rentradВестник рентгенологии и радиологииJournal of radiology and nuclear medicine0042-46762619-0478Limited Liability Company "LUCHEVAYA DIAGNOSTIKA", Russian Association of Radiologists10.20862/0042-4676-2018-99-6-287-294rentrad-395Research ArticleОРИГИНАЛЬНЫЕ СТАТЬИORIGINAL RESEARCHВоксель-ориентированная морфометрия при боковом амиотрофическом склерозеVoxel-based morphometry in amyotrophic lateral sclerosishttps://orcid.org/0000-0003-0716-3737БакулинИ. С.BakulinI. S.

Бакулин Илья Сергеевич - младший научный сотрудник.

Волоколамское ш., 80, Москва, 125367

Il’ya S. Bakulin - Junior Researcher.

Volokolamskoe shosse, 80, Moscow, 125367

bakulin@neurology.ruhttps://orcid.org/0000-0001-5539-245XКоноваловР. Н.KonovalovR. N.

Кандидат медицинских наук, старший научный сотрудник.

Волоколамское ш., 80, Москва, 125367

Cand. Med. Sc., Senior Researcher.

Volokolamskoe shosse, 80, Moscow, 125367

https://orcid.org/0000-0003-3820-4554КротенковаМ. В.KrotenkovaM. V.

Доктор медицинских наук, руководитель отделения лучевой диагностики.

Волоколамское ш., 80, Москва, 125367

Dr. Med. Sc., Head of Radiology Department.

Volokolamskoe shosse, 80, Moscow, 125367

https://orcid.org/0000-0003-3956-6362СупоневаН. А.SuponevaN. A.

Доктор медицинских наук, руководитель отделения нейрореабилитации и физиотерапии.

Волоколамское ш., 80, Москва, 125367

Dr. Med. Sc., Head of Neurorehabilitation and Physiotherapy Department.

Volokolamskoe shosse, 80, Moscow, 125367

https://orcid.org/0000-0002-1072-9968ЗахароваМ. Н.ZakharovaM. N.

Доктор медицинских наук, профессор, руководитель VI неврологического отделения.

Волоколамское ш., 80, Москва, 125367

Dr. Med. Sc., Professor, Head of 6th Neurology Department.

Volokolamskoe shosse, 80, Moscow, 125367

ФГБНУ Научный центр неврологииРоссияResearch Center of NeurologyRussian Federation201802012019996287294Copyright © Бакулин И.С., Коновалов Р.Н., Кротенкова М.В., Супонева Н.А., Захарова М.Н., 20192019Бакулин И.С., Коновалов Р.Н., Кротенкова М.В., Супонева Н.А., Захарова М.Н.Bakulin I.S., Konovalov R.N., Krotenkova M.V., Suponeva N.A., Zakharova M.N.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.russianradiology.ru/jour/article/view/395

Цель исследования – изучить изменения объема серого вещества (СВ) головного мозга с помощью воксель-ориентированной морфометрии (ВОМ) у пациентов с классическим боковым амиотрофическим склерозом (БАС) и пациентов с синдромом изолированного поражения нижнего мотонейрона (СИПНМ).

Материал и методы

Материал и методы. В исследование были включены 30 пациентов с классическим БАС, 22 пациента с СИПНМ и23 сопоставимых по полу и возрасту здоровых добровольца. Всем участникам исследования проводилась МРТ головного мозга в режиме Т1-MPR (multiplanar reconstruction) с последующей обработкой (пространственная нормализация, сегментация и сглаживание). ВОМ использовалась для выявления различий в объеме СВ между группами.

Результаты

Результаты. У пациентов с классическим БАС при сравнении с группой контроля выявлено статистически значимое уменьшение объема СВ в средней части левых пре- и постцентральных извилин, средней части правой прецентральной извилины, правой и левой затылочной долях. У пациентов с СИПНМ при сравнении с группой контроля статистически значимых изменений объема серого вещества выявлено не было. При сравнении с пациентами с СИПНМ у пациентов с классическим БАС обнаружено статистически значимое уменьшение объема СВ в средней части левых пре- и постцентральных извилин, верхней части левой прецентральной извилины, средней и верхней частях правой прецентральной извилины, правой и левой затылочной долях. Статистически значимой корреляционной связи между объемом СВ и клиническими данными у пациентов с классическим БАС и СИПНМ отмечено не было.

Objective

Objective: to investigate changes in grey matter volume in patients with classical amyotrophic lateral sclerosis (ALS) and lower motor neuron syndrome (LMNS) with voxel-based morphometry (VBM).

Material and methods

Material and methods. 30 patients with classical ALS, 22 patients with LMNS and 23 age and gender matched healthy controls were enrolled in this study. All participants underwent a T1MPR (multiplanar reconstruction) magnetic resonance imaging with post-processing included spatial normalization, segmentation and smoothing. VBM was used to investigate changes in grey matter volume across the groups.

Results

Results. There was a significant decrease in grey matter volume of middle part of left pre- and postcentral gyri, middle part of right precentral gyrus, right and left occipital lobes in patients with classical ALS compared to healthy subjects. There was no difference in grey matter volume between patients with LMNS and healthy controls. Patients with classical ALS showed a significant decrease in grey matter volume of middle part of left preand postcentral gyri, upper part of left precentral gyrus, middle and upper parts of right precentral gyrus, right and left occipital lobes compared to patients with LMNS. There was no significant correlation between grey matter volume and clinical findings in patients with ALS and LMNS.

Conclusion

Conclusion. VBM reveals a decrease in grey matter volume of motor and nonmotor brain regions in patients with classical ALS, but not in patients with LMNS.

боковой амиотрофический склерозболезнь двигательного нейронамагнитно-резонансная томографиянейровизуализациявоксель-ориентированная морфометриябиомаркерыamyotrophic lateral sclerosismotor neuron diseasemagnetic resonance imagingneuroimagingvoxel-based morphometrybiomarkersReferencesVan Es M.A., Hardiman O., Chio A., Al-Chalabi A., Pasterkamp R.J., Veldink J.H. et al. Amyotrophic lateral sclerosis. Lancet. 2017; 390 (10107): 2084–98. DOI: 10.1016/S0140-6736(17)31287-4Van Es M.A., Hardiman O., Chio A., Al-Chalabi A., Pasterkamp R.J., Veldink J.H. et al. Amyotrophic lateral sclerosis. Lancet. 2017; 390 (10107): 2084–98. DOI: 10.1016/S0140-6736(17)31287-4Brooks B.R., Miller R.G., Swash M., Munsat T.L. World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral. Scler. Other. Motor. Neuron. Disord. 2000; 1 (5); 293–9.Brooks B.R., Miller R.G., Swash M., Munsat T.L. World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral. Scler. Other. Motor. Neuron. Disord. 2000; 1 (5); 293–9.Huynh W., Simon N.G., Grosskreutz J., Turner M.R., Vucic S., Kiernan M.C. Assessment of the upper motor neuron in amyotrophic lateral sclerosis. Clin. Neurophysiol. 2016; 127 (7): 2643–60. DOI: 10.1016/j.clinph.2016.04.025Huynh W., Simon N.G., Grosskreutz J., Turner M.R., Vucic S., Kiernan M.C. Assessment of the upper motor neuron in amyotrophic lateral sclerosis. Clin. Neurophysiol. 2016; 127 (7): 2643–60. DOI: 10.1016/j.clinph.2016.04.025Бакулин И.С., Червяков А.В., Кремнева Е.И., Коновалов Р.Н., Захарова М.Н. Структурная и функциональная нейровизуализация при боковом амиотрофическом склерозе. Анналы клинической и экспериментальной неврологии. 2017; 11 (2): 72–82. DOI: 10.18454/ACEN.2017.2.11Бакулин И.С., Червяков А.В., Кремнева Е.И., Коновалов Р.Н., Захарова М.Н. Структурная и функциональная нейровизуализация при боковом амиотрофическом склерозе. Анналы клинической и экспериментальной неврологии. 2017; 11 (2): 72–82. DOI: 10.18454/ACEN.2017.2.11Chio` A., Calvo A., Moglia C., Mazzini L., Mora G., PARALS study group. Phenotypic heterogeneity of amyotrophic lateral sclerosis: a population based study. J. Neurol.Neurosurg. Psychiatry. 2011; 82 (7): 740–6. DOI: 10.1136/jnnp.2010.235952Chio` A., Calvo A., Moglia C., Mazzini L., Mora G., PARALS study group. Phenotypic heterogeneity of amyotrophic lateral sclerosis: a population based study. J. Neurol.Neurosurg. Psychiatry. 2011; 82 (7): 740–6. DOI: 10.1136/jnnp.2010.235952Swinnen B., Robberecht W. The phenotypic variability of amyotrophic lateral sclerosis. Nat. Rev. Neurol. 2014; 10 (11): 661–70. DOI: 10.1038/nrneurol.2014.184Swinnen B., Robberecht W. The phenotypic variability of amyotrophic lateral sclerosis. Nat. Rev. Neurol. 2014; 10 (11): 661–70. DOI: 10.1038/nrneurol.2014.184Бакулин И.С., Закройщикова И.В., Супонева Н.А., Захарова М.Н. Боковой амиотрофический склероз: клиническая гетерогенность и подходы к классификации. Нервно-мышечные болезни. 2017; 7 (3): 10–20. DOI: 10.17650/22228721-2017-7-3-10-20Бакулин И.С., Закройщикова И.В., Супонева Н.А., Захарова М.Н. Боковой амиотрофический склероз: клиническая гетерогенность и подходы к классификации. Нервно-мышечные болезни. 2017; 7 (3): 10–20. DOI: 10.17650/22228721-2017-7-3-10-20 DOI: 10.17650/2222-8721-20177-3-10-20]Turner M.R., Swash M. The expanding syndrome of amyotrophic lateral sclerosis: a clinical and molecular odyssey. J. Neurol. Neurosurg. Psychiatry. 2015; 86 (6): 667–73. DOI: 10.1136/jnnp-2014308946Turner M.R., Swash M. The expanding syndrome of amyotrophic lateral sclerosis: a clinical and molecular odyssey. J. Neurol. Neurosurg. Psychiatry. 2015; 86 (6): 667–73. DOI: 10.1136/jnnp-2014308946Chio` A., Pagani M., Agosta F., Calvo A., Cistaro A., Filippi M. Neuroimaging in amyotrophic lateral sclerosis: insights into structural and functional changes. Lancet Neurol. 2014; 13 (12): 1228–40. DOI: 10.1016/S14744422(14)70167-XChio` A., Pagani M., Agosta F., Calvo A., Cistaro A., Filippi M. Neuroimaging in amyotrophic lateral sclerosis: insights into structural and functional changes. Lancet Neurol. 2014; 13 (12): 1228–40. DOI: 10.1016/S14744422(14)70167-XPradat P.F., El Mendili M.M. Neuroimaging to investigate multisystem involvement and provide biomarkers in amyotrophic lateral sclerosis. Biomed. Res. Int. 2014; 2014: 467560. DOI: 10.1155/2014/467560Pradat P.F., El Mendili M.M. Neuroimaging to investigate multisystem involvement and provide biomarkers in amyotrophic lateral sclerosis. Biomed. Res. Int. 2014; 2014: 467560. DOI: 10.1155/2014/467560Пирадов М.А., Танашян М.М., Кротенкова М.В., Брюхов В.В., Кремнева Е.И., Коновалов Р.Н. Передовые технологии нейровизуализации. Анналы клинической и экспериментальной неврологии. 2015; 9 (4): 11–8.Пирадов М.А., Танашян М.М., Кротенкова М.В., Брюхов В.В., Кремнева Е.И., Коновалов Р.Н. Передовые технологии нейровизуализации. Анналы клинической и экспериментальной неврологии. 2015; 9 (4): 11–8.Whitwell J.L. Voxel-based morphometry: an automated technique for assessing structural changes in the brain. J. Neurosci. 2009; 29 (31): 9661–4. DOI: 10.1523/JNEUROSCI.2160-09.2009Whitwell J.L. Voxel-based morphometry: an automated technique for assessing structural changes in the brain. J. Neurosci. 2009; 29 (31): 9661–4. DOI: 10.1523/JNEUROSCI.2160-09.2009Chen Z., Ma L. Grey matter volume changes over the whole brain in amyotrophic lateral sclerosis: a voxel-wise meta-analysis of voxel based morphometry studies. Amyotroph. Lateral. Scler. 2010; 11 (6): 549–54. DOI: 10.3109/17482968.2010.516265Chen Z., Ma L. Grey matter volume changes over the whole brain in amyotrophic lateral sclerosis: a voxel-wise meta-analysis of voxel based morphometry studies. Amyotroph. Lateral. Scler. 2010; 11 (6): 549–54. DOI: 10.3109/17482968.2010.516265Sheng L., Ma H., Zhong J., Shang H., Shi H., Pan P. Motor and extramotor gray matter atrophy in amyotrophic lateral sclerosis: quantitative meta-analyses of voxel-based morphometry studies. Neurobiol. Aging. 2015; 36 (12): 3288–99. DOI: 10.1016/j.neurobiolaging.2015.08.018Sheng L., Ma H., Zhong J., Shang H., Shi H., Pan P. Motor and extramotor gray matter atrophy in amyotrophic lateral sclerosis: quantitative meta-analyses of voxel-based morphometry studies. Neurobiol. Aging. 2015; 36 (12): 3288–99. DOI: 10.1016/j.neurobiolaging.2015.08.018Shen D., Cui L., Fang J., Cui B., Li D., Tai H. Voxel-Wise Meta-Analysis of Gray Matter Changes in Amyotrophic Lateral Sclerosis. Front. Aging. Neurosci. 2016; 8: 64. DOI: 10.3389/fnagi.2016.00064Shen D., Cui L., Fang J., Cui B., Li D., Tai H. Voxel-Wise Meta-Analysis of Gray Matter Changes in Amyotrophic Lateral Sclerosis. Front. Aging. Neurosci. 2016; 8: 64. DOI: 10.3389/fnagi.2016.00064Schuster C., Kasper E., Machts J., Bittner D., Kaufmann J., BeneckeR. et al. Focal thinning of the motor cortex mirrors clinical features of amyotrophic lateral sclerosis and their phenotypes: a neuroimaging study. J. Neurol. 2013; 260 (11): 2856–64. DOI: 10.1007/s00415-013-7083-zSchuster C., Kasper E., Machts J., Bittner D., Kaufmann J., BeneckeR. et al. Focal thinning of the motor cortex mirrors clinical features of amyotrophic lateral sclerosis and their phenotypes: a neuroimaging study. J. Neurol. 2013; 260 (11): 2856–64. DOI: 10.1007/s00415-013-7083-zWalhout R., Westeneng H.J., Verstraete E., Hendrikse J., Veldink J.H., van den Heuvel M.P. et al. Cortical thickness in ALS: towards a marker for upper motor neuron involvement. J. Neurol. Neurosurg. Psychiatry. 2015; 86 (3): 288–94. DOI: 10.1136/jnnp-2013-306839Walhout R., Westeneng H.J., Verstraete E., Hendrikse J., Veldink J.H., van den Heuvel M.P. et al. Cortical thickness in ALS: towards a marker for upper motor neuron involvement. J. Neurol. Neurosurg. Psychiatry. 2015; 86 (3): 288–94. DOI: 10.1136/jnnp-2013-306839Spinelli E.G., Agosta F., Ferraro P.M., Riva N., Lunetta C., Falzone Y.M. et al. Brain MR imaging in patients with lower motor neuron-predominant disease. Radiology. 2016; 280 (2): 545–56. DOI: 10.1148/radiol.2016151846Spinelli E.G., Agosta F., Ferraro P.M., Riva N., Lunetta C., Falzone Y.M. et al. Brain MR imaging in patients with lower motor neuron-predominant disease. Radiology. 2016; 280 (2): 545–56. DOI: 10.1148/radiol.2016151846Cedarbaum J.M., Stambler N., Malta E., Fuller C., Hilt D., Thurmond B., Nakanishi A. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J. Neurol. Sci. 1999; 169 (1–2): 13–21.Cedarbaum J.M., Stambler N., Malta E., Fuller C., Hilt D., Thurmond B., Nakanishi A. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J. Neurol. Sci. 1999; 169 (1–2): 13–21.Filippini N., Douaud G., MackayC.E., Knight S., Talbot K., Turner M.R. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology. 2010; 75 (18): 1645–52. DOI: 10.1212/WNL.0b013e3181fb84d1Filippini N., Douaud G., MackayC.E., Knight S., Talbot K., Turner M.R. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology. 2010; 75 (18): 1645–52. DOI: 10.1212/WNL.0b013e3181fb84d1Cosottini M., Pesaresi I., Piazza S., Diciotti S., Cecchi P., Fabbri S. et al. Structural and functional evaluation of cortical motor areas in Amyotrophic Lateral Sclerosis. Exp. Neurol. 2012; 234 (1): 169–80. DOI: 10.1016/j.expneurol.2011Cosottini M., Pesaresi I., Piazza S., Diciotti S., Cecchi P., Fabbri S. et al. Structural and functional evaluation of cortical motor areas in Amyotrophic Lateral Sclerosis. Exp. Neurol. 2012; 234 (1): 169–80. DOI: 10.1016/j.expneurol.2011Kwan J.Y., Meoded A., Danielian L.E., Wu T., Floeter M.K. Structural imaging differences and longitudinal changes in primary lateral sclerosis and amyotrophic lateral sclerosis. Neuroimage Clin. 2012; 2: 151–60. DOI: 10.1016/j.nicl.2012.12.003Kwan J.Y., Meoded A., Danielian L.E., Wu T., Floeter M.K. Structural imaging differences and longitudinal changes in primary lateral sclerosis and amyotrophic lateral sclerosis. Neuroimage Clin. 2012; 2: 151–60. DOI: 10.1016/j.nicl.2012.12.003Grosskreutz J., Kaufmann J., Frädrich J., Dengler R., Heinze H.J., Peschel T. Widespread sensorimotor and frontal cortical atrophy in amyotrophic lateral sclerosis. BMC Neurol. 2006; 25: 6–17. DOI: 10.1186/1471-2377-6-17Grosskreutz J., Kaufmann J., Frädrich J., Dengler R., Heinze H.J., Peschel T. Widespread sensorimotor and frontal cortical atrophy in amyotrophic lateral sclerosis. BMC Neurol. 2006; 25: 6–17. DOI: 10.1186/1471-2377-6-17Xiong J., Parsons L.M., Gao J.H., Fox P.T. Interregional connectivity to primary motor cortex revealed using MRI resting states images. Hum. Brain. Mapp. 1999; 8 (2–3): 151–6.Xiong J., Parsons L.M., Gao J.H., Fox P.T. Interregional connectivity to primary motor cortex revealed using MRI resting states images. Hum. Brain. Mapp. 1999; 8 (2–3): 151–6.Zhou F., Xu R., Dowd E., Zang Y., Gong H., Wang Z. Alterations in regional functional coherence within the sensory-motor network in amyotrophic lateral sclerosis. Neurosci Lett. 2014; 558: 192–6. DOI: 10.1016/j.neulet.2013.11.022Zhou F., Xu R., Dowd E., Zang Y., Gong H., Wang Z. Alterations in regional functional coherence within the sensory-motor network in amyotrophic lateral sclerosis. Neurosci Lett. 2014; 558: 192–6. DOI: 10.1016/j.neulet.2013.11.022Schieber M.H. Comparative anatomy and physiology of the corticospinal system. Handb. Clin. Neurol. 2007; 82: 15–37. DOI: 10.1016/S0072-9752(07)80005-4Schieber M.H. Comparative anatomy and physiology of the corticospinal system. Handb. Clin. Neurol. 2007; 82: 15–37. DOI: 10.1016/S0072-9752(07)80005-4Menon P., Geevasinga N., van den Bos M., Yiannikas C., Kiernan M.C., Vucic S. Cortical hyperexcitability and disease spread in amyotrophic lateral sclerosis. Eur. J. Neurol. 2017; 24 (6): 816–24. DOI: 10.1111/ene.13295Menon P., Geevasinga N., van den Bos M., Yiannikas C., Kiernan M.C., Vucic S. Cortical hyperexcitability and disease spread in amyotrophic lateral sclerosis. Eur. J. Neurol. 2017; 24 (6): 816–24. DOI: 10.1111/ene.13295Ravits J., Paul P., Jorg C. Focality of upper and lower motor neuron degeneration at the clinical onset of ALS. Neurology. 2007; 68 (19): 1571–5.Ravits J., Paul P., Jorg C. Focality of upper and lower motor neuron degeneration at the clinical onset of ALS. Neurology. 2007; 68 (19): 1571–5.Riku Y., Atsuta N., Yoshida M., Tatsumi S., Iwasaki Y., Mimuro M. et al. Differential motor neuron involvement in progressive muscular atrophy: a comparative study with amyotrophic lateral sclerosis. BMJ Open. 2014; 4 (5): e005213. DOI: 10.1136/bmjopen-2014-005213Riku Y., Atsuta N., Yoshida M., Tatsumi S., Iwasaki Y., Mimuro M. et al. Differential motor neuron involvement in progressive muscular atrophy: a comparative study with amyotrophic lateral sclerosis. BMJ Open. 2014; 4 (5): e005213. DOI: 10.1136/bmjopen-2014-005213Menon P., Kiernan M.C., Vucic S. Cortical hyperexcitability precedes lower motor neuron dysfunction in ALS. Clin. Neurophysiol. 2015; 126 (4): 803–9. DOI: 10.1016/j.clinph.2014.04.023Menon P., Kiernan M.C., Vucic S. Cortical hyperexcitability precedes lower motor neuron dysfunction in ALS. Clin. Neurophysiol. 2015; 126 (4): 803–9. DOI: 10.1016/j.clinph.2014.04.023Bede P., Bokde A., Elamin M., Byrne S., McLaughlin R.L., Jordan N. et al. Grey matter correlates of clinical variables in amyotrophic lateral sclerosis (ALS): a neuroimaging study of ALS motor phenotype heterogeneity and cortical focality. J. Neurol. Neurosurg. Psychiatry. 2013; 84 (7): 766–73. DOI: 10.1136/jnnp-2012302674Bede P., Bokde A., Elamin M., Byrne S., McLaughlin R.L., Jordan N. et al. Grey matter correlates of clinical variables in amyotrophic lateral sclerosis (ALS): a neuroimaging study of ALS motor phenotype heterogeneity and cortical focality. J. Neurol. Neurosurg. Psychiatry. 2013; 84 (7): 766–73. DOI: 10.1136/jnnp-2012302674Agosta F., ValsasinaP., Riva N., Copetti M.,Messina M.J., Prelle A. et al. The cortical signature of amyotrophic lateral sclerosis. PLoS One. 2012; 7 (8): e42816. DOI: 10.1371/journal.pone.0042816Agosta F., ValsasinaP., Riva N., Copetti M.,Messina M.J., Prelle A. et al. The cortical signature of amyotrophic lateral sclerosis. PLoS One. 2012; 7 (8): e42816. DOI: 10.1371/journal.pone.0042816Pagani M., Chio A., Valentini M.C., Oberg J., Nobili F., Calvo A. et al. Functional pattern of brain FDGPET in amyotrophic lateral sclerosis. Neurology. 2014; 83 (12): 1067–74. DOI: 10.1212/WNL.0000000000000792Pagani M., Chio A., Valentini M.C., Oberg J., Nobili F., Calvo A. et al. Functional pattern of brain FDGPET in amyotrophic lateral sclerosis. Neurology. 2014; 83 (12): 1067–74. DOI: 10.1212/WNL.0000000000000792Lule D., Diekmann V., Muller H.P., Kassubek J., Ludolph A.C., Birbaumer N. Neuroimaging of multimodal sensory stimulation in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry. 2010; 81 (8): 899–906. DOI: 10.1136/jnnp.2009.192260Lule D., Diekmann V., Muller H.P., Kassubek J., Ludolph A.C., Birbaumer N. Neuroimaging of multimodal sensory stimulation in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry. 2010; 81 (8): 899–906. DOI: 10.1136/jnnp.2009.192260Münte T.F., Tröger M.C., Nusser I., Wieringa B.M., Johannes S., Matzke M. et al. Alteration of early components of the visual evoked potential in amyotrophic lateral sclerosis. J. Neurol. 1998; 245 (4): 206–10.Münte T.F., Tröger M.C., Nusser I., Wieringa B.M., Johannes S., Matzke M. et al. Alteration of early components of the visual evoked potential in amyotrophic lateral sclerosis. J. Neurol. 1998; 245 (4): 206–10.Loewe K., Machts J., Kaufmann J., Petri S., Heinze H.J., Borgelt C. etal. Widespread temporo-occipital lobe dysfunction in amyotrophic lateral sclerosis. Sci Rep. 2017; 7: 40252. DOI: 10.1038/srep40252Loewe K., Machts J., Kaufmann J., Petri S., Heinze H.J., Borgelt C. etal. Widespread temporo-occipital lobe dysfunction in amyotrophic lateral sclerosis. Sci Rep. 2017; 7: 40252. DOI: 10.1038/srep40252Kushner P.D., Stephenson D.T., Wright S. Reactive astrogliosis is widespread in the subcortical white matter of amyotrophic lateral sclerosis brain. J. Neuropathol. Exp. Neurol. 1991; 50 (3): 263–77.Kushner P.D., Stephenson D.T., Wright S. Reactive astrogliosis is widespread in the subcortical white matter of amyotrophic lateral sclerosis brain. J. Neuropathol. Exp. Neurol. 1991; 50 (3): 263–77.

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