.0000000000000426.CrossRefGoogle Scholar
Wang, J., Wei, Q., Bai, T., Zhou, X., Sun, H., Becker, B., … Kendrick, K. (2017). Electroconvulsive therapy selectively enhanced feedforward connectivity from fusiform face area to amygdala in major depressive disorder. Social Cognitive and Affective Neuroscience, 12(12), 1983–1992. doi: 10.1093/scan/nsx100.CrossRefGoogle ScholarPubMed
Wang, N., Zhang, L., Yang, H., Luo, X., & Fan, G. (2019). Do multiple system atrophy and Parkinson's disease show distinct patterns of volumetric alterations across hippocampal subfields? An exploratory study. European Journal of Radiology, 29(9), 4948–4956. doi: 10.1007/s00330-019-06043-9.CrossRefGoogle ScholarPubMed
Wannan, C. M. J., Cropley, V. L., Chakravarty, M. M., Van Rheenen, T. E., Mancuso, S., Bousman, C., … Bartholomeusz, C. F. (2019). Hippocampal subfields and visuospatial associative memory across stages of schizophrenia-spectrum disorder. Psychological Medicine, 49(14), 2452–2462. doi: 10.1017/S0033291718003458.CrossRefGoogle ScholarPubMed
Wildburger, N. C., Lin-Ye, A., Baird, M. A., Lei, D., & Bao, J. (2009). Neuroprotective effects of blockers for T-type calcium channels. Molecular Neurodegeneration, 4, 44. doi: 10.1186/1750-1326-4-44.CrossRefGoogle ScholarPubMed
Xu, R., Hu, X., Jiang, X., Zhang, Y., Wang, J., & Zeng, X. (2020). Longitudinal volume changes of hippocampal subfields and cognitive decline in Parkinson's disease. Quantitative Imaging in Medicine and Surgery, 10(1), 220–232. doi: 10.21037/qims.2019.10.17.CrossRefGoogle ScholarPubMed
Yang, J., Yin, Y., Svob, C., Long, J., He, X., Zhang, Y., … Yuan, Y. (2017). Amygdala atrophy and its functional disconnection with the cortico-striatal-pallidal-thalamic circuit in major depressive disorder in females. PLoS One, 12(1), e0168239. doi: 10.1371/journal.pone.0168239.CrossRefGoogle ScholarPubMed
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