Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T17:18:14.781Z Has data issue: false hasContentIssue false

Motor abnormalities and basal ganglia in first-episode psychosis (FEP)

Published online by Cambridge University Press:  02 March 2020

Manuel J. Cuesta*
Affiliation:
Department of Psychiatry, Complejo Hospitalario de Navarra, Pamplona, Spain IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
Pablo Lecumberri
Affiliation:
IdiSNA, Navarra Institute for Health Research, Pamplona, Spain Movalsys S. L., NavarraBiomed, Pamplona, Spain
Lucia Moreno-Izco
Affiliation:
Department of Psychiatry, Complejo Hospitalario de Navarra, Pamplona, Spain IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
Jose M. López-Ilundain
Affiliation:
Department of Psychiatry, Complejo Hospitalario de Navarra, Pamplona, Spain IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
María Ribeiro
Affiliation:
Department of Psychiatry, Complejo Hospitalario de Navarra, Pamplona, Spain IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
Teresa Cabada
Affiliation:
IdiSNA, Navarra Institute for Health Research, Pamplona, Spain Department of Neuroradiology, Complejo Hospitalario de Navarra, Pamplona, Spain
Ruth Lorente-Omeñaca
Affiliation:
Department of Psychiatry, Complejo Hospitalario de Navarra, Pamplona, Spain IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
Gabriel de Erausquin
Affiliation:
Zachry Foundation, The Glenn Biggs Institute of Alzheimer's & Neurodegenerative Disorders, UT Heath San Antonio, Texas, USA
Gracian García-Martí
Affiliation:
Radiology Department, CIBERSAM, Valencia, España, Quirón Salud Hospital, Valencia, España
Julio Sanjuan
Affiliation:
Research Institute of Clinic University Hospital of Valencia (INCLIVA), Valencia, Spain CIBERSAM, Biomedical Research Network on Mental Health Area, Madrid, Spain Department of Psychiatric, University of Valencia School of Medicine, Valencia, Spain
Ana M. Sánchez-Torres
Affiliation:
Department of Psychiatry, Complejo Hospitalario de Navarra, Pamplona, Spain IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
Marisol Gómez
Affiliation:
IdiSNA, Navarra Institute for Health Research, Pamplona, Spain Movalsys S. L., NavarraBiomed, Pamplona, Spain Department of Statistics, Computer Science and Mathematics, Universidad Pública de Navarra (UPNA), Pamplona, Spain
Victor Peralta
Affiliation:
IdiSNA, Navarra Institute for Health Research, Pamplona, Spain Mental Health Department, Servicio Navarro de Salud, Pamplona, Spain
*
Author for correspondence: Manuel J. Cuesta, E-mail: [email protected]

Abstract

Background

Motor abnormalities (MAs) are the primary manifestations of schizophrenia. However, the extent to which MAs are related to alterations of subcortical structures remains understudied.

Methods

We aimed to investigate the associations of MAs and basal ganglia abnormalities in first-episode psychosis (FEP) and healthy controls. Magnetic resonance imaging was performed on 48 right-handed FEP and 23 age-, gender-, handedness-, and educational attainment-matched controls, to obtain basal ganglia shape analysis, diffusion tensor imaging techniques (fractional anisotropy and mean diffusivity), and relaxometry (R2*) to estimate iron load. A comprehensive motor battery was applied including the assessment of parkinsonism, catatonic signs, and neurological soft signs (NSS). A fully automated model-based segmentation algorithm on 1.5T MRI anatomical images and accurate corregistration of diffusion and T2* volumes and R2* was used.

Results

FEP patients showed significant local atrophic changes in left globus pallidus nucleus regarding controls. Hypertrophic changes in left-side caudate were associated with higher scores in sensory integration, and in right accumbens with tremor subscale. FEP patients showed lower fractional anisotropy measures than controls but no significant differences regarding mean diffusivity and iron load of basal ganglia. However, iron load in left basal ganglia and right accumbens correlated significantly with higher extrapyramidal and motor coordination signs in FEP patients.

Conclusions

Taken together, iron load in left basal ganglia may have a role in the emergence of extrapyramidal signs and NSS of FEP patients and in consequence in the pathophysiology of psychosis.

Type
Original Article
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andreasen, N. C., Flaum, M., & Arndt, S. (1992). The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. Archives of General Psychiatry, 49(8), 615623.CrossRefGoogle ScholarPubMed
Baumann, C. R., Held, U., Valko, P. O., Wienecke, M., & Waldvogel, D. (2014). Body side and predominant motor features at the onset of Parkinson's disease are linked to motor and nonmotor progression. Movement Disorders, 29(2), 207213. doi: 10.1002/mds.25650CrossRefGoogle Scholar
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289300.CrossRefGoogle Scholar
Bora, E., Fornito, A., Radua, J., Walterfang, M., Seal, M., Wood, S. J., … Pantelis, C. (2011). Neuroanatomical abnormalities in schizophrenia: A multimodal voxelwise meta-analysis and meta-regression analysis. Schizophrenia Research, 127(1–3), 4657. doi: 10.1016/j.schres.2010.12.020CrossRefGoogle ScholarPubMed
Brugger, S. P., Angelescu, I., Abi-Dargham, A., Mizrahi, R., Shahrezaei, V., & Howes, O. D. (2020). Heterogeneity of striatal dopamine function in schizophrenia: Meta-analysis of variance. Biological Psychiatry, 87(3), 215224. doi: 10.1016/j.biopsych.2019.07.008CrossRefGoogle ScholarPubMed
Brugger, S. P., & Howes, O. D. (2017). Heterogeneity and homogeneity of regional brain structure in schizophrenia: A meta-analysis. JAMA Psychiatry, 74(11), 11041111. doi: 10.1001/jamapsychiatry.2017.2663CrossRefGoogle ScholarPubMed
Buchanan, R. W., & Heinrichs, D. W. (1989). The Neurological Evaluation Scale (NES): A structured instrument for the assessment of neurological signs in schizophrenia. Psychiatry Research, 27(3), 335350.CrossRefGoogle Scholar
Bulk, M., van der Weerd, L., Breimer, W., Lebedev, N., Webb, A., Goeman, J. J., … Bossoni, L. (2018). Quantitative comparison of different iron forms in the temporal cortex of Alzheimer patients and control subjects. Scientific Reports, 8(1), 6898. doi: 10.1038/s41598-018-25021-7CrossRefGoogle ScholarPubMed
Bunzeck, N., Singh-Curry, V., Eckart, C., Weiskopf, N., Perry, R. J., Bain, P. G., … Husain, M. (2013). Motor phenotype and magnetic resonance measures of basal ganglia iron levels in Parkinson's disease. Parkinsonism & Related Disorders, 19(12), 11361142. doi: 10.1016/j.parkreldis.2013.08.011CrossRefGoogle ScholarPubMed
Bush, G., Fink, M., Petrides, G., Dowling, F., & Francis, A. (1996). Catatonia. II. Treatment with lorazepam and electroconvulsive therapy. Acta Psychiatrica Scandinavica, 93(2), 137143.CrossRefGoogle ScholarPubMed
Casanova, M. F., Comparini, S. O., Kim, R. W., & Kleinman, J. E. (1992). Staining intensity of brain iron in patients with schizophrenia: A postmortem study. Journal of Neuropsychiatry and Clinical Neurosciences, 4(1), 3641. doi: 10.1176/jnp.4.1.36Google ScholarPubMed
Costa-Mallen, P., Gatenby, C., Friend, S., Maravilla, K. R., Hu, S. C., Cain, K. C., … Anzai, Y. (2017). Brain iron concentrations in regions of interest and relation with serum iron levels in Parkinson disease. Journal of the Neurological Sciences, 378, 3844. doi: 10.1016/j.jns.2017.04.035CrossRefGoogle ScholarPubMed
Cuesta, M. J., Garcia de Jalon, E., Campos, M. S., Moreno-Izco, L., Lorente-Omenaca, R., Sanchez-Torres, A. M., & Peralta, V. (2018a). Motor abnormalities in first-episode psychosis patients and long-term psychosocial functioning. Schizophrenia Research, 200, 97103. doi: 10.1016/j.schres.2017.08.050CrossRefGoogle Scholar
Cuesta, M. J., Lecumberri, P., Cabada, T., Moreno-Izco, L., Ribeiro, M., Lopez-Ilundain, J. M., … Gomez, M. (2017). Basal ganglia and ventricle volume in first-episode psychosis. A family and clinical study. Psychiatry Research: Neuroimaging, 269, 9096. doi: 10.1016/j.pscychresns.2017.09.010CrossRefGoogle ScholarPubMed
Cuesta, M. J., Moreno-Izco, L., Ribeiro, M., Lopez-Ilundain, J. M., Lecumberri, P., Cabada, T., … Peralta, V. (2018b). Motor abnormalities and cognitive impairment in first-episode psychosis patients, their unaffected siblings and healthy controls. Schizophrenia Research, 200, 5055. doi: 10.1016/j.schres.2017.10.035CrossRefGoogle Scholar
Cuesta, M. J., Sanchez-Torres, A. M., de Jalon, E. G., Campos, M. S., Ibanez, B., Moreno-Izco, L., & Peralta, V. (2014). Spontaneous parkinsonism is associated with cognitive impairment in antipsychotic-naive patients with first-episode psychosis: A 6-month follow-up study. Schizophrenia Bulletin, 40(5), 11641173. doi: 10.1093/schbul/sbt125CrossRefGoogle ScholarPubMed
Daugherty, A. M., & Raz, N. (2015). Appraising the role of iron in brain aging and cognition: Promises and limitations of MRI methods. Neuropsychology Review, 25(3), 272287. doi: 10.1007/s11065-015-9292-yCrossRefGoogle ScholarPubMed
Dazzan, P., Morgan, K. D., Orr, K. G., Hutchinson, G., Chitnis, X., Suckling, J., … Murray, R. M. (2004). The structural brain correlates of neurological soft signs in AESOP first-episode psychoses study. Brain, 127(Pt 1), 143153.CrossRefGoogle ScholarPubMed
Dempster, K., Norman, R., Theberge, J., Densmore, M., Schaefer, B., & Williamson, P. (2017). Cognitive performance is associated with gray matter decline in first-episode psychosis. Psychiatry Research: Neuroimaging, 264, 4651. doi: 10.1016/j.pscychresns.2017.04.007CrossRefGoogle ScholarPubMed
Djaldetti, R., Ziv, I., & Melamed, E. (2006). The mystery of motor asymmetry in Parkinson's disease. Lancet Neurology, 5(9), 796802. doi: 10.1016/S1474-4422(06)70549-XCrossRefGoogle ScholarPubMed
Duan, M., Chen, X., He, H., Jiang, Y., Jiang, S., Xie, Q., … Yao, D. (2015). Altered basal ganglia network integration in schizophrenia. Frontiers in Human Neuroscience, 9, 561. doi: 10.3389/fnhum.2015.00561CrossRefGoogle Scholar
Eisinger, R. S., Urdaneta, M. E., Foote, K. D., Okun, M. S., & Gunduz, A. (2018). Non-motor characterization of the basal ganglia: Evidence from human and non-human primate electrophysiology. Frontiers in Neuroscience, 12, 385. doi: 10.3389/fnins.2018.00385CrossRefGoogle ScholarPubMed
Eustache, P., Nemmi, F., Saint-Aubert, L., Pariente, J., & Peran, P. (2016). Multimodal magnetic resonance imaging in Alzheimer's disease patients at prodromal stage. Journal of Alzheimer's Disease, 50(4), 10351050. doi: 10.3233/JAD-150353CrossRefGoogle ScholarPubMed
Feis, D. L., Pelzer, E. A., Timmermann, L., & Tittgemeyer, M. (2015). Classification of symptom-side predominance in idiopathic Parkinson's disease. NPJ Parkinson's Disease, 1, 15018. doi: 10.1038/npjparkd.2015.18CrossRefGoogle ScholarPubMed
Filatova, S., Koivumaa-Honkanen, H., Hirvonen, N., Freeman, A., Ivandic, I., Hurtig, T., … Miettunen, J. (2017). Early motor developmental milestones and schizophrenia: A systematic review and meta-analysis. Schizophrenia Research, 188, 1320. doi: 10.1016/j.schres.2017.01.029CrossRefGoogle ScholarPubMed
Garvey, M. A., & Cuthbert, B. N. (2017). Developing a motor systems domain for the NIMH RDoC Program. Schizophrenia Bulletin, 43(5), 935936. doi: 10.1093/schbul/sbx095CrossRefGoogle ScholarPubMed
Gay, O., Plaze, M., Oppenheim, C., Mouchet-Mages, S., Gaillard, R., Olie, J. P., … Cachia, A. (2013). Cortex morphology in first-episode psychosis patients with neurological soft signs. Schizophrenia Bulletin, 39(4), 820829. doi: 10.1093/schbul/sbs083CrossRefGoogle ScholarPubMed
Griffiths, P. D., Dobson, B. R., Jones, G. R., & Clarke, D. T. (1999). Iron in the basal ganglia in Parkinson's disease. An in vitro study using extended X-ray absorption fine structure and cryo-electron microscopy. Brain, 122(Pt 4), 667673.CrossRefGoogle Scholar
Guo, W., Jiang, J., Xiao, C., Zhang, Z., Zhang, J., Yu, L., … Liu, G. (2014). Decreased resting-state interhemispheric functional connectivity in unaffected siblings of schizophrenia patients. Schizophrenia Research, 152(1), 170175. doi: 10.1016/j.schres.2013.11.030CrossRefGoogle ScholarPubMed
Gur, R. E., Maany, V., Mozley, P. D., Swanson, C., Bilker, W., & Gur, R. C. (1998). Subcortical MRI volumes in neuroleptic-naive and treated patients with schizophrenia. American Journal of Psychiatry, 155(12), 17111717. doi: 10.1176/ajp.155.12.1711CrossRefGoogle ScholarPubMed
Haijma, S. V., Van Haren, N., Cahn, W., Koolschijn, P. C., Hulshoff Pol, H. E., & Kahn, R. S. (2013). Brain volumes in schizophrenia: A meta-analysis in over 18 000 subjects. Schizophrenia Bulletin, 39(5), 11291138.CrossRefGoogle ScholarPubMed
Hare, D. J., & Double, K. L. (2016). Iron and dopamine: A toxic couple. Brain, 139(Pt 4), 10261035. doi: 10.1093/brain/aww022CrossRefGoogle ScholarPubMed
Hashimoto, R., Mori, T., Nemoto, K., Moriguchi, Y., Noguchi, H., Nakabayashi, T., … Ohnishi, T. (2009). Abnormal microstructures of the basal ganglia in schizophrenia revealed by diffusion tensor imaging. World Journal of Biological Psychiatry, 10(1), 6569. doi: 10.1080/15622970701762536CrossRefGoogle ScholarPubMed
Hibar, D. P., Westlye, L. T., van Erp, T. G., Rasmussen, J., Leonardo, C. D., Faskowitz, J., … Andreassen, O. A. (2016). Subcortical volumetric abnormalities in bipolar disorder. Molecular Psychiatry, 21(12), 17101716. doi: 10.1038/mp.2015.227CrossRefGoogle ScholarPubMed
Hill, K., Bolo, N., Sarvode Mothi, S., Lizano, P., Guimond, S., Tandon, N., … Keshavan, M. (2017). Subcortical surface shape in youth at familial high risk for schizophrenia. Psychiatry Research: Neuroimaging, 267, 3644. doi: 10.1016/j.pscychresns.2017.07.002CrossRefGoogle ScholarPubMed
Hirjak, D., Thomann, P. A., Kubera, K. M., Wolf, N. D., Sambataro, F., & Wolf, R. C. (2015). Motor dysfunction within the schizophrenia-spectrum: A dimensional step towards an underappreciated domain. Schizophrenia Research, 169(1–3), 217233. doi: 10.1016/j.schres.2015.10.022CrossRefGoogle ScholarPubMed
Ho, B. C., Andreasen, N. C., Ziebell, S., Pierson, R., & Magnotta, V. (2011). Long-term antipsychotic treatment and brain volumes: A longitudinal study of first-episode schizophrenia. Archives of General Psychiatry, 68(2), 128137. doi: 10.1001/archgenpsychiatry.2010.199CrossRefGoogle ScholarPubMed
Hoptman, M. J., Zuo, X. N., D'Angelo, D., Mauro, C. J., Butler, P. D., Milham, M. P., & Javitt, D. C. (2012). Decreased interhemispheric coordination in schizophrenia: A resting state fMRI study. Schizophrenia Research, 141(1), 17. doi: 10.1016/j.schres.2012.07.027CrossRefGoogle ScholarPubMed
IBM Corp. (2011). IBM SPSS Statistics for Windows, Version 20.0.Google Scholar
Jahanshahi, M., Obeso, I., Rothwell, J. C., & Obeso, J. A. (2015). A fronto-striato-subthalamic-pallidal network for goal-directed and habitual inhibition. Nature Reviews Neuroscience, 16(12), 719732. doi: 10.1038/nrn4038CrossRefGoogle ScholarPubMed
Kahn, R. S., & Sommer, I. E. (2015). The neurobiology and treatment of first-episode schizophrenia. Molecular Psychiatry, 20(1), 8497. doi: 10.1038/mp.2014.66CrossRefGoogle ScholarPubMed
Kamis, D., Stratton, L., Calvo, M., Padilla, E., Florenzano, N., Guerrero, G., … de Erausquin, G. A. (2015). Sex and laterality differences in parkinsonian impairment and transcranial ultrasound in never-treated schizophrenics and their first degree relatives in an Andean population. Schizophrenia Research, 164(1–3), 250255. doi: 10.1016/j.schres.2015.01.035CrossRefGoogle Scholar
Katzen, H. L., Levin, B. E., & Weiner, W. (2006). Side and type of motor symptom influence cognition in Parkinson's disease. Movement Disorders, 21(11), 19471953. doi: 10.1002/mds.21105CrossRefGoogle ScholarPubMed
Kim, J., & Wessling-Resnick, M. (2014). Iron and mechanisms of emotional behavior. Journal of Nutritional Biochemistry, 25(11), 11011107. doi: 10.1016/j.jnutbio.2014.07.003CrossRefGoogle ScholarPubMed
Li, T., Wang, Q., Zhang, J., Rolls, E. T., Yang, W., Palaniyappan, L., … Feng, J. (2017). Brain-wide analysis of functional connectivity in first-episode and chronic stages of schizophrenia. Schizophrenia Bulletin, 43(2), 436448. doi: 10.1093/schbul/sbw099Google ScholarPubMed
Li, H. J., Xu, Y., Zhang, K. R., Hoptman, M. J., & Zuo, X. N. (2015). Homotopic connectivity in drug-naive, first-episode, early-onset schizophrenia. Journal of Child Psychology and Psychiatry and Allied Disciplines, 56(4), 432443. doi: 10.1111/jcpp.12307CrossRefGoogle ScholarPubMed
Lieberman, J. A., Tollefson, G. D., Charles, C., Zipursky, R., Sharma, T., Kahn, R. S., … Group, H. S. (2005). Antipsychotic drug effects on brain morphology in first-episode psychosis. Archives of General Psychiatry, 62(4), 361370. doi: 10.1001/archpsyc.62.4.361CrossRefGoogle ScholarPubMed
Lingjaerde, O., Ahlfors, U. G., Bech, P., Dencker, S. J., & Elgen, K. (1987). The UKU side effect rating scale. A new comprehensive rating scale for psychotropic drugs and a cross-sectional study of side effects in neuroleptic-treated patients. Acta Psychiatrica Scandinavica. Supplementum, 334, 1100.CrossRefGoogle Scholar
Mamah, D., Alpert, K. I., Barch, D. M., Csernansky, J. G., & Wang, L. (2016). Subcortical neuromorphometry in schizophrenia spectrum and bipolar disorders. Neuroimage: Clinical, 11, 276286. doi: 10.1016/j.nicl.2016.02.011CrossRefGoogle ScholarPubMed
Mancuso, L., Costa, T., Nani, A., Manuello, J., Liloia, D., Gelmini, G., … Cauda, F. (2019). The homotopic connectivity of the functional brain: A meta-analytic approach. Scientific Reports, 9(1), 3346. doi: 10.1038/s41598-019-40188-3CrossRefGoogle ScholarPubMed
McCutcheon, R. A., Abi-Dargham, A., & Howes, O. D. (2019). Schizophrenia, dopamine and the Striatum: From biology to symptoms. Trends in Neurosciences, 42(3), 205220. doi: 10.1016/j.tins.2018.12.004CrossRefGoogle ScholarPubMed
McCutcheon, R. A., Krystal, J. H., & Howes, O. D. (2020). Dopamine and glutamate in schizophrenia: Biology, symptoms and treatment. World Psychiatry, 19(1), 1533. doi: 10.1002/wps.20693CrossRefGoogle ScholarPubMed
Mittal, V. A., Bernard, J. A., & Northoff, G. (2017). What can different motor circuits tell us about psychosis? An RDoC Perspective. Schizophrenia Bulletin, 43(5), 949955.CrossRefGoogle ScholarPubMed
Molina, J. L., Gonzalez Aleman, G., Florenzano, N., Padilla, E., Calvo, M., Guerrero, G., … de Erausquin, G. A. (2016). Prediction of neurocognitive deficits by parkinsonian motor impairment in schizophrenia: A study in neuroleptic-naive subjects, unaffected first-degree relatives and healthy controls from an indigenous population. Schizophrenia Bulletin, 42(6), 14861495. doi: 10.1093/schbul/sbw023CrossRefGoogle ScholarPubMed
Musliner, K. L., Mortensen, P. B., McGrath, J. J., Suppli, N. P., Hougaard, D. M., Bybjerg-Grauholm, J., … Bipolar Disorder Working Group of the Psychiatric Genomics, C. (2019). Association of polygenic liabilities for major depression, bipolar disorder, and schizophrenia with risk for depression in the Danish population. JAMA Psychiatry, 76(5), 516525. doi:10.1001/jamapsychiatry.2018.4166.CrossRefGoogle ScholarPubMed
Obeso, J. A., Rodriguez-Oroz, M. C., Stamelou, M., Bhatia, K. P., & Burn, D. J. (2014). The expanding universe of disorders of the basal ganglia. Lancet (London, England), 384(9942), 523531. doi: 10.1016/S0140-6736(13)62418-6CrossRefGoogle ScholarPubMed
Okada, N., Fukunaga, M., Yamashita, F., Koshiyama, D., Yamamori, H., Ohi, K., … Hashimoto, R. (2016). Abnormal asymmetries in subcortical brain volume in schizophrenia. Molecular Psychiatry, 21(10), 14601466. doi: 10.1038/mp.2015.209CrossRefGoogle Scholar
Patenaude, B., Smith, S. M., Kennedy, D. N., & Jenkinson, M. (2011). A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage, 56(3), 907922. doi: 10.1016/j.neuroimage.2011.02.046CrossRefGoogle ScholarPubMed
Peralta, V., Campos, M. S., García de Jalon, E., & Cuesta, M. J. (2010). Motor behavior abnormalities in drug-naive patients with schizophrenia spectrum disorders. Movement Disorders, 25(8), 10681076.CrossRefGoogle ScholarPubMed
Peralta, V., & Cuesta, M. J. (2017). Motor abnormalities: From neurodevelopmental to neurodegenerative through ‘functional’ (neuro)psychiatric disorders. Schizophrenia Bulletin, 43(5), 956971. doi: 10.1093/schbul/sbx089CrossRefGoogle ScholarPubMed
Peralta, V., Cuesta, M. J., Mata, I., Serrano, J. F., Perez-Nievas, F., & Natividad, M. C. (1999). Serum iron in catatonic and noncatatonic psychotic patients. Biological Psychiatry, 45(6), 788790.CrossRefGoogle ScholarPubMed
Peran, P., Cherubini, A., Assogna, F., Piras, F., Quattrocchi, C., Peppe, A., … Sabatini, U. (2010). Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. Brain, 133(11), 34233433. doi: 10.1093/brain/awq212CrossRefGoogle ScholarPubMed
Pfefferbaum, A., Adalsteinsson, E., Rohlfing, T., & Sullivan, E. V. (2009). MRI Estimates of brain iron concentration in normal aging: Comparison of field-dependent (FDRI) and phase (SWI) methods. Neuroimage, 47(2), 493500. doi: 10.1016/j.neuroimage.2009.05.006CrossRefGoogle ScholarPubMed
Quattrone, D., Di Forti, M., Gayer-Anderson, C., Ferraro, L., Jongsma, H. E., Tripoli, G., … Reininghaus, U. (2019). Transdiagnostic dimensions of psychopathology at first episode psychosis: Findings from the multinational EU-GEI study. Psychological Medicine, 49(8), 13781391. doi: 10.1017/S0033291718002131CrossRefGoogle ScholarPubMed
Roiz-Santianez, R., Ayesa-Arriola, R., Tordesillas-Gutierrez, D., Ortiz-Garcia de la Foz, V., Perez-Iglesias, R., Pazos, A., … Crespo-Facorro, B. (2014). Three-year longitudinal population-based volumetric MRI study in first-episode schizophrenia spectrum patients. Psychological Medicine, 44(8), 15911604. doi: 10.1017/S0033291713002365CrossRefGoogle ScholarPubMed
Sedlacik, J., Boelmans, K., Lobel, U., Holst, B., Siemonsen, S., & Fiehler, J. (2014). Reversible, irreversible and effective transverse relaxation rates in normal aging brain at 3T. Neuroimage, 84, 10321041. doi: 10.1016/j.neuroimage.2013.08.051CrossRefGoogle ScholarPubMed
Shenton, M. E., Whitford, T. J., & Kubicki, M. (2010). Structural neuroimaging in schizophrenia: From methods to insights to treatments. Dialogues in Clinical Neuroscience, 12(3), 317332.Google ScholarPubMed
Sian-Hulsmann, J., Mandel, S., Youdim, M. B., & Riederer, P. (2011). The relevance of iron in the pathogenesis of Parkinson's disease. Journal of Neurochemistry, 118(6), 939957. doi: 10.1111/j.1471-4159.2010.07132.xCrossRefGoogle ScholarPubMed
Simonyan, K. (2019). Recent advances in understanding the role of the basal ganglia. F1000 Research, 8, pii: F1000 Faculty Rev-122. doi: 10.12688/f1000research.16524.1.CrossRefGoogle ScholarPubMed
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl 1), S208S219. doi: 10.1016/j.neuroimage.2004.07.051CrossRefGoogle ScholarPubMed
Spinks, R., Nopoulos, P., Ward, J., Fuller, R., Magnotta, V. A., & Andreasen, N. C. (2005). Globus pallidus volume is related to symptom severity in neuroleptic naive patients with schizophrenia. Schizophrenia Research, 73(2–3), 229233. doi: 10.1016/j.schres.2004.05.020CrossRefGoogle ScholarPubMed
Spoletini, I., Cherubini, A., Banfi, G., Rubino, I. A., Peran, P., Caltagirone, C., & Spalletta, G. (2011). Hippocampi, thalami, and accumbens microstructural damage in schizophrenia: A volumetry, diffusivity, and neuropsychological study. Schizophrenia Bulletin, 37(1), 118130. doi: 10.1093/schbul/sbp058CrossRefGoogle ScholarPubMed
Tanner, J. J., McFarland, N. R., & Price, C. C. (2017). Striatal and hippocampal atrophy in idiopathic Parkinson's disease patients without dementia: A morphometric analysis. Frontiers in Neurology, 8, 139. doi: 10.3389/fneur.2017.00139CrossRefGoogle ScholarPubMed
Tarcijonas, G., Foran, W., Blazer, A., Eack, S. M., Luna, B., & Sarpal, D. K. (2019). Independent support for corticopallidal contributions to schizophrenia-related functional impairment. Schizophrenia Research. pii: S0920-9964(19)30576-6. doi: 10.1016/j.schres.2019.12.006Google ScholarPubMed
Tomer, R., Levin, B. E., & Weiner, W. J. (1993). Side of onset of motor symptoms influences cognition in Parkinson's disease. Annals of Neurology, 34(4), 579584. doi: 10.1002/ana.410340412CrossRefGoogle ScholarPubMed
van Erp, T. G., Hibar, D. P., Rasmussen, J. M., Glahn, D. C., Pearlson, G. D., Andreassen, O. A., … Turner, J. A. (2016). Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Molecular Psychiatry, 21(4), 547553. doi: 10.1038/mp.2015.63CrossRefGoogle ScholarPubMed
Veenith, T. V., Carter, E., Grossac, J., Newcombe, V. F., Outtrim, J. G., Lupson, V., … Coles, J. P. (2013). Inter subject variability and reproducibility of diffusion tensor imaging within and between different imaging sessions. PLoS ONE, 8(6), e65941. doi: 10.1371/journal.pone.0065941CrossRefGoogle ScholarPubMed
Walker, E. F., Savoie, T., & Davis, D. (1994). Neuromotor precursors of schizophrenia. Schizophrenia Bulletin, 20(3), 441451.CrossRefGoogle ScholarPubMed
Walther, S. (2015). Psychomotor symptoms of schizophrenia map on the cerebral motor circuit. Psychiatry Research, 233(3), 293298. doi: 10.1016/j.pscychresns.2015.06.010CrossRefGoogle ScholarPubMed
Walther, S., & Strik, W. (2012). Motor symptoms and schizophrenia. Neuropsychobiology, 66(2), 7792.CrossRefGoogle Scholar
Wang, J. Y., Zhuang, Q. Q., Zhu, L. B., Zhu, H., Li, T., Li, R., … Zhu, J. H. (2016). Meta-analysis of brain iron levels of Parkinson's disease patients determined by postmortem and MRI measurements. Scientific Reports, 6, 36669. doi: 10.1038/srep36669CrossRefGoogle ScholarPubMed
Ward, R. J., Zucca, F. A., Duyn, J. H., Crichton, R. R., & Zecca, L. (2014). The role of iron in brain ageing and neurodegenerative disorders. The Lancet. Neurology, 13(10), 10451060. doi: 10.1016/s1474-4422(14)70117-6CrossRefGoogle ScholarPubMed
Wei, P., Zhang, Z., Lv, Z., & Jing, B. (2017). Strong functional connectivity among homotopic brain areas is vital for motor control in unilateral limb movement. Frontiers in Human Neuroscience, 11, 366. doi: 10.3389/fnhum.2017.00366CrossRefGoogle ScholarPubMed
Weiser, M., Levkowitch, Y., Neuman, M., & Yehuda, S. (1994). Decrease of serum iron in acutely psychotic schizophrenic patients. International Journal of Neuroscience, 78(1–2), 4952.CrossRefGoogle ScholarPubMed
Wheeler, A. L., & Voineskos, A. N. (2014). A review of structural neuroimaging in schizophrenia: From connectivity to connectomics. Frontiers in Human Neuroscience, 8, 653. doi: 10.3389/fnhum.2014.00653CrossRefGoogle ScholarPubMed
Winkler, A. M., Ridgway, G. R., Webster, M. A., Smith, S. M., & Nichols, T. E. (2014). Permutation inference for the general linear model. Neuroimage, 92, 381397. doi: 10.1016/j.neuroimage.2014.01.060CrossRefGoogle ScholarPubMed
Woodward, N. D., & Heckers, S. (2016). Mapping thalamocortical functional connectivity in chronic and early stages of psychotic disorders. Biological Psychiatry, 79(12), 10161025. doi: 10.1016/j.biopsych.2015.06.026CrossRefGoogle ScholarPubMed
Zhao, W., Guo, S., Linli, Z., Yang, A. C., Lin, C. P., & Tsai, S. J. (2019). Functional, anatomical, and morphological networks highlight the role of basal ganglia-thalamus-cortex circuits in schizophrenia. Schizophrenia Bulletin. pii: sbz062. doi: 10.1093/schbul/sbz062CrossRefGoogle Scholar
Zhao, Q., Li, Z., Huang, J., Yan, C., Dazzan, P., Pantelis, C., … Chan, R. C. (2014). Neurological soft signs are not ‘soft’ in brain structure and functional networks: Evidence from ALE meta-analysis. Schizophrenia Bulletin, 40(3), 626641. doi: 10.1093/schbul/sbt063CrossRefGoogle Scholar
Supplementary material: File

Cuesta et al. supplementary material

Tables S1-S2

Download Cuesta et al. supplementary material(File)
File 22.3 KB