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Comparison of structural connectivity in Parkinson's disease with depressive symptoms versus non-depressed: a diffusion MRI connectometry study

Published online by Cambridge University Press:  21 March 2018

Mina Ansari ,
Sahand Adib Moradi ,
Farzaneh Ghazi Sherbaf ,
Abozar Hedayatnia  and
Mohammad Hadi Aarabi Open the ORCID record for Mohammad Hadi Aarabi [Opens in a new window]
Mina Ansari
Affiliation:
Neuroimaging Network (NIN), Universal Scientific Education and Research Network (USERN), Tehran, Iran Students’ Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran
Sahand Adib Moradi
Affiliation:
Neuroimaging Network (NIN), Universal Scientific Education and Research Network (USERN), Tehran, Iran Students’ Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran
Farzaneh Ghazi Sherbaf
Affiliation:
Neuroimaging Network (NIN), Universal Scientific Education and Research Network (USERN), Tehran, Iran Students’ Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran
Abozar Hedayatnia
Affiliation:
Neuroimaging Network (NIN), Universal Scientific Education and Research Network (USERN), Tehran, Iran
Mohammad Hadi Aarabi*
Affiliation:
Neuroimaging Network (NIN), Universal Scientific Education and Research Network (USERN), Tehran, Iran Students’ Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran
*
Correspondence should be addressed to: Mohammad Hadi Aarabi, Neuroimaging Network (NIN), Universal Scientific Education and Research Network (USERN) Office, Children's Medical Center Hospital, Dr. Qarib Street, Keshavarz Blvd, Tehran 14194, Iran. Phone: +98-21-6692-9234. Email: mohammadhadiarabi@gmail.com.
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Abstract

Objective:

Research on psychobiological markers of Parkinson's disease (PD) remains a hot topic. Non-motor symptoms such as depression and REM sleep behavior disorder (RBD) each attribute to a particular neurodegenerative cluster in PD, and might enlighten the way for early prediction/detection of PD. The neuropathology of mood disturbances remains unclear. In fact, a few studies have investigated depression using diffusion magnetic resonance imaging (diffusion MRI).

Method:

Diffusion MRI of PD patients without comorbid RBD was used to assess whether microstructural abnormalities are detectable in the brain of 40 PD patients with depression compared to 19 patients without depression. Diffusion MRI connectometry was used to carry out group analysis between age- and gender-matched PD patients with and without depressive symptoms. Diffusion MRI connectometry is based on spin distribution function, which quantifies the density of diffusing water and is a sensitive and specific analytical method to psychological differences between groups.

Results:

A significant difference (FDR = 0.016129) was observed in the left and right uncinate fasciculi, left and right inferior longitudinal fasciculi, left and right fornices, left inferior fronto-occipital fasciculus, right corticospinal tract, genu of corpus callosum, and middle cerebellar peduncle.

Conclusion:

These results suggest the prominent circuits involved in emotion recognition, particularly negative emotions, might be impaired in comorbid depressive symptoms in PD.

Keywords

Parkinson's diseasedepressiondiffusion MRIconnectometry
Type
Original Research Article
Information
International Psychogeriatrics , Volume 31 , Issue 1: Issue Theme: Parkinson's Disease , January 2019 , pp. 5 - 12
Copyright
Copyright © International Psychogeriatric Association 2018 

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Footnotes

*

Mina Ansari and Sahand Adib Moradi contributed equally to this work.

References

Ansari, M., Rahmani, F., Dolatshahi, M., Pooyan, A. and Aarabi, M. H. (2017). Brain pathway differences between Parkinson's disease patients with and without REM sleep behavior disorder. Sleep Breath, 21, 155–161.Google Scholar
Ashtari, M. (2012). Anatomy and functional role of the inferior longitudinal fasciculus: a search that has just begun. Development Medicine Child Neurology, 54, 6–7.Google Scholar
Bach, M. et al. (2014). Methodological considerations on tract-based spatial statistics (TBSS). NeuroImage, 100, 358–369.Google Scholar
Bagga, D. et al. (2014). Decreased white matter integrity in fronto-occipital fasciculus bundles: relation to visual information processing in alcohol-dependent subjects. Alcohol, 48, 43–53.Google Scholar
Balestrino, R. and Martinez-Martin, P. (2017). Neuropsychiatric symptoms, behavioural disorders, and quality of life in Parkinson's disease. Journal of the Neurological Sciences, 373, 173–178.Google Scholar
Berg, D. et al. (2015). MDS research criteria for prodromal Parkinson's disease. Movement Disorders, 30, 1600–1611.Google Scholar
Bohnen, N. I., Kaufer, D. I., Hendrickson, R., Constantine, G. M., Mathis, C. A. and Moore, R. Y. (2007). Cortical cholinergic denervation is associated with depressive symptoms in Parkinson's disease and parkinsonian dementia. Journal Neurological, Neurosurgery, and Psychiatry, 78, 641–643.Google Scholar
Buchy, L., Luck, D., Czechowska, Y., Malla, A., Joober, R. and Lepage, M. (2012). Diffusion tensor imaging tractography of the fornix and belief confidence in first-episode psychosis. Schizophrenia Research, 137, 80–84.Google Scholar
Chaudhuri, K. R., Healy, D. G. and Schapira, A. H. (2006). Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurology, 5, 235–245.Google Scholar
Chen, P.-H. and Cheng, S.-J. (2008). Depression in Parkinson disease: current understanding and treatment. International Journal of Gerontology, 2, 172–182.Google Scholar
Cole, J. et al. (2012). White matter abnormalities and illness severity in major depressive disorder. The British Journal of Psychiatry, 201, 33–39.Google Scholar
de Kwaasteniet, B. et al. (2013). Relation between structural and functional connectivity in major depressive disorder. Biological Psychiatry, 74, 40–47.Google Scholar
Delaparte, L. et al. (2017). A comparison of structural connectivity in anxious depression versus non-anxious depression. Journal of Psychiatric Research, 89, 38–47.Google Scholar
Duffy, S. L., Paradise, M., Hickie, I. B., Lewis, S. J., Naismith, S. L. and Lagopoulos, J. (2014). Cognitive impairment with and without depression history: an analysis of white matter microstructure. Journal of Psychiatry & Neuroscience, 39, 135–143.Google Scholar
Emsell, L. et al. (2013). Limbic and callosal white matter changes in euthymic bipolar I disorder: an advanced diffusion magnetic resonance imaging tractography study. Biological Psychiatry, 73, 194–201.Google Scholar
Foster, P. S. et al. (2011). Anxiety and depression severity are related to right but not left onset Parkinson's disease duration. Journal of Neurological Sciences, 305, 131–135.Google Scholar
Fujishiro, H. et al. (2017). REM sleep without atonia in middle-aged and older psychiatric patients and Lewy body disease: a case series. International Journal of Geriatric Psychiatry, 32, 397–406.Google Scholar
Gallagher, D. A. and Schrag, A. (2012). Psychosis, apathy, depression and anxiety in Parkinson's disease. Neurobiology Disease, 46, 581–589.Google Scholar
Greicius, M. D. et al. (2007). Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biological Psychiatry, 62, 429–437.Google Scholar
Hau, J. et al. (2016). Cortical terminations of the inferior Fronto-Occipital and uncinate fasciculi: anatomical stem-based virtual dissection. Frontiers in Neuroanatomy, 10, 58.Google Scholar
Hettema, J. M. et al. (2012). Pilot multimodal twin imaging study of generalized anxiety disorder. Depression and Anxiety, 29, 202–209.Google Scholar
Hollocks, M. J. et al. (2015). Differential relationships between apathy and depression with white matter microstructural changes and functional outcomes. Brain, 138, 3803–3815.Google Scholar
Hoogenboom, W. S. et al. (2014). Limbic system white matter microstructure and long-term treatment outcome in major depressive disorder: a diffusion tensor imaging study using legacy data. The World Journal of Biological Psychiatry, 15, 122–134.Google Scholar
Huang, P. et al. (2014). Disrupted white matter integrity in depressed versus non-depressed Parkinson's disease patients: a tract-based spatial statistics study. Journal of Neurological Sciences, 346, 145–148.Google Scholar
Ishihara, L. and Brayne, C. (2006). A systematic review of depression and mental illness preceding Parkinson's disease. Acta Neurologica Scandinavica, 113, 211–220.Google Scholar
Kemp, A. et al. (2013). Age of onset and corpus callosal morphology in major depression. Journal of Affective Disorder, 150, 703–706.Google Scholar
Koenigs, M. and Grafman, J. (2009). The functional neuroanatomy of depression: distinct roles for ventromedial and dorsolateral prefrontal cortex. Behavioural Brain Research, 201, 239–243.Google Scholar
Kummer, A., Cardoso, F. and Teixeira, A. L. (2009). Suicidal ideation in Parkinson's disease. CNS Spectrums, 14, 431–436.Google Scholar
Lai, C. H. and Wu, Y. T. (2014). Alterations in white matter micro-integrity of the superior longitudinal fasciculus and anterior thalamic radiation of young adult patients with depression. Psychological Medicine, 44, 2825–2832.Google Scholar
Lai, C. H. and Wu, Y. T. (2016). The white matter microintegrity alterations of neocortical and limbic association fibers in major depressive disorder and panic disorder: the comparison. Medicine (Baltimore), 95, e2982.Google Scholar
Lemke, M. (2008). Depressive symptoms in Parkinson's disease. European Journal of Neurology, 15, 21–25.Google Scholar
Li, W., Liu, J., Skidmore, F., Liu, Y., Tian, J. and Li, K. (2010). White matter microstructure changes in the thalamus in Parkinson disease with depression: a diffusion tensor MR imaging study. American Journal of Neuroradiology, 31, 1861–1866.Google Scholar
Liao, Y. et al. (2013). Is depression a disconnection syndrome? Meta-analysis of diffusion tensor imaging studies in patients with MDD. Journal of Psychiatry & Neuroscience, 38, 49–56.Google Scholar
Lou, Y. et al. (2015). Altered brain network centrality in depressed Parkinson's disease patients. Movement Disorders, 30, 1777–1784.Google Scholar
Mahajan, A. et al. (2014). REM sleep behavior and motor findings in Parkinson's disease: a cross-sectional analysis. Tremor and Other Hyperkinetic Movements (NY), 4, 245.Google Scholar
Marsh, L. (2013). Depression and Parkinson's disease: current knowledge. Current Neurology and Neuroscience Reports, 13, 409.Google Scholar
Marsh, L., McDonald, W. M., Cummings, J. and Ravina, B. (2006). Provisional diagnostic criteria for depression in Parkinson's disease: report of an NINDS/NIMH work group. Movement Disorders, 21, 148–158.Google Scholar
Matsui, H. et al. (2007). Depression in Parkinson's disease. Diffusion tensor imaging study. Journal of Neurology, 254, 1170–1173.Google Scholar
Phan, K. L. et al. (2009). Preliminary evidence of white matter abnormality in the uncinate fasciculus in generalized social anxiety disorder. Biological Psychiatry, 66, 691–694.Google Scholar
Reijnders, J. S., Ehrt, U., Weber, W. E., Aarsland, D. and Leentjens, A. F. (2008). A systematic review of prevalence studies of depression in Parkinson's disease. Movement Disorders, 23, 183–189; quiz 313.Google Scholar
Rogers, M. A. et al. (2004). Executive and prefrontal dysfunction in unipolar depression: a review of neuropsychological and imaging evidence. Neuroscience Research, 50, 1–11.Google Scholar
Scheuerecker, J. et al. (2010). Orbitofrontal volume reductions during emotion recognition in patients with major depression. Journal of Psychiatry & Neuroscience, 35, 311–320.Google Scholar
Schrag, A. (2006). Quality of life and depression in Parkinson's disease. Journal of the Neurological Sciences, 248, 151–157.Google Scholar
Schrag, A. et al. (2007). Depression rating scales in Parkinson's disease: critique and recommendations. Movement Disorders, 22, 1077–1092.Google Scholar
Sheline, Y. I. (2000). 3D MRI studies of neuroanatomic changes in unipolar major depression: the role of stress and medical comorbidity. Biological Psychiatry, 48, 791–800.Google Scholar
Shiba, M. et al. (2000). Anxiety disorders and depressive disorders preceding Parkinson's disease: a case-control study. Movement Disorders, 15, 669–677.Google Scholar
Storch, A. et al. (2008). Depression in Parkinson's disease. Part 1: epidemiology, signs and symptoms, pathophysiology and diagnosis. Fortschritte der Neurologie-Psychiatrie, 76, 715–724.Google Scholar
Sveinbjornsdottir, S. (2016). The clinical symptoms of Parkinson's disease. Journal of Neurochemistry, 139 (Suppl. 1), 318–324.Google Scholar
Tham, M. W., San Woon, P., Sum, M. Y., Lee, T.-S. and Sim, K. (2011). White matter abnormalities in major depression: evidence from post-mortem, neuroimaging and genetic studies. Journal of Affective Disorders, 132, 26–36.Google Scholar
Thobois, S., Prange, S., Sgambato-Faure, V., Tremblay, L. and Broussolle, E. (2017). Imaging the etiology of apathy, anxiety, and depression in Parkinson's disease: implication for treatment. Current Neurology Neuroscience Reports, 17, 76.Google Scholar
Torbey, E., Pachana, N. A. and Dissanayaka, N. N. (2015). Depression rating scales in Parkinson's disease: a critical review updating recent literature. Journal of Affective Disorders, 184, 216–224.Google Scholar
Tromp, D. P. et al. (2012). Reduced structural connectivity of a major frontolimbic pathway in generalized anxiety disorder. Archives of General Psychiatry, 69, 925–934.Google Scholar
van Mierlo, T. J., Chung, C., Foncke, E. M., Berendse, H. W. and van den Heuvel, O. A. (2015). Depressive symptoms in Parkinson's disease are related to decreased hippocampus and amygdala volume. Movement Disorders, 30, 245–252.Google Scholar
Weintraub, D. et al. (2005). Striatal dopamine transporter imaging correlates with anxiety and depression symptoms in Parkinson's disease. The Journal of Nuclear Medicine, 46, 227–232.Google Scholar
Wen, M. C., Chan, L. L., Tan, L. C. and Tan, E. K. (2016). Depression, anxiety, and apathy in Parkinson's disease: insights from neuroimaging studies. European Journal of Neurology, 23, 1001–1019.Google Scholar
Williams, M. R., Sharma, P., Fung, K. L., Pearce, R. K., Hirsch, S. R. and Maier, M. (2015). Axonal myelin increase in the callosal genu in depression but not schizophrenia. Psychological Medicine, 45, 2145–2155.Google Scholar
Yamada, S. et al. (2015). Microstructural abnormalities in anterior callosal fibers and their relationship with cognitive function in major depressive disorder and bipolar disorder: a tract-specific analysis study. Journal of Affective Disorders, 174, 542–548.Google Scholar
Yeh, F. C., Badre, D. and Verstynen, T. (2016). Connectometry: a statistical approach harnessing the analytical potential of the local connectome. NeuroImage, 125, 162–171.Google Scholar
Yesavage, J. A. et al. (1983). Development and validation of a geriatric depression screening scale: a preliminary report. Journal of Psychiatric Research, 17, 37–49.Google Scholar
Zhang, Y. and Schuff, N. (2014). Differential patterns of white matter degradation in relation to cognitive and motor deficits in Parkinson's disease (P2.004). Neurology, 82, P2.004.Google Scholar