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Volumetric Evaluation of Substantia Nigra in Major Depressive Disorder Using Atlas-Based Method

Year 2024, Volume: 6 Issue: 2, 190 - 195, 16.05.2024
https://doi.org/10.37990/medr.1409810

Abstract

Aim: The substantia nigra pars compacta (SNc), a vital part of the brain that produces dopamine, is being closely studied due to its potential role in the monoamine hypothesis, which aims to explain the causes of Major Depressive Disorder (MDD). Dopamine, a chemical messenger in the brain, is linked to the monoamine hypothesis, suggesting that imbalances in these chemicals may contribute to MDD. This study aimed to calculate volumetric changes in the substantia nigra (SN), using brain magnetic resonance imaging (MRI) in individuals diagnosed with MDD.
Material and Method: Sixty-six participants, comprising 33 individuals diagnosed with MDD (mean age=44.30±13.98 years) and 33 healthy individuals (mean age=46.27±14.94 years), were recruited from the university hospital psychiatry outpatient clinic. In the MDD group, there were 15 male participants (45%) and 18 female participants (55%). The healthy control group consisted of 28 males (84.8%) and 5 females (16.2%). Potential confounding factors, such as underlying chronic diseases, were ruled out by the clinician through a thorough examination of the patient's medical history, ensuring the study outcomes were not influenced. Three-dimensional brain MRI scans were conducted using a 1.5 Tesla MRI scanner. Volumes of the SN and midbrain were automatically computed using MRIStudio, an atlas-based image analysis program.
Results: Statistically significant higher volumes were observed in the right SN in the MDD group compared to controls (0.146±0.045 cm³ vs. 0.122±0.035 cm³, p=0.02, p<0.05). The ratio of SN to midbrain volume was higher in MDD patients on both sides, with a 22.4% higher value on the right side and a 12.7% higher on the left side relative to controls (p=0.002 for the right, p=0.01 for the left; p<0.05). Moreover, a negative correlation between left and right SN volumes and age was identified in the MDD group (p=0.01 for the left, p=0.05 for the right side; p<0.05).
Conclusion: Our study revealed an increase in SN volume in MDD patients. Identifying volumetric discrepancies in brain regions responsible for dopamine release could hold significant value in elucidating the underlying causes of the disease and guiding treatment strategies.

References

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  • Kessler RC, Berglund P, Demler O, et al. The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). JAMA. 2003;289:3095-105.
  • Beyer JL, Krishnan KRR. Volumetric brain imaging findings in mood disorders. Bipolar Disord. 2002;4:89-104.
  • Delgado PL. Depression: the case for a monoamine deficiency. J Clin Psychiatry. 2000;61:7-11.
  • Perez-Caballero L, Torres-Sanchez S, Romero-López-Alberca C, et al. Monoaminergic system and depression. Cell Tissue Res. 2019;377:107-13.
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  • Neuroanatomy, substantia nigra. https://www.ncbi.nlm.nih.gov/books/NBK536995 access date 16.08.2023
  • Güzelad Ö, Özkan A, Parlak H, et al. Protective mechanism of Syringic acid in an experimental model of Parkinson's disease. Metab Brain Dis. 2021;36:1003-14.
  • Dallé E, Mabandla MV. Early life stress, depression and parkinson's disease: a new approach. Mol Brain. 2018;11:1-13.
  • Chinta SJ, Andersen JK. Dopaminergic neurons. Int J Biochem Cell Biol. 2005;37:942-6.
  • Blomstedt P, Hariz MI, Lees A, et al. Acute severe depression induced by intraoperative stimulation of the substantia nigra: a case report. Parkinsonism Relat Disord. 2008;14:253-6.
  • Gao L, Xue Q, Gong S, et al. Structural and functional alterations of substantia nigra and associations with anxiety and depressive symptoms following traumatic brain injury. Front Neurol. 2022;13:719778.
  • Hwang KS, Langley J, Tripathi R, et al. In vivo detection of substantia nigra and locus coeruleus volume loss in Parkinson’s disease using neuromelanin-sensitive MRI: Replication in two cohorts. PLoS One. 2023;18:e0282684.
  • Jiang H, Van Zijl PC, Kim J, et al. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput Methods Programs Biomed. 2006;81:106-16.
  • Roberts N, Puddephat M, Mcnulty V. The benefit of stereology for quantitative radiology. Br J Radiol. 2000;73:679-97.
  • Faria AV, Hoon A, Stashinko E, et al. Quantitative analysis of brain pathology based on MRI and brain atlases—applications for cerebral palsy. Neuroimage. 2011;54:1854-61.
  • Johansen-Berg H, Gutman DA, Behrens TE, et al. Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cereb Cortex. 2008;18:1374-83.
  • Cacciola A, Milardi D, Anastasi GP, et al. A direct cortico-nigral pathway as revealed by constrained spherical deconvolution tractography in humans. Front Hum Neurosci. 2016;10:374.
  • Schmaal L, Veltman DJ, Van Erp TG, et al. Subcortical brain alterations in major depressive disorder: findings from the ENIGMA major depressive disorder working group. Mol Psychiatry. 2016;21:806-12.
  • Goldstein Ferber S, Weller A, Yadid G, Friedman A. Discovering the lost reward: critical locations for endocannabinoid modulation of the cortico–striatal loop that are implicated in major depression. Int J Mol Sci. 2021;22:1867.
  • Jiang Y, Zou M, Wang Y, Wang Y. Nucleus accumbens in the pathogenesis of major depressive disorder: a brief review. Brain Res Bull. 2023;196:68-75.
  • Rigucci S, Serafini G, Pompili M, et al. Anatomical and functional correlates in major depressive disorder: the contribution of neuroimaging studies. World J Biol Psychiatry. 2010;11:165-80.
  • Öngür D, Price JL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex. 2000;10:206-19.
  • Wise T, Radua J, Via E, et al. Common and distinct patterns of grey-matter volume alteration in major depression and bipolar disorder: evidence from voxel-based meta-analysis. Mol Psychiatry. 2017;22:1455-63.
  • Williams MR, Galvin K, O'sullivan B, et al. Neuropathological changes in the substantia nigra in schizophrenia but not depression. Eur Arch Psychiatry Clin Neurosci. 2014;264:285-96.
  • Ziegler DA, Wonderlick JS, Ashourian P, et al. Substantia nigra volume loss before basal forebrain degeneration in early Parkinson disease. JAMA Neurol. 2013;70:241-7.
  • Hoeppner J, Prudente-Morrissey L, Herpertz SC, et al. Substantia nigra hyperechogenicity in depressive subjects relates to motor asymmetry and impaired word fluency. Eur Arch Psychiatry Clin Neurosci. 2009;259:92-7.
  • Ogisu K, Kudo K, Sasaki M, et al. 3D neuromelanin-sensitive magnetic resonance imaging with semi-automated volume measurement of the substantia nigra pars compacta for diagnosis of Parkinson's disease. Neuroradiology. 2013;55:719-24.
  • Huddleston DE, Langley J, Dusek P, et al. Imaging parkinsonian pathology in substantia nigra with MRI. Curr Radiol Rep. 2018;6:15.
  • Schwarz ST, Rittman T, Gontu V, et al. T1-weighted MRI shows stage-dependent substantia nigra signal loss in Parkinson's disease. Mov Disord. 2011;26:1633-8.
  • Kempton MJ, Haldane M, Jogia J, et al. Dissociable brain structural changes associated with predisposition, resilience, and disease expression in bipolar disorder. J Neurosci. 2009;29:10863-8.
  • Li W, Yang Y, An FR, et al. Prevalence of comorbid depression in schizophrenia: a meta-analysis of observational studies. J Affect Disord. 2020;273:524-31.
  • Dubol M, Trichard C, Leroy C, et al. Lower midbrain dopamine transporter availability in depressed patients: report from high-resolution PET imaging. J Affect Disord. 2020;262:273-7.
  • Meyer JH, Krüger S, Wilson AA, et al. Lower dopamine transporter binding potential in striatum during depression. Neuroreport. 2001;12:4121-5.
  • Schulz J, Zimmermann J, Sorg C, et al. Magnetic resonance imaging of the dopamine system in schizophrenia–a scoping review. Front Psychiatry. 2022;13:925476.
  • Yüksel D, Engelen J, Schuster V, et al. Longitudinal brain volume changes in major depressive disorder. J Neural Transm (Vienna). 2018;125:1433-47.
  • Shen Z, Cheng Y, Yang S, et al. Changes of grey matter volume in first-episode drug-naive adult major depressive disorder patients with different age-onset. Neuroimage Clin. 2016;12:492-8.
  • Shen Z, Jiang H, Cheng Y, et al. Association of cortical thickness with age of onset in first-episode, drug-naïve major depression. Neuroreport. 2019;30:1074-80.
Year 2024, Volume: 6 Issue: 2, 190 - 195, 16.05.2024
https://doi.org/10.37990/medr.1409810

Abstract

References

  • Pitsillou E, Bresnehan SM, Kagarakis EA, et al. The cellular and molecular basis of major depressive disorder: towards a unified model for understanding clinical depression. Mol Biol Rep. 2020;47:753-70.
  • WHO. Depression and other common mental disorders: global health estimates. Vol. 24. Geneva: World Health Organization, 2017;8-16.
  • Gutiérrez-Rojas L, Porras-Segovia A, Dunne H, et al. Prevalence and correlates of major depressive disorder: a systematic review. Braz J Psychiatry. 2020;42:657-72.
  • Kessler RC, Berglund P, Demler O, et al. The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). JAMA. 2003;289:3095-105.
  • Beyer JL, Krishnan KRR. Volumetric brain imaging findings in mood disorders. Bipolar Disord. 2002;4:89-104.
  • Delgado PL. Depression: the case for a monoamine deficiency. J Clin Psychiatry. 2000;61:7-11.
  • Perez-Caballero L, Torres-Sanchez S, Romero-López-Alberca C, et al. Monoaminergic system and depression. Cell Tissue Res. 2019;377:107-13.
  • Stahl SM. Stahl's essential psychopharmacology: neuroscientific basis and practical applications. In: The Monoamine Hypothesis of Depression. 5nd edition.Cambridge University Press, 2021;264.
  • Neuroanatomy, substantia nigra. https://www.ncbi.nlm.nih.gov/books/NBK536995 access date 16.08.2023
  • Güzelad Ö, Özkan A, Parlak H, et al. Protective mechanism of Syringic acid in an experimental model of Parkinson's disease. Metab Brain Dis. 2021;36:1003-14.
  • Dallé E, Mabandla MV. Early life stress, depression and parkinson's disease: a new approach. Mol Brain. 2018;11:1-13.
  • Chinta SJ, Andersen JK. Dopaminergic neurons. Int J Biochem Cell Biol. 2005;37:942-6.
  • Blomstedt P, Hariz MI, Lees A, et al. Acute severe depression induced by intraoperative stimulation of the substantia nigra: a case report. Parkinsonism Relat Disord. 2008;14:253-6.
  • Gao L, Xue Q, Gong S, et al. Structural and functional alterations of substantia nigra and associations with anxiety and depressive symptoms following traumatic brain injury. Front Neurol. 2022;13:719778.
  • Hwang KS, Langley J, Tripathi R, et al. In vivo detection of substantia nigra and locus coeruleus volume loss in Parkinson’s disease using neuromelanin-sensitive MRI: Replication in two cohorts. PLoS One. 2023;18:e0282684.
  • Jiang H, Van Zijl PC, Kim J, et al. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput Methods Programs Biomed. 2006;81:106-16.
  • Roberts N, Puddephat M, Mcnulty V. The benefit of stereology for quantitative radiology. Br J Radiol. 2000;73:679-97.
  • Faria AV, Hoon A, Stashinko E, et al. Quantitative analysis of brain pathology based on MRI and brain atlases—applications for cerebral palsy. Neuroimage. 2011;54:1854-61.
  • Johansen-Berg H, Gutman DA, Behrens TE, et al. Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cereb Cortex. 2008;18:1374-83.
  • Cacciola A, Milardi D, Anastasi GP, et al. A direct cortico-nigral pathway as revealed by constrained spherical deconvolution tractography in humans. Front Hum Neurosci. 2016;10:374.
  • Schmaal L, Veltman DJ, Van Erp TG, et al. Subcortical brain alterations in major depressive disorder: findings from the ENIGMA major depressive disorder working group. Mol Psychiatry. 2016;21:806-12.
  • Goldstein Ferber S, Weller A, Yadid G, Friedman A. Discovering the lost reward: critical locations for endocannabinoid modulation of the cortico–striatal loop that are implicated in major depression. Int J Mol Sci. 2021;22:1867.
  • Jiang Y, Zou M, Wang Y, Wang Y. Nucleus accumbens in the pathogenesis of major depressive disorder: a brief review. Brain Res Bull. 2023;196:68-75.
  • Rigucci S, Serafini G, Pompili M, et al. Anatomical and functional correlates in major depressive disorder: the contribution of neuroimaging studies. World J Biol Psychiatry. 2010;11:165-80.
  • Öngür D, Price JL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex. 2000;10:206-19.
  • Wise T, Radua J, Via E, et al. Common and distinct patterns of grey-matter volume alteration in major depression and bipolar disorder: evidence from voxel-based meta-analysis. Mol Psychiatry. 2017;22:1455-63.
  • Williams MR, Galvin K, O'sullivan B, et al. Neuropathological changes in the substantia nigra in schizophrenia but not depression. Eur Arch Psychiatry Clin Neurosci. 2014;264:285-96.
  • Ziegler DA, Wonderlick JS, Ashourian P, et al. Substantia nigra volume loss before basal forebrain degeneration in early Parkinson disease. JAMA Neurol. 2013;70:241-7.
  • Hoeppner J, Prudente-Morrissey L, Herpertz SC, et al. Substantia nigra hyperechogenicity in depressive subjects relates to motor asymmetry and impaired word fluency. Eur Arch Psychiatry Clin Neurosci. 2009;259:92-7.
  • Ogisu K, Kudo K, Sasaki M, et al. 3D neuromelanin-sensitive magnetic resonance imaging with semi-automated volume measurement of the substantia nigra pars compacta for diagnosis of Parkinson's disease. Neuroradiology. 2013;55:719-24.
  • Huddleston DE, Langley J, Dusek P, et al. Imaging parkinsonian pathology in substantia nigra with MRI. Curr Radiol Rep. 2018;6:15.
  • Schwarz ST, Rittman T, Gontu V, et al. T1-weighted MRI shows stage-dependent substantia nigra signal loss in Parkinson's disease. Mov Disord. 2011;26:1633-8.
  • Kempton MJ, Haldane M, Jogia J, et al. Dissociable brain structural changes associated with predisposition, resilience, and disease expression in bipolar disorder. J Neurosci. 2009;29:10863-8.
  • Li W, Yang Y, An FR, et al. Prevalence of comorbid depression in schizophrenia: a meta-analysis of observational studies. J Affect Disord. 2020;273:524-31.
  • Dubol M, Trichard C, Leroy C, et al. Lower midbrain dopamine transporter availability in depressed patients: report from high-resolution PET imaging. J Affect Disord. 2020;262:273-7.
  • Meyer JH, Krüger S, Wilson AA, et al. Lower dopamine transporter binding potential in striatum during depression. Neuroreport. 2001;12:4121-5.
  • Schulz J, Zimmermann J, Sorg C, et al. Magnetic resonance imaging of the dopamine system in schizophrenia–a scoping review. Front Psychiatry. 2022;13:925476.
  • Yüksel D, Engelen J, Schuster V, et al. Longitudinal brain volume changes in major depressive disorder. J Neural Transm (Vienna). 2018;125:1433-47.
  • Shen Z, Cheng Y, Yang S, et al. Changes of grey matter volume in first-episode drug-naive adult major depressive disorder patients with different age-onset. Neuroimage Clin. 2016;12:492-8.
  • Shen Z, Jiang H, Cheng Y, et al. Association of cortical thickness with age of onset in first-episode, drug-naïve major depression. Neuroreport. 2019;30:1074-80.
There are 40 citations in total.

Details

Primary Language English
Subjects Psychiatry, Anatomy
Journal Section Original Articles
Authors

Ömür Karaca 0000-0002-8218-8881

Deniz Demirtaş 0009-0004-8082-5754

Emrah Özcan 0000-0002-6373-4744

Merve Şahin Can 0000-0002-4985-5689

Aybars Kökce 0000-0002-2389-468X

Publication Date May 16, 2024
Submission Date December 26, 2023
Acceptance Date February 9, 2024
Published in Issue Year 2024 Volume: 6 Issue: 2

Cite

AMA Karaca Ö, Demirtaş D, Özcan E, Şahin Can M, Kökce A. Volumetric Evaluation of Substantia Nigra in Major Depressive Disorder Using Atlas-Based Method. Med Records. May 2024;6(2):190-195. doi:10.37990/medr.1409810

17741

Chief Editors

Assoc. Prof. Zülal Öner
Address: İzmir Bakırçay University, Department of Anatomy, İzmir, Türkiye

Assoc. Prof. Deniz Şenol
Address: Düzce University, Department of Anatomy, Düzce, Türkiye

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