Neurosurgery

doi: 10.25005/2074-0581-2023-25-1-94-107
SUPPLEMENTARY MOTOR AREA AND CLINICAL PICTURE OF ITS LESION

I.M. Alekseev, A.A. Zuev

Pirogov National Medical and Surgical Center, Moscow, Russian Federation

Methods: The supplementary motor area (SMA) is a cortical region, that is located on the medial surface of the frontal lobe entirely within the interhemispheric fissure between the primary motor cortex (PMC) and prefrontal cortex (PFC). This area is a heterogeneous region in its structure, as well as in its connections with other parts of the brain; on the basis of these differences, the pre-SMA and SMA-proper regions are distinguished in it. Numerous neural connections with other parts of the central nervous system (CNS) suggest the involvement of the SMA in many cognitive functions, and not only in higher motor ones, as previously was thought. In particular, in the dominant hemisphere, the SMA performs the speech function through the frontal oblique fascicle (FOF), a bundle of association fibers that connects the SMA with Broca's area. In the event of various pathologies affecting the SMA and after neurosurgical manipulations in this area, a variety of neurological disorders can occur both motor and verbal. With the damage of this cortical region in the dominant hemisphere, SMA syndrome (akinetic mutism) can occur. This paper provides a review of the anatomical, cytoarchitectonic, and functional features of the SMA, as well as a detailed description of the clinical picture of the lesion of this cortical region.

Keywords: Brain, supplementary motor area, SMA syndrome.

Download file:


References
  1. Brodmann K. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig, Germany: Barth; 1909. 324 p. https://doi.org/10.1097/00005053-191012000-00013
  2. Campbell AW. Histological studies on the localization of cerebral function. Cambridge, UK: University Press; 1905. 360 p. https://doi.org/10.5962/bhl. title.1903
  3. Penfield W. The supplementary motor area in the cerebral cortex of man. Arch F Psychiatr U Z Neur. 1950;185:670-4. https://doi.org/10.1007/BF00935517
  4. Penfield W, Welch K. The supplementary motor area of the cerebral cortex; a clinical and experimental study. AMA Arch Neurol Psychiatry. 1951;66(3):289- 317. https://doi.org/10.1001/archneurpsyc.1951.02320090038004
  5. Penfield W, Jasper H. Epilepsy and the functional anatomy of the human brain. Boston, USA: Little, Brown and Co.; 1954. https://doi.org/10.1126/ science.119.3097.645-b
  6. . Talairach J, Bancaud J. The supplementary motor area in man (Anatomofunctional findings by stereoelectroencephalography in epilepsy). International Journal of Neurology. 1966;5:330-47.
  7. . Erickson T, Woolsey C. Observations of the supplementary motor area of man. Transactions of the American Neurological Association. 1982;76:50-2.
  8. Murray E, Coulter J. Organization of corticospinal neurons in the monkey. Journal of Comparative Neurology. 1981;195:339-65. https://doi.org/10.1002/ cne.901950212
  9. Tanji J, Kurata K. Comparison of movement-related activity in two cortical motor areas of primates. Journal of Neurophysiology. 1982;48:633-53. https:// doi.org/10.1152/jn.1982.48.3.633
  10. . Deecke L, Kornhuber H. An electrical sign of participation of the mesial "supplementary" motor area in human voluntary finger movement. Brain Resear. 1978;159:473-6. https://doi.org/10.1016/0006-8993(78)90561-9
  11. Orgogozo J, Larsen B, Roland P. Activation de I'aire motrice supplementaire au cours des mouvements volontaire chez 1'homme: Etudes par le dibit sanguin cerebral focal. Revue Neurologique. 1979;135:705-17.
  12. Laplane D, Talairach J, Meininger V, Bancaud J, Orgogozo J. Clinical consequences of corticectomies involving the supplementary motor area in man. Journal of Neurological Sciences. 1977;34:310-4. https://doi.org/10.1016/0022- 510x(77)90148-4
  13. . Ford A, McGregor K, Case K, Crosson B, White K. Structural connectivity of Broca's area and medial frontal cortex. Neuroimage. 2010;52(4):1230-7. https://doi.org/10.1016/j.neuroimage.2010.05.018
  14. Vergani F, Lacerda L, Martino J, Attems J, Morris C, Mitchell P, et al. White matter connections of the supplementary motor area in humans. J Neurol Neurosurg Psychiatry. 2014;85(12):1377-85. https://doi.org/10.1136/jnnp2013-307492
  15. Nachev P, Kennard C, Husain M. Functional role of the supplementary and presupplementary motor areas. Nat Rev Neurosci. 2008;9:856-69. https://doi. org/10.1038/nrn2478
  16. Ruan J, Bludau S, Palomero‑Gallagher N, Caspers S, Mohlberg H, Eickhoff S, et al. Cytoarchitecture, probability maps, and functions of the human supplementary and pre-supplementary motor areas. Brain Structure and Function. 2018;223:4169-86. https://doi.org/10.1007/s00429-018-1738-6
  17. Matsuzaka Y, Aizawa H, Tanji J. A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: Neuronal activity during a learned motor task. J Neurophysiol. 1992;68:653-62. https://doi. org/10.1152/jn.1992.68.3.653
  18. Zilles K, Schlaug G, Matelli M, Luppino G, Schleicher A, Dabringhaus A, et al. Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. J Anat. 1995;187(Pt 3):515-37.
  19. Picard N, Strick P. Imaging the premotor areas. Curr Opin Neurobiol. 2001;11:663-72. https://doi.org/10.1016/s0959-4388(01)00266-5
  20. . Inase M, Tokuno H, Nambu A, Akazawa T, Takada M. Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: Comparison with the input zones from the supplementary motor area. Brain Res. 1998;833:191-201. https://doi.org/10.1016/s0006- 8993(99)01531-0
  21. Luppino G, Matelli M, Camarda R, Rizzolatti G. Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol. 1993;338:114-40. https://doi.org/10.1002/cne.903380109
  22. Tehovnik E, Sommer M, Chou I, Slocum W, Schiller P. Eye fields in the frontal lobes of primates. Brain Res. 2000;Rev.32:413-48. https://doi.org/10.1016/ s0165-0173(99)00092-2
  23. Geyer S, Matelli M, Luppino G, Schleicher A, Jansen Y, Palomero-Gallagher N, et al. Receptor autoradiographic mapping of the mesial motor and premotor cortex of the macaque monkey. J Comp Neurol. 1998;397:231- 50. https://doi.org/10.1002/(sici)1096-9861(19980727)397:2%3C231::aidcne6%3E3.0.co;2-1
  24. Fujii N, Mushiake H, Tanji J. Distribution of eye and arm-movement-related neuronal activity in the SEF and in the SMA and Pre-SMA of monkeys. Neurophysiol. 2002;87:2158-66. https://doi.org/10.1152/jn.00867.2001
  25. . Picard N, Strick P. Motor areas of the medial wall: A review of their location and functional activation. Cereb Cortex. 1996;6:342-53. https://doi.org/10.1093/ cercor/6.3.342
  26. Potgieser A, de Jong B, Wagemakers M, Hoving E, Groen R. Insights from the supplementary motor area syndrome in balancing movement initiation and inhibition. Front Hum Neurosci. 2014;8:960. https://doi.org/10.3389/ fnhum.2014.00960
  27. Akkal D, Dum R, Strick P. Supplementary motor area and presupplementary motor area: Targets of basal ganglia and cerebellar output. J Neurosci. 2007;27(40):10659-73. https://doi.org/10.1523/JNEUROSCI.3134-07.2007
  28. Kandel ER. Essentials of neural science and behavior. NY, USA: McGraw-Hill; 2007.
  29. Schmahmann J, Pandya D. Fiber Pathways of the Brain. Oxford, UK: Oxford University Press; 2009. 654 p
  30. Kim J, Lee J, Jo H, Kim S, Lee J, Kim S, et. al. Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: Functional connectivity based parcellation method. Neuroimage. 2010;49:2375-86. https://doi.org/10.1016/j.neuroimage.2009.10.016
  31. Heiferman D, Ackerman P, Hayward D, Primeau M, Anderson D, Prabhu V. Bilateral supplementary motor area syndrome causing akinetic mutism following parasagittal meningioma resection. Neuroscience Discovery. 2014;2(1):7. https://doi.org/10.7243/2052-6946-2-7
  32. . Fernandez-Miranda J, Rhoton A, Kakizawa Y, Choi C, Alvarez-Linera J. The claustrum and its projection system in the human brain: A microsurgical and tractographic anatomical study. J Neurosurg. 2008;108(4):764-74. https://doi. org/10.3171/jns/2008/108/4/0764
  33. Kinoshita M, de Champfleur N, Deverdun J, Moritz-Gasser S, Herbet G, Duffau H. Role of fronto-striatal tract and frontal aslant tract in movement and speech: An axonal mapping study. Brain Struct Funct. 2015;220(6):3399-412. https:// doi.org/10.1007/s00429-014-0863-0
  34. Bozkurt B, Yagmurlu K, Middlebrooks E, Karadag A, Ovalioglu T, Jagadeesan B. The Microsurgical and tractographic anatomy of the supplementary motor area complex in human. World Neurosurgery. 2016;95:99-107. https://doi. org/10.1016/j.wneu.2016.07.072
  35. Yagmurlu K, Middlebrooks E, Tanriover N, Rhoton A. Fiber tracts of the dorsal language stream in the human brain. Journal of Neurosurgery. 2015;124(5):1396-405. https://doi.org/10.3171/2015.5.jns15455
  36. Zhang S, Ide J, Li C. Resting-state functional connectivity of the medial superior frontal cortex. Cerebral Cortex. 2012;22:99-111. https://doi.org/10.1093/ cercor/bhr088
  37. Xue G, Lu Z, Levin I, Bechara A. The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage. 2010;50:709-16. https://doi.org/10.1016/j.neuroimage.2009.12.097
  38. Frank M, Samanta J, Moustafa A, Sherman S. Hold your horses: Impulsivity, deep brain stimulation, and medication in parkinsonism. Science. 2007;318:1309- 312. https://doi.org/10.1126/science.1146157
  39. Wise S. Corticospinal efferents of the supplementary sensorimotor area in relation to the primary motor area. Adv Neurol. 1996;70:57-69.
  40. Grogan A, Green D, Ali N, Crinion J, Price C. Structural correlates of semantic and phonemic fluency ability in first and second languages. Cerebr Cortex. 2019;19(11):2690-8. https://doi.org/10.1093/cercor/bhp023
  41. Sjöberg R, Stålnackea M, Andersson M, Eriksson J. The supplementary motor area syndrome and cognitive control. Neuropsychologia. 2019;129:141-5. https://doi.org/10.1016/j.neuropsychologia.2019.03.013
  42. Thiebaut de Schotten M, Dell'Acqua F, Valabregue R, Catani M. Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex. 2012;48:82-96. https://doi.org/10.1016/j.cortex.2011.10.001
  43. Dick A, Bernal B, Tremblay P. The language connectome: New pathways, new concepts. Neuroscientist. 2014;20:453-67. https://doi. org/10.1177/1073858413513502
  44. Vassal F, Boutet C, Lemaire J, Nuti C. New insights into the functional significance of the frontal aslant tract – an anatomo-functional study using intraoperative electrical stimulations combined with diffusion tensor imagingbased fiber tracking. British Journal of Neurosurgery. 2014;28:685-7. https:// doi.org/10.3109/02688697.2014.889810
  45. Kinoshita M, Shinohara H, Hori O, Ozaki N, Ueda F, Nakada M, et al. Association fibers connecting the Broca center and the lateral superior frontal gyrus: A microsurgical and tractographic anatomy. J Neurosurg. 2012;116(2):323-30. https://doi.org/10.3171/2011.10.JNS11434
  46. Catani M, Mesulam M, Jakobsen E, Malik F, Martersteck A, Wieneke C, et al. A novel frontal pathway underlies verbal fluency in primary progressive aphasia. Brain. 2013;136(Pt8):2619-28. https://doi.org/10.1093/brain/awt163
  47. Catani M, Dell'acqua F, Vergani F, Malik F, Hodge H, Roy P, et al. Short frontal lobe connections of the human brain. Cortex. 2012;48(2):273-91. https://doi. org/10.1016/j.cortex.2011.12.001
  48. Narayana S, Laird A, Tandon N, Franklin C, Lancaster J, Fox P. Electrophysiological and functional connectivity of the human supplementary motor area. NeuroImage. 2012;62:250-65. https://doi.org/10.1016/j.neuroimage.2012.04.060
  49. . Vergara J, Rivera N, Rossi-Pool R, Romo R. A neural parametric code for storing information of more than one sensory modality in working memory. Neuron. 2016;89:54-62. https://doi.org/10.1016/j.neuron.2015.11.026
  50. Tanji J. Sequential organization of multiple movements: Involvement of cortical motor areas. Annu Rev Neurosci. 2001;24:631-51. https://doi.org/10.1146/ annurev.neuro.24.1.631
  51. Shima K, Tanji J. Neuronal activity in the supplementary and presupplementary motor areas for temporal organization of multiple movements. J Neurophysiol. 2000;84:2148-60. https://doi.org/10.1152/jn.2000.84.4.2148
  52. Wymbs N, Grafton S. Contributions from the left PMd and the SMA during sequence retrieval as determined by depth of training. Exp Brain Res. 2013;224(1):49-58. https://doi.org/10.1007/s00221-012-3287-1
  53. Klein P, Duque J, Labruna L, Ivry R. Comparison of the two cerebral hemispheres in inhibitory processes operative during movement preparation. NeuroImage. 2016;125:220-32. https://doi.org/10.1016/j.neuroimage.2015.10.007
  54. Jahanshahi M, Jenkins H, Brown R, Marsden D, Passingham R, Brooks D. Selfinitiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain. 1995;118:913-33. https://doi.org/10.1093/brain/118.4.913
  55. Grezes J, Decety J. Does visual perception of object afford action? Evidence from a neuroimaging study. Neuropsychologia. 2002;40:212-22. https://doi. org/10.1016/s0028-3932(01)00089-6
  56. Tanji J, Shima K. Role for supplementary motor area cells in planning several movements ahead. Nature. 1994;371:413-16. https://doi. org/10.1038/371413a0
  57. Shima K, Mushiake H, Saito N, Tanji J. Role for cells in the presupplementary motor area in updating motor plans. Proc Natl Acad. Sci. 1996;93:8694-98. https://doi.org/10.1073/pnas.93.16.8694
  58. Isoda M, Tanji J. Participation of the primate presupplementary motor area in sequencing multiple saccades. J Neurophysiol. 2004;92:653-5. https://doi. org/10.1152/jn.01201.2003
  59. . Hikosaka O, Sakai K, Miyauchi S, Takino R, Sasaki Y, Putz B. Activation of human presupplementary motor area in learning of sequential procedures: A functional MRI study. J Neurophysiol. 1996;76(1):617-21. https://doi. org/10.1152/jn.1996.76.1.617
  60. Nakamura K, Sakai K, Hikosaka O. Neuronal activity in medial frontal cortex during learning of sequential procedures. J Neurophysiol. 1998;80(5):2671-87. https://doi.org/10.1152/jn.1998.80.5.2671
  61. Halsband U, Lange R. Motor learning in man: A review of functional and clinical studies. J Physiol Paris. 2006;99(4-6):414-24. https://doi.org/10.1016/j. jphysparis.2006.03.007.
  62. Nachev P, Wydell H, O’Neill K, Husain M, Kennard C. The role of the pre-supplementary motor area in the control of action. Neuroimage. 2007;36:T155-T163. https://doi.org/10.1016/j.neuroimage.2007.03.034
  63. Coull J, Cheng R, Meck W. Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology. 2011;36:3-25. https://doi.org/10.1038/ npp.2010.113
  64. Coull J, Charras P, Donadieu M, Droit-Volet S, Vidal F. Sma selectively codes the active accumulation of temporal, not spatial, magnitude. J Cogn Neurosci. 2015;27(11):2281-98. https://doi.org/10.1162/jocn_a_00854
  65. Coull J, Vidal F, Burle B. When to act, or not to act: That’s the SMA’s question. Curr Opin Neurobiol. 2016;8:1-8. https://doi.org/10.1016/j.cobeha.2016.01.003
  66. Wiener M, Turkeltaub P, Coslett H. The image of time: A voxel-wise metaanalysis. Neuroimage. 2010;49(2);1728-40. https://doi.org/10.1016/j. neuroimage.2009.09.064
  67. Schwartze M, Rothermich K, Kotz S. Functional dissociation of pre-SMA and SMA-proper in temporal processing. Neuroimage. 2012;60(1):290-8. https:// doi.org/10.1016/j.neuroimage.2011.11.089
  68. Zacks J. Neuroimaging studies of mental rotation: A meta-analysis and review. Journal of Cognitive Neuroscience. 2008;20(1):1-19. https://doi.org/10.1162/ jocn.2008.20013
  69. Wood G, Nuerk H, Moeller K, Geppert B, Schnitker R, Weber J, et al. All for one but not one for all: How multiple number representations are recruited in one numerical task. Brain Res. 2008;1187(1):154-66. https://doi.org/10.1016/j. brainres.2007.09.094
  70. Fehr T, Code C, Herrmann M. Common brain regions underlying different arithmetic operations as revealed by conjunct fMRI-BOLD activation. Brain Res. 2007;1172(1):93-102. https://doi.org/10.1016/j.brainres.2007.07.043
  71. Fehr T. A hybrid model for the neural representation of complex mental processing in the human brain. Cognit Neurodyn. 2013;7(2):89-103. https:// doi.org/10.1007/s11571-012-9220-2
  72. Tsai C, Chen C, Chou T, Chen J. Neural mechanisms involved in the oral representation of percussion music: An fMRI study. Brain Cogn. 2010;74(2):123- 31. https://doi.org/10.1016/j.bandc.2010.07.008
  73. Donnay G, Rankin S, Lopez-Gonzalez M, Jiradejvong P, Limb C. Neural substrates of interactive musical improvisation: An fMRI study of ‘‘trading fours” in jazz. PLoS One. 2014;3:e88665. https://doi.org/10.1371/journal.pone.0088665
  74. Meister I, Krings T, Foltys H, Boroojerdi B, Muller M, Topper R, et al. Playing piano in the mind – an fMRI study on music imagery and performance in pianists. Cogn Brain Res. 2004;19(3):219-28. https://doi.org/10.1016/j. cogbrainres.2003.12.005
  75. Baumann S, Koeneke S, Schmidt C, Meyer M, Lutz K, Jancke L. A network for audio-motor coordination in skilled pianists and non-musicians. Brain Res. 2007;1161(1):65-78. https://doi.org/10.1016/j.brainres.2007.05.045
  76. Rottschy C, Langner R, Dogan I, Reetz K, Laird A, Schulz J, et al. Modelling neural correlates of working memory: A coordinate-based meta-analysis. Neuroimage. 2012;60(1):830-46. https://doi.org/10.1016/j.neuroimage.2011.11.050
  77. Langner R, Sternkopf M, Kellermann T, Grefkes C, Kurth F, Schneider F, et al. Translating working memory into action: Behavioral and neural evidence for using motor representations in encoding visuo-spatial sequences. Human Brain Mapping. 2014;35(7):3465-84. https://doi.org/10.1002/hbm.22415
  78. Bledowski C, Kadosh K, Wibral M, Rahm B, Bittner R, Hoechstetter K, et al. Mental chronometry of working memory retrieval: A combined functional magnetic resonance imaging and event-related potentials approach. J Neurosci. 2006;26(3):821-9. https://doi.org/10.1523/jneurosci.3542-05.2006
  79. Hertrich I, Dietrich S, Ackermann H. The role of the supplementary motor area for speech and language processing. Neuroscience & Biobehavioral Reviews. 2016;68:602-10. https://doi.org/10.1016/j.neubiorev.2016.06.030
  80. Brendel B, Hertrich I, Erb M, Lindner A, Riecker A, Grodd W. The contribution of mesiofrontal cortex to the preparation and execution of repetitive syllable productions: An fMRI study. NeuroImage. 2010;50:1219-30. https://doi. org/10.1016/j.neuroimage.2010.01.039
  81. Segaert K, Menenti L, Weber K, Petersson K, Hagoort P. Shared syntax in language production and language comprehension – An fMRI study. Cereb Cortex. 2012;22(7):1662-70. https://doi.org/10.1093/cercor/bhr249
  82. Conaa G, Semenzaa C. Supplementary motor area as key structure for domaingeneral sequence processing: A unified account. Neuroscience and Biobehavioral Reviews. 2017;72:28-42. https://doi.org/10.1016/j.neubiorev.2016.10.033
  83. Duffau H, Capelle L. Preferential brain locations of low-grade gliomas. Cancer. 2004;100:2622-6. https://doi.org/10.1002/cncr.20297
  84. Chassagnon S, Minotti L, Kremer S, Hoffmann D, Kahane P. Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas. J Neurosurg. 2008;109:593-604. https://doi. org/10.3171/JNS/2008/109/10/0593
  85. Mohebi N, Arab M, Moghaddasi M, Ghader B, Emamikhah M. Stroke in supplementary motor area mimicking functional disorder: A case report. J Neurol. 2019;266:2584-6. https://doi.org/10.1007/s00415-019-09479-7
  86. Minshew N, Keller T. The nature of brain dysfunction in autism: Functional brain imaging studies. Curr Opin Neurol. 2010;23:124-30. https://doi.org/10.1097/ wco.0b013e32833782d4
  87. Lu C, Peng D, Chen C, Ning N, Ding G, Li K, et al. Altered effective connectivity and anomalous anatomy in the basal gangliathalamocortical circuit of stuttering speakers. Cortex. 2010;46:49-67. https://doi.org/10.1016/j. cortex.2009.02.017
  88. Young J, Gogos A, Aabedi A, Morshed R, Pereira M, Lashof-Regas S, et al. Resection of supplementary motor area gliomas: Revisiting supplementary motor syndrome and the role of the frontal aslant tract. J Neurosurg. 2021;1-7. https://doi.org/10.3171/2021.4.JNS21187
  89. Kasasbeh A, Yarbrough K, Limbrick D, Steger-May K, Leach J, Mangano F, et al. Characterization of the supplementary motor area syndrome and seizure outcome after medial frontal lobe resections in pediatric epilepsy surgery. Neurosurgery. 2012;70:1152-68. https://doi.org/10.1227/neu.0b013e31823f6001
  90. Fontaine D, Capelle L, Duffau H. Somatotopy of the supplementary motor area: Evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery. 2002;50(2):297-303. https://doi. org/10.1227/00006123-200202000-00011
  91. Della Sala S, Francescani A, Spinnler H. Gait apraxia after bilateral supplementary motor area lesion. J Neurol Neurosurg Psychiatry. 2002;72:77-85. https://doi. org/10.1136/jnnp.72.1.77
  92. Feinberg T, Schindler R, Flanagan N, Haber L. Two alien hand syndromes. Neurology. 1992;42:19-24. https://doi.org/10.1212/wnl.42.1.19
  93. Boccardi E, Della Sala S, Motto C, Spinnler H. Utilisation behaviour consequent to bilateral SMA softening. Cortex. 2002;38:289-308. https://doi.org/10.1016/ s0010-9452(08)70661-0
  94. Ziegler W, Kilian B, Deger K. The role of the left mesial frontal cortex in fluent speech: Evidence from a case of left supplementary motor area hemorrhage. Neuropsychologia. 1997;35:1197-208. https://doi.org/10.1016/s0028- 3932(97)00040-7
  95. Mendez M. Aphemia-like syndrome from a right supplementary motor area lesion. Clinical Neurology and Neurosurgery. 2004;106:337-9. https://doi. org/10.1016/j.clineuro.2003.12.008
  96. Chainay H, Alario F, Krainik A, Duffau H, Capelle L, Volle E, et al. Motor and language deficits before and after surgical resection of mesial frontal tumour. Clinical Neurology and Neurosurgery. 2009;111:39-46. https://doi. org/10.1016/j.clineuro.2008.07.004
  97. Acioly MA, Cunha AM, Parise M, Rodrigues E, Tovar-Moll F. Recruitment of contralateral supplementary motor area in functional recovery following medial frontal lobe surgery: An fMRI case study. Journal of Neurological Surgery Part A – Central European Neurosurgery. 2015;76:508-12. https://doi. org/10.1055/s-0035-1558408
  98. Rubens A. Aphasia with infarction in the territory of the anterior cerebral artery. Cortex. 1975;11:239-50. https://doi.org/10.1016/s0010-9452(75)80006-2
  99. Ardila A, Lopez M. Transcortical motor aphasia: One or two aphasias? Brain and Language. 1984;22(2):350-3. https://doi.org/10.1016/0093-934x(84)90099-3
  100. Ardila A. A proposed reinterpretation and reclassification of aphasic syndromes. Aphasiology. 2010;24(3):363-94. https://doi. org/10.1080/02687030802553704
  101. Lahiri D, Dubey S, Ardila A, Sawale V, Roy B, Sen S, et al. Incidence and types of aphasia after first-ever acute stroke in Bengali speakers: Age, gender, and educational effect on the type of aphasia. Aphasiology. 2020;34:709-22. https://doi.org/10.1080/02687038.2019.1630597
  102. Ardila A. Supplementary motor area aphasia revisited. Journal of Neurolinguistics. 2020;54:100888. https://doi.org/10.1016/j.jneuroling.2020.100888
  103. Berthier M, Dávila G, Moreno-Torres I, Beltran-Corbellini A, Santana-Moreno D, Roe-Vellve N, et al. Loss of regional accent after damage to the speech production network. Frontiers in Human Neuroscience. 2015;9:610. https:// doi.org/10.3389/fnhum.2015.00610
  104. Kronfeld-Duenias V, Amir O, Ezrati-Vinacour R, Civier O, Ben-Shachar M. The frontal aslant tract underlies speech fluency in persistent developmental stuttering. Brain Structure and Function. 2016;221(1):365-81. https://doi. org/10.1007/s00429-014-0912-8
  105. Basilakos A, Fillmore P, Rorden C, Guo D, Bonilha L, Fridriksson J. Regional white matter damage predicts speech fluency in chronic post-stroke aphasia. Front Hum Neurosci. 2014;8:845. https://doi.org/10.3389/fnhum.2014.00845
  106. Cañas A, Juncadella M, Lau R, Gabarros A, Hernandez M. Working memory deficits after lesions involving the supplementary motor area. Front Psychol. 2018;9:765. https://doi.org/10.3389/fpsyg.2018.00765
  107. Wu S, Maloney T, Gilbert D, Dixon S, Horn P, Huddleston D, et al. Functional MRInavigated repetitive transcranial magnetic stimulation over supplementary motor area in chronic tic disorders. Brain Stimul. 2014;7:212-8. https://doi. org/10.1016/j.brs.2013.10.005
  108. D’Urso G, Brunoni A, Mazzaferro M, Anastasia A, Bartolomeis A, Mantovani A. Transcranial direct current stimulation for obsessive compulsive disorder: A randomized, controlled, partial crossover trial. Depress Anxiety. 2016;33:1132- 40. https://doi.org/10.1002/da.22578
  109. Shirota Y, Ohtsu H, Hamada M, Enomoto H, Ugawa Y. Supplementary motor area stimulation for Parkinson disease: A randomized controlled study. Neurology. 2013;80:1400-5. https://doi.org/10.1212/wnl.0b013e31828c2f66
  110. Grafton S. Contributions of functional imaging to understanding parkinsonian symptoms. Curr Opin Neurobiol. 2004;14:715-9. https://doi.org/10.1016/j. conb.2004.10.010
  111. Haslinger B, Erhard P, Kampfe N, Boecker H, Rummeny E, Schwaiger M, et al. Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain. 2001;124:558-70. https://doi.org/10.1093/ brain/124.3.558
  112. Grafton S, Turner R, Desmurget M, Bakay R, Delong M, Vitek J, et al. Normalizing motor-related brain activity: Subthalamic nucleus stimulation in Parkinson disease. Neurology. 2006;66:1192-9. https://doi.org/10.1212/01. wnl.0000214237.58321.c3
  113. MacDonald V, Halliday G. Selective loss of pyramidal neurons in the presupplementary motor cortex in Parkinson’s disease. Mov Disord. 2002;17:1166- 73. https://doi.org/10.1002/mds.10258
  114. Hamada M, Ugawa Y, Tsuji S. High-frequency rTMS over the supplementary motor area for treatment of Parkinson’s disease. Mov Disord. 2008;23:1524- 31. https://doi.org/10.1002/mds.22168
  115. Cerasa A, Koch G, Donzuso G, Mangone G, Morelli M, Brusa L, et al. A network centred on the inferior frontal cortex is critically involved in levodopa-induced dyskinesias. Brain. 2014;138:414-27. https://doi.org/10.1093/brain/awu329

Author information:


Alekseev Ivan Maksimovich,
Neurosurgeon, Postgraduate Student of the Department of Neurosurgery of the Institute for Postgraduate Medical Education, Pirogov National Medical and Surgical Center
ORCID ID: 0000-0001-8107-3065
E-mail: alexeev.im@yandex.ru

Zuev Andrey Aleksandrovich,
Doctor of Medical Sciences, Head of the Department of Neurosurgery of the Institute for Postgraduate Medical Education, Pirogov National Medical and Surgical Center
ORCID ID: 0000-0003-2974-1462
E-mail: mosbrain@gmail.com

Information about support in the form of grants, equipment, medications

The authors did not receive financial support from manufacturers of medicines and medical equipment

Conflicts of interest: No conflict

Address for correspondence:


Alekseev Ivan Maksimovich
Neurosurgeon, Postgraduate Student of the Department of Neurosurgery of the Institute for Postgraduate Medical Education, Pirogov National Medical and Surgical Center

105203, Russian Federation, Moscow, Nizhnyaya Pervomayskaya str., 70

Tel.: +7 (918) 5844004

E-mail: alexeev.im@yandex.ru

Materials on the topic: