psychiatryПСИХИАТРИЯPsychiatry (Moscow) (Psikhiatriya)1683-83192618-6667FSBSI “The Mental Health Research Centre”; LLC «Publisher «MIA»10.30629/2618-6667-2022-20-3-6-15psychiatry-856Research ArticleПСИХОПАТОЛОГИЯ, КЛИНИЧЕСКАЯ И БИОЛОГИЧЕСКАЯ ПСИХИАТРИЯPSYCHOPATHOLOGY, CLINICAL AND BIOLOGICAL PSYCHIATRYДефицит перинейрональных олигодендроцитов сателлитов в слое 3 префронтальной коры при шизофренииDeficit of Perineuronal Satellite Oligodendrocytes in Layer 3 of the Prefrontal Cortex in Schizophreniahttps://orcid.org/0000-0003-3710-8456КоломеецН. С.KolomeetsN. S.

Наталья Степановна Коломеец, доктор биологических наук, лаборатория клинической нейроморфологии

Москва

Natalya S. Kolomeets, Dr. of Sci. (Biol.), Clinical Neuropathology Laboratory

Moscow

ns-kolomeets@mail.ruhttps://orcid.org/0000-0003-1489-7915ВостриковВ. М.VostrikovV. M.

Виктор Михайлович Востриков, доктор медицинских наук, лаборатория клинической нейроморфологии

Москва

Viktor M. Vostrikov, Dr. of Sci. (Med.)

Moscow

https://orcid.org/0000-0001-9543-7421УрановаН. А.UranovaN. A.

Уранова Наталия Александровна, доктор медицинских наук, заведующий лабораторией, лаборатория клинической нейроморфологии

Москва

Natalya A. Uranova, Dr. of Sci. (Med.), Head of Neuropathology Laboratory

Moscow

uranovan@mail.ruФГБНУ «Научный центр психического здоровья»РоссияFSBSI “Mental Health Research Centre”Russian Federation202227092022203615Copyright © Коломеец Н.С., Востриков В.М., Уранова Н.А., 20222022Коломеец Н.С., Востриков В.М., Уранова Н.А.Kolomeets N.S., Vostrikov V.M., Uranova N.A.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.journalpsychiatry.com/jour/article/view/856

Обоснование: дефицит внутрикорковой миелинизации при шизофрении наиболее выражен в префронтальной коре и тесно связан с нарушением процессинга информации в мозге. Ранее мы показали снижение численной плотности (Nv) миелинизирующих олигодендроцитов (Ол) и кластеров олигодендроцитов (ОлК), образуемых их предшественниками, в 3-м и 5-м слоях поля 10 при шизофрении. Однако роль перинейрональных олигодендроцитов сателлитов (Сат-Ол) в патологии мозга человека на сегодня мало исследована.Цель исследования: оценить число Сат-Ол на пирамидный нейрон в слое 3 поля 10 префронтальной коры при шизофрении по сравнению с контролем и исследовать корреляционные связи между числом Сат-Ол на нейрон и Nv Ол, а также Nv ОлК в норме и при шизофрении.Материал и методы: изучены образцы мозга префронтальной коры из коллекции лаборатории клинической нейроморфологии НЦПЗ РАМН. Определяли число Сат-Ол на нейрон в подслоях 3а, 3в и 3с слоя 3 в поле 10 префронтальной коры в контроле (20 случаев) и при шизофрении (20 случаев) на тех же срезах, которые ранее использовались для определения Nv Ол и Nv ОлК.Результаты и заключение: число Сат-Ол на пирамидный нейрон достоверно снижено во всех подслоях слоя 3 при шизофрении по сравнению с контролем (на 17 и 24% соответственно, р < 0,01). Не выявлено достоверных корреляций между числом Сат-Ол на нейрон и Nv Ол или Nv ОлК. Сравнение данных с результатами ранее проведенного аналогичного исследования в полях 39 и 40 нижней теменной коры свидетельствует о том, что изменения числа Сат-Ол на нейрон и их корреляционных связей в различных областях коры могут быть связаны с особенностями функционирования соответствующих нейронных сетей в норме и при шизофрении.

Background: impaired intracortical myelination most pronounced in prefrontal cortex is tightly linked to inadequate information processing in schizophrenia. Previously we reported a significant decrease in the numerical density (Nv) of oligodendrocytes (Ol) and oligodendrocyte clusters (OlC) in layers 3 and 5 of the prefrontal cortex, Brodmann area 10 (BA10) in schizophrenia. To date there are few studies on the possible role of perineuronal oligodendrocyte satellites (Sat-Ol) in human brain pathology.Aim of the study: to estimate the number of Sat-Ol per pyramidal neuron in layer 3 of BA10 in schizophrenia as compared to healthy controls and to evaluate the possible correlations between the number of Sat-Ol and NvOl or NvOlC in schizophrenia and normal controls.Material and methods: we investigated the number of Sat-Ol per pyramidal neuron in sublayers 3a, 3b and 3c of layer 3 of BA10 in schizophrenia (n = 20) as compared to healthy controls (n = 20) in the same section collection previously used for the study of the NvOl and NvOlC.Rеsults and conclusion: we found a significant reduction in the number of Sat-Ol in schizophrenia as compared to the control group (17 and 24% resp., p < 0.01). There were no correlations between the number of Sat-Ol and the NvOl or NvOlC. The comparison of current data to similar findings from our previous studies in BA39 and BA40 of the inferior parietal cortex indicates that specific features of oligodendrocyte alterations and their correlation patterns may be associated with specific activity-driven plasticity of corresponding networks in normal and schizophrenia brains.

префронтальная кораолигодендроциты сателлитыморфометрияшизофренияprefrontal cortexoligodendrocyte satellitesmorphometryschizophreniaReferencesCassoli JS, Guest PC, Malchow B, Schmitt A, Falkai P, Martins-de-Souz D. Disturbed macroconnectivity in schizophrenia linked to oligodendrocyte dysfunction: from structural findings to molecules. NPJ Schizophr. 2015;1:15034. doi: 10.1038/npjschz.2015.34Cassoli JS, Guest PC, Malchow B, Schmitt A, Falkai P, Martins-de-Souz D. Disturbed macroconnectivity in schizophrenia linked to oligodendrocyte dysfunction: from structural findings to molecules. NPJ Schizophr. 2015;1:15034. doi: 10.1038/npjschz.2015.34Bartzokis G. Neuroglialpharmacology: myelination as a shared mechanism of action of psychotropic treatments. Neuropharmacology. 2012;62(7):2137–2153. doi: 10.1016/j.neuropharm.2012.01.015Bartzokis G. Neuroglialpharmacology: myelination as a shared mechanism of action of psychotropic treatments. Neuropharmacology. 2012;62(7):2137–2153. doi: 10.1016/j.neuropharm.2012.01.015Grydeland H, Walhovd KB, Tamnes CK, Westlye LT, Fjell AM. Intracortical myelin links with performance variability across the human lifespan: results from T1- and T2-weighted MRI myelin mapping and diffusion tensor imaging. J Neurosci. 2013;33(47):18618–18630. doi: 10.1523/JNEUROSCI.2811-13.2013Grydeland H, Walhovd KB, Tamnes CK, Westlye LT, Fjell AM. Intracortical myelin links with performance variability across the human lifespan: results from T1- and T2-weighted MRI myelin mapping and diffusion tensor imaging. J Neurosci. 2013;33(47):18618–18630. doi: 10.1523/JNEUROSCI.2811-13.2013Huntenburg JM, Bazin P-L, Goulas A, Villringer А, Margulies DA. A Systematic Relationship Between Functional Connectivity and Intracortical Myelin in the Human Cerebral Cortex. Cereb Cortex. 2017;27(2):981–997. doi: 10.1093/cercor/bhx030Huntenburg JM, Bazin P-L, Goulas A, Villringer А, Margulies DA. A Systematic Relationship Between Functional Connectivity and Intracortical Myelin in the Human Cerebral Cortex. Cereb Cortex. 2017;27(2):981–997. doi: 10.1093/cercor/bhx030Sui YV, Bertisch H, Lee H-H, Storey P, Babb JS, Goff DC, Samsonov A, Lazar M. Quantitative Macromolecular Proton Fraction Mapping Reveals Altered Cortical Myelin Pro-le in Schizophrenia Spectrum Disorders. Cereb Cortex Commun. 2021;2(2):tgab015. doi: 10.1093/texcom/tgab015 eCollection 2021.Sui YV, Bertisch H, Lee H-H, Storey P, Babb JS, Goff DC, Samsonov A, Lazar M. Quantitative Macromolecular Proton Fraction Mapping Reveals Altered Cortical Myelin Profile in Schizophrenia Spectrum Disorders. Cereb Cortex Commun. 2021;2(2):tgab015. doi: 10.1093/texcom/tgab015 eCollection 2021.Wei W, Zhang Y, Li Y, Meng Y, Li M, Wang Q, Deng W, Ma X, Palaniyappan L, Zhang N. Depth dependent abnormal cortical myelination in first episode treatment naïve schizophrenia. Hum Brain Mapp. 2020;41(10):2782–2793. doi: 10.1002/hbm.24977Wei W, Zhang Y, Li Y, Meng Y, Li M, Wang Q, Deng W, Ma X, Palaniyappan L, Zhang N. Depth dependent abnormal cortical myelination in first episode treatment naïve schizophrenia. Hum Brain Mapp. 2020;41(10):2782–2793. doi: 10.1002/hbm.24977Hof PR, Haroutunian V, Friedrich VL, Byne W, Buitron C, Perl DP, Davis KL. Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia Biol Psychiatry. 2003;53:1075–1085. doi: 10.1016/S0006-3223(03)00237-3Hof PR, Haroutunian V, Friedrich VL, Byne W, Buitron C, Perl DP, Davis KL. Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia Biol Psychiatry. 2003;53:1075–1085. doi: 10.1016/S0006-3223(03)00237-3Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, Starkey M, Webster MJ, Yolken RH, Bahn S. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder Lancet. 2003;362(9386):798–805. doi: 10.1016/S0140-6736(03)14289-4Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, Starkey M, Webster MJ, Yolken RH, Bahn S. Oligodendrocyte dysfunction in schizophrenia and bipolar disorder Lancet. 2003;362(9386):798–805. doi: 10.1016/S0140-6736(03)14289-4Polito A, Reynolds R. NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat. 2005;207(6):707–716. doi: 10.1111/j.1469-7580.2005.00454.xPolito A, Reynolds R. NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat. 2005;207(6):707–716. doi: 10.1111/j.1469-7580.2005.00454.xZhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development. 2011;138(4):745–753. doi: 10.1242/dev.047951Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development. 2011;138(4):745–753. doi: 10.1242/dev.047951Gibson EM, Purger D, Mount CW, Goldstein AK, Lin GL, Wood LS, Inema I, Miller SE, Bieri G, Zuchero JB, Barres BA, Woo PJ, Vogel H, Monje M. Neronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science. 2014;344(6183):1252304. doi: 10.1126/science.1252304 Epub 2014 Apr 10. PMID: 24727982.Gibson EM, Purger D, Mount CW, Goldstein AK, Lin GL, Wood LS, Inema I, Miller SE, Bieri G, Zuchero JB, Barres BA, Woo PJ, Vogel H, Monje M. Neronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science. 2014;344(6183):1252304. doi: 10.1126/science.1252304 Epub 2014 Apr 10. PMID: 24727982.Востриков ВМ, Уранова НА. Дефицит олигодендроцитов в лобной коре при шизофрении. Журнал неврологии и психиатрии имени С.С. Корсакова. 2018;118(5):100–103. doi: 10.17116/jnevro201811851100Vostrikov VM, Uranova NA. Deficit of oligodendrocytes in the frontal cortex in schizophrenia. S.S. Korsakov Journal of Neurology and Psychiatry/ Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova. 2018;118(5):100–103. (In Russ.). doi: 10.17116/jnevro201811851100Kolomeets NS, Uranova NA. Reduced oligodendrocyte density in layer 5 of the prefrontal cortex in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2018;23:1– 8. doi: 10.1007/s00406-018-0888-0Kolomeets NS, Uranova NA. Reduced oligodendrocyte density in layer 5 of the prefrontal cortex in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2018;23:1– 8. doi: 10.1007/s00406-018-0888-0Kolomeets NS, Vostrikov VM. Uranova NA. Abnormalities in oligodendrocyte clusters in the inferior parietal cortex in schizophrenia are associated with insight. Eur J Psychiat. 2013;27(4):248–258. doi: 10.4321/S0213-61632013000400003Kolomeets NS, Vostrikov VM. Uranova NA. Abnormalities in oligodendrocyte clusters in the inferior parietal cortex in schizophrenia are associated with insight. Eur J Psychiat. 2013;27(4):248–258. doi: 10.4321/S0213-61632013000400003Uranova NA, Vostrikov VM, Kolomeets NS, Oligodendrocyte abnormalities in layer 5 in the inferior parietal lobule are associated with lack of insight: a postmortem morphometric study. Eur J Psychiat. 2015;29(3):215–222. doi: 10.4321/S0213-61632015000300006Uranova NA, Vostrikov VM, Kolomeets NS, Oligodendrocyte abnormalities in layer 5 in the inferior parietal lobule are associated with lack of insight: a postmortem morphometric study. Eur J Psychiat. 2015;29(3):215–222. doi: 10.4321/S0213-61632015000300006Коломеец НС, Уранова НА. Нарушение кластеризации олигодендроцитов в теменной коре при шизофрении: связь с возрастом к началу заболевания. Психиатрия. 2015;3(67):52–57.Kolomeets NS, Uranova NA. Abnormalities of oligodendrocyte clusters in the inferior parietal cortex: effect of age at onset of disease. Psychiatry (Moscow) (Psikhiatryia). (In Russ.). 2015:3(67):52–57.Bernstein H-G, Keilhoff G, Dobrowolny H, Guest PC, Steiner J. Perineuronal oligodendrocytes in health and disease: the journey so far. Rev Neurosci. 2019;31(1):89–99. doi: 10.1515/revneuro-2019-0020Bernstein H-G, Keilhoff G, Dobrowolny H, Guest PC, Steiner J. Perineuronal oligodendrocytes in health and disease: the journey so far. Rev Neurosci. 2019;31(1):89–99. doi: 10.1515/revneuro-2019-0020Takasaki C, Yamasaki M, Uchigashima M, Konno K, Yanagawa Y, Watanabe M. Cytochemical and cytological properties of perineuronal oligodendrocytes in the mouse cortex. Eur J Neurosci. 2010;32:1326–1336. doi: 10.1111/j.1460-9568.2010.07377.xTakasaki C, Yamasaki M, Uchigashima M, Konno K, Yanagawa Y, Watanabe M. Cytochemical and cytological properties of perineuronal oligodendrocytes in the mouse cortex. Eur J Neurosci. 2010;32:1326–1336. doi: 10.1111/j.1460-9568.2010.07377.xBattefeld A, Klooster J, Kole MHP. Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity. Nat Commun. 2016;7:11298. doi: 10.1038/ncomms11298Battefeld A, Klooster J, Kole MHP. Myelinating satellite oligodendrocytes are integrated in a glial syncytium constraining neuronal high-frequency activity. Nat Commun. 2016;7:11298. doi: 10.1038/ncomms11298Kolomeets NS, Uranova NA. Reduced number of satellite oligodendrocytes of pyramidal neurons in layer 5 of the prefrontal cortex in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2022;272(6):947–955. doi: 10.1007/s00406-021-01353-wKolomeets NS, Uranova NA. Reduced number of satellite oligodendrocytes of pyramidal neurons in layer 5 of the prefrontal cortex in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2022;272(6):947–955. doi: 10.1007/s00406-021-01353-wVostrikov VM, Kolomeets NS, Uranova NA. De-cit of perineuronal oligodendrocytes in the inferior parietal lobule is associated with lack of insight in schizophrenia. Eur J Psychiat. 2014;28(2):114–123. doi: 10.4321/S0213-61632014000200005Vostrikov VM, Kolomeets NS, Uranova NA. Deficit of perineuronal oligodendrocytes in the inferior parietal lobule is associated with lack of insight in schizophrenia. Eur J Psychiat. 2014;28(2):114–123. doi: 10.4321/S0213-61632014000200005Szuchet S, Nielsen JA, Lovas G, Domowicz MS, de Velasco JM, Maric D, Hudson LD. The genetic signature of perineuronal oligodendrocytes reveals their unique phenotype. Eur J Neurosci. 2011;34(12):1906–1922. doi: 10.1111/j.1460-9568.2011.07922.xSzuchet S, Nielsen JA, Lovas G, Domowicz MS, de Velasco JM, Maric D, Hudson LD. The genetic signature of perineuronal oligodendrocytes reveals their unique phenotype. Eur J Neurosci. 2011;34(12):1906–1922. doi: 10.1111/j.1460-9568.2011.07922.xКоломеец НС, Востриков ВМ, Уранова НА Нарушения кластеризации олигодендроцитов в супра- и инфрагранулярных слоях поля 10 префронтальной коры при шизофрении. Журнал неврологии и психиатрии имени С.С. Корсакова. 2019;119(12):62–68. doi: 10.17116/jnevro 201911912162Kolomeets NS, Vostrikov VM, Uranova NA. Abnormalities of oligodendrocyte clusters in supra- and infragranular layers of the prefrontal cortex in schizophrenia. S.S. Korsakov Journal of Neurology and Psychiatry/Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova. 2019;119(12):62–68. (In Russ.). doi: 10.17116/jnevro201911912162Schmidt A, Diwadkar VA, Smieskova R, Harrisberger F, Lang UE, McGuire P, Fusar-Poli P, Borgwardt S. Approaching a network connectivity-driven classification of the psychosis continuum: a selective review and suggestions for future research. Front Hum Neurosci. 2014;8:1047. doi: 10.3389/fnhum.2014.01047Schmidt A, Diwadkar VA, Smieskova R, Harrisberger F, Lang UE, McGuire P, Fusar-Poli P, Borgwardt S. Approaching a network connectivity-driven classi-- cation of the psychosis continuum: a selective review and suggestions for future research. Front Hum Neurosci. 2014;8:1047. doi: 10.3389/fnhum.2014.01047Whitfield-Gabrieli S, Ford JM. Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol. 2012;8:49–76. doi: 10.1146/annurev-clinpsy-032511-43049Whit-eld-Gabrieli S, Ford JM. Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol. 2012;8:49–76. doi: 10.1146/annurev-clinpsy-032511-43049Sakurai T, Gamo NJ, Hikida T, Kim S-H, Murai T, Tomoda T, Sawa A. Cnvoerging models of schizophrenia — Network alterations of prefrontal cortex underlying cognitive impairments. Prog Neurobiol. 2015;134:178–201. doi: 10.1016/j.pneurobio.2015.09.010Sakurai T, Gamo NJ, Hikida T, Kim S-H, Murai T, Tomoda T, Sawa A. Cnvoerging models of schizophrenia — Network alterations of prefrontal cortex underlying cognitive impairments. Prog Neurobiol. 2015;134:178–201. doi: 10.1016/j.pneurobio.2015.09.010Davis JM. Dose equivalence of the antipsychotic drugs. J Psychiatr Res. 1974;11:65–69. doi: 10.1016/0022-3956(74)90071-5Davis JM. Dose equivalence of the antipsychotic drugs. J Psychiatr Res. 1974;11:65–69. doi: 10.1016/0022-3956(74)90071-5Tachikawa M, Fukaya M, Terasaki T, Ohtsuki SM, Watanabe M. Distinct cellular expressions of creatine synthetic enzyme GAMT and creatine kinases uCK-Mi and CK-B suggest a novel neuron–glial relationship for brain energy homeostasis. Eur J Neurosci. 2004;20:144–160. doi: 10.1111/j.1460-9568.2004.03478.xTachikawa M, Fukaya M, Terasaki T, Ohtsuki SM, Watanabe M. Distinct cellular expressions of creatine synthetic enzyme GAMT and creatine kinases uCK-Mi and CK-B suggest a novel neuron–glial relationship for brain energy homeostasis. Eur J Neurosci. 2004;20:144–160. doi: 10.1111/j.1460-9568.2004.03478.xIchihara A, Greenberg DM. Further studies on the pathway of serine formation from carbohydrate. J Biol Chem. 1957;224:331–340.Ichihara A, Greenberg DM. Further studies on the pathway of serine formation from carbohydrate. J Biol Chem. 1957;224:331–340.Furuya S, Tabata T, Mitoma J, Yamada K, Yamasaki M, Makino A, Yamamoto T, Watanabe M, Kano M, Hirabayashi Y. l-serine and glycine serve as major astroglia-derived trophic factors for cerebellar Purkinje neurons. Proc Natl Acad Sci USA. 2000;97:11528–11533. doi: 10.1073/pnas.200364497Furuya S, Tabata T, Mitoma J, Yamada K, Yamasaki M, Makino A, Yamamoto T, Watanabe M, Kano M, Hirabayashi Y. l-serine and glycine serve as major astroglia-derived trophic factors for cerebellar Purkinje neurons. Proc Natl Acad Sci USA. 2000;97:11528–11533. doi: 10.1073/pnas.200364497Rajkowska G, Selemon LD, Goldman-Rakic PS. Neuronal and glial somal size in the prefrontal cortex:a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry. 1998;55:215–224. doi: 10.1001/archpsyc.55.3.2154Rajkowska G, Selemon LD, Goldman-Rakic PS. Neuronal and glial somal size in the prefrontal cortex:a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry. 1998;55:215–224. doi: 10.1001/archpsyc.55.3.2154Pierri JN, Volk CLE, Auh S, Sampson A, Lewis DA. Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry. 2001;58:466–473. doi: 10.1001/archpsyc.58.5.466Pierri JN, Volk CLE, Auh S, Sampson A, Lewis DA. Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry. 2001;58:466–473. doi: 10.1001/archpsyc.58.5.466Garey LJ, Ong WY, Patel TS, Kanani M, Davis A, Mortimer AM, Barnes TR, Hirsch SR. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry. 1998;65(4):446–453. doi: 10.1136/jnnp.65.4.446Garey LJ, Ong WY, Patel TS, Kanani M, Davis A, Mortimer AM, Barnes TR, Hirsch SR. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry. 1998;65(4):446–453. doi: 10.1136/jnnp.65.4.446Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry. 2000;57(1):65–73. doi: 10.1001/archpsyc.57.1.65Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry. 2000;57(1):65–73. doi: 10.1001/archpsyc.57.1.65Black JE, Kodish IM, Grossman AW, Klintsova AY, Orlovskaya D, Vostrikov V, Uranova N, Greenough WT. Pathology of layer V pyramidal neurons in the prefrontal cortex of patients with schizophrenia. Am J Psychiatry. 2004;161:742–744. doi: 10.1176/appi.ajp.161.4.742Black JE, Kodish IM, Grossman AW, Klintsova AY, Orlovskaya D, Vostrikov V, Uranova N, Greenough WT. Pathology of layer V pyramidal neurons in the prefrontal cortex of patients with schizophrenia. Am J Psychiatry. 2004;161:742–744. doi: 10.1176/appi.ajp.161.4.742Broadbelt K, Byne W, Jones LB. Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex. Schizophr Res. 2002;58(1):75–81. doi: 10.1016/s0920-9964(02)00201-3Broadbelt K, Byne W, Jones LB. Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex. Schizophr Res. 2002;58(1):75–81. doi: 10.1016/s0920-9964(02)00201-3Smiley JF, Konnova K, Bleiwas C. Cortical thickness, neuron density and size in the inferior parietal lobe in schizophrenia. Schizophr Res. 2012;136(1–3):43–50. doi: 10.1016/j.schres.2012.01.006Smiley JF, Konnova K, Bleiwas C. Cortical thickness, neuron density and size in the inferior parietal lobe in schizophrenia. Schizophr Res. 2012;136(1–3):43–50. doi: 10.1016/j.schres.2012.01.006Felleman DJ, Van Essen DC. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex. 1991;1(1):1–47. doi: 10.1093/cercor/1.1.1-aFelleman DJ, Van Essen DC. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex. 1991;1(1):1–47. doi: 10.1093/cercor/1.1.1-aSherman SM, Guillery RW. Distinct function for direct and transthalamic corticocortical connections. J Neurophysiol. 2016;106(3):1068–1077. doi: 10.1152/jn.00429.2011Sherman SM, Guillery RW. Distinct function for direct and transthalamic corticocortical connections. J Neurophysiol. 2016;106(3):1068–1077. doi: 10.1152/jn.00429.2011Hoftman GD, Datta D, Lewis DA. Layer 3 excitatory and inhibitory circuitry in the prefrontal cortex: Developmental trajectories and alterations in schizophrenia. Biol Psychiatry. 2017;81(10):862–873. doi: 10.1016/j.biopsych.2016.05.022 Epub 2016 Jun 4. PMID: 27455897Hoftman GD, Datta D, Lewis DA. Layer 3 excitatory and inhibitory circuitry in the prefrontal cortex: Developmental trajectories and alterations in schizophrenia. Biol Psychiatry. 2017;81(10):862–873. doi: 10.1016/j.biopsych.2016.05.022 Epub 2016 Jun 4. PMID: 27455897Xiao D, Zikopoulos B, Barbas H. Laminar and modular organization of prefrontal projections to multiple thalamic nuclei. Neuroscience. 2009;161:1067–1081. doi: 10.1016/j.neuroscience.2009.04.034Xiao D, Zikopoulos B, Barbas H. Laminar and modular organization of prefrontal projections to multiple thalamic nuclei. Neuroscience. 2009;161:1067–1081. doi: 10.1016/j.neuroscience.2009.04.034Keefe RS, Harvey PD. Cognitive impairment in schizophrenia. Handb Exp Pharmacol. 2012;(213):11–37. doi: 10.1007/978-3-642-25758-2_2Keefe RS, Harvey PD. Cognitive impairment in schizophrenia. Handb Exp Pharmacol. 2012;(213):11–37. doi: 10.1007/978-3-642-25758-2_2Giraldo-Chica M, Woodward ND. Review of thalamocortical resting-state fMRI studies in schizophrenia. Schizophr Res. 2017;180:58–63. doi: 10.1016/j.schres.2016.08.005Giraldo-Chica M, Woodward ND. Review of thalamocortical resting-state fMRI studies in schizophrenia. Schizophr Res. 2017;180:58–63. doi: 10.1016/j.schres.2016.08.005Chahine G, Richter A, Wolter S, Maldonado RG, Gruber O. Disruptions in the left frontoparietal network underlie resting state endophenotypic markers in schizophrenia. Hum Brain Mapp. 2017;38(4):1741–1750. doi: 10.1002/hbm.23477Chahine G, Richter A, Wolter S, Maldonado RG, Gruber O. Disruptions in the left frontoparietal network underlie resting state endophenotypic markers in schizophrenia. Hum Brain Mapp. 2017;38(4):1741–1750. doi: 10.1002/hbm.23477Liu X, Zhuo C, Qin W, Zhu J, Xu L, Xu Y, Yu C. Selective functional connectivity abnormality of the transition zone of the inferior parietal lobule in schizophrenia. Neuroimage Clin. 2016;11:789–795. doi: 10.1016/j.nicl.2016.05.021Liu X, Zhuo C, Qin W, Zhu J, Xu L, Xu Y, Yu C. Selective functional connectivity abnormality of the transition zone of the inferior parietal lobule in schizophrenia. Neuroimage Clin. 2016;11:789–795. doi: 10.1016/j.nicl.2016.05.021Chen M, Zhuo CJ, Ji F, Li GY, Ke XY. Brain function differences in drug-naive first-episode auditory verbal hallucination- schizophrenia patients with versus without insight. Chin Med J (Engl). 2019;132(18):2199–2205. doi: 10.1097/CM9.0000000000000419Chen M, Zhuo CJ, Ji F, Li GY, Ke XY. Brain function differences in drug-naive -rst-episode auditory verbal hallucination- schizophrenia patients with versus without insight. Chin Med J (Engl). 2019;132(18):2199–2205. doi: 10.1097/CM9.0000000000000419van Landeghem FK, Weiss T, von Deimling A. Expression of PACAP and glutamate transporter proteins in satellite oligodendrocytes of the human CNS. Regul Pept. 2007;142(1–2):52–59. doi: 10.1016/j.regpep.2007.01.008van Landeghem FK, Weiss T, von Deimling A. Expression of PACAP and glutamate transporter proteins in satellite oligodendrocytes of the human CNS. Regul Pept. 2007;142(1–2):52–59. doi: 10.1016/j.regpep.2007.01.008Kim S, Webster MJ. Integrative genome-wide association analysis of cytoarchitectural abnormalities in the prefrontal cortex of psychiatric disorders. Mol Psychiatry. 2011;4:452–461. doi: 10.1038/mp.2010.23Kim S, Webster MJ. Integrative genome-wide association analysis of cytoarchitectural abnormalities in the prefrontal cortex of psychiatric disorders. Mol Psychiatry. 2011;4:452–461. doi: 10.1038/mp.2010.23Price CJ. The anatomy of language: contributions from functional neuroimaging. J Anat. 2000;197:335–359. doi: 10.1046/j.1469-7580.2000.19730335.xPrice CJ. The anatomy of language: contributions from functional neuroimaging. J Anat. 2000;197:335–359. doi: 10.1046/j.1469-7580.2000.19730335.xBuckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA. Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer’s disease. J Neurosci. 2009;29:1860–1873. doi: 10.1523/JNEUROSCI.5062-08.2009Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA. Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer’s disease. J Neurosci. 2009;29:1860–1873. doi: 10.1523/JNEUROSCI.5062-08.2009Humphreys GF, Lambon Ralph MA. Fusion and fission of cognitive functions in the human parietal cortex. Cereb Cortex. 2014;25:3547–3560. doi: 10.1093cercor/bhu198Humphreys GF, Lambon Ralph MA. Fusion and -ssion of cognitive functions in the human parietal cortex. Cereb Cortex. 2014;25:3547–3560. doi: 10.1093cercor/bhu198Cunningham SI, Tomasi D, Volkow ND. Structural and functional connectivity of the precuneus and thalamus to the default mode network. Hum Brain Mapp. 2017;38(2):938–956. doi: 10.1002/hbm.23429Cunningham SI, Tomasi D, Volkow ND. Structural and functional connectivity of the precuneus and thalamus to the default mode network. Hum Brain Mapp. 2017;38(2):938–956. doi: 10.1002/hbm.23429Fang F, Zhang H, Zhang Y, Xu H, Huang Q, Adilijiang A, Wang J, Zhang Z, Zhang D, Tan Q, He J, Kong L, Liu Y, Li XM. Antipsychotics promote the differentiation of oligodendrocyte progenitor cells by regulating oligodendrocyte lineage transcription factors 1 and 2. Life Sci. 2013;93(12–14):429–434. doi: 10.1016/j.lfs.2013.08.004Fang F, Zhang H, Zhang Y, Xu H, Huang Q, Adilijiang A, Wang J, Zhang Z, Zhang D, Tan Q, He J, Kong L, Liu Y, Li XM. Antipsychotics promote the differentiation of oligodendrocyte progenitor cells by regulating oligodendrocyte lineage transcription factors 1 and 2. Life Sci. 2013;93(12–14):429–434. doi: 10.1016/j.lfs.2013.08.004Bi X, Zhang Y, Yan B, Fang S, He J, Zhang D, Zhang Z, Kong J, Tan Q, Li XM. Quetiapine prevents oligodendrocyte and myelin loss and promotes maturation of oligodendrocyte progenitors in the hippocampus of global cerebral ischemia mice. J Neurochem. 2012;123(1):14–20. doi: 10.1111/j.1471-4159.2012.07883.xBi X, Zhang Y, Yan B, Fang S, He J, Zhang D, Zhang Z, Kong J, Tan Q, Li XM. Quetiapine prevents oligodendrocyte and myelin loss and promotes maturation of oligodendrocyte progenitors in the hippocampus of global cerebral ischemia mice. J Neurochem. 2012;123(1):14–20. doi: 10.1111/j.1471-4159.2012.07883.x

The authors declare that there are no conflicts of interest present.