Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas: Clinical article

Journal of Neurosurgery

Volumn 109, Issue 4, 2008, Pages 593-604

  Chassagnon, Serge ^a,c   Minotti, Lorella ^a   Kremer, Stéphane ^b   Hoffmann, Dominique ^b   Kahane, Philippe ^a  

^a UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^b GRENOBLE UNIVERSITY HOSPITAL   (France)

^c CH de Saint Malo   (France)

Author keywords

Anterior cingulate cortex; Electrical stimulation; Intracranial recording; Supplementary motor area

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; CHILD; CINGULATE GYRUS; ELECTROENCEPHALOGRAPHY; ELECTROSTIMULATION; EPILEPSY; FEMALE; FRONTAL LOBE; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PREMOTOR CORTEX; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SOMATOSENSORY STIMULATION; X RAY; BRAIN MAPPING; ELECTRODE; EVOKED MUSCLE RESPONSE; FRONTAL LOBE EPILEPSY; HAND STRENGTH; HISTOLOGY; MIDDLE AGED; MOTOR CORTEX; PATHOPHYSIOLOGY; PATIENT MONITORING; PHYSIOLOGY; SOMATOSENSORY CORTEX; TREATMENT OUTCOME;

ADOLESCENT; ADULT; BRAIN MAPPING; CHILD; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; EPILEPSY, FRONTAL LOBE; EVOKED POTENTIALS, MOTOR; FEMALE; GYRUS CINGULI; HAND STRENGTH; HUMANS; MALE; MIDDLE AGED; MONITORING, INTRAOPERATIVE; MOTOR CORTEX; SOMATOSENSORY CORTEX; TREATMENT OUTCOME;

EID: 55949124492     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/JNS/2008/109/10/0593     Document Type: Article

References (57)

1. Akkal D, Bioulac B, Audin J, Burbaud P: Comparison of neuronal activity in the rostral supplementary and cingulate motor areas during a task with cognitive and motor demands. Eur J Neurosci 15:887-904, 2002 (Pubitemid 35463653)
2. Ball T, Schreiber A, Feige B, Wagner M, Lücking C, Kristeva-Feige R: The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage 10:682-694, 1999 (Pubitemid 30026762)
3. Bancaud J, Talairach J: Clinical semiology of frontal lobe seizures. Adv Neurol 57:3-58, 1992
4. Bancaud J, Talairach J, Geier S, Bonis A, Trottier S, Manrique M: Manifestations comportementales induites par la stimulation électrique du gyrus cingulaire antérieur chez l'homme. Rev Neurol 132:705-724, 1976 (Pubitemid 8102599)
5. Baumgartner C, Flint R, Tuxhorn I, Van Ness PC, Kosalko J, Olbrich A, et al: Supplementary motor area seizures: propagation pathways as studied with invasive recordings. Neurology 46:508-514, 1996 (Pubitemid 26081342)
6. Beurze SM, de Lange FP, Toni I, Medendorp WP: Integration of target and effector information in the human brain during reach planning. J Neurophysiol 97:188-199, 2007 (Pubitemid 46143349)
7. Braak H: A primitive gigantopyramidal field buried in the depth of the cingulate sulcus of the human brain. Brain Res 109:219-223, 1976
8. Brazdil M, Kuba R, Rektor I: Rostral cingulate motor area and paroxysmal alien hand syndrome. J Neurol Neurosurg Psychiatry 77:992-993, 2006 (Pubitemid 44174095)
9. Brodmann K: Beiträge zur histologischen Lokalisation der Grosshirnrinde. VI Mitteilung: Die Cortex-gleiderung des Menschen. Journal für Psychologie und Neurologie Psychol Neurol 10:231-246, 1908
10. Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, et al: Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc Natl Acad Sci U S A 99:523-528, 2002 (Pubitemid 34060394)
11. Cadoret G, Smith AM: Input-output properties of hand-related cells in the ventral cingulate cortex in the monkey. J Neurophysiol 73:2584-2590, 1995
12. Chainay H, Krainik A, Tanguy ML, Gerardin E, Le Bihan D, Lehericy S: Foot, face and hand representation in the human supplementary motor area. Neuroreport 15:765-769, 2004 (Pubitemid 38453454)
13. Chassagnon S, Minotti L, Kremer S, Vercueil L, Hoffmann D, Benabid AL, et al: Restricted frontomesial epileptogenic focus generating dyskinetic behavior and laughter. Epilepsia 44:859-863, 2003 (Pubitemid 36754015)
14. Chauvel PY, Rey M, Buser P, Bancaud J: What stimulation of the supplementary motor area in humans tells about its functional organization. Adv Neurol 70:199-209, 1996
15. Chung GH, Han YM, Jeong SH, Jack CR: Functional heterogeneity of the supplementary motor area. AJNR Am J Neuroradiol 26:1819-1823, 2005
16. Deecke L, Scheid P, Kornhuber H: Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements. Exp Brain Res 7:158-168, 1969
17. Deiber MP, Ibañez V, Sadato N, Hallett M: Cerebral structures participating in motor preparation in humans: a positron emission tomography study. J Neurophysiol 75:233-247, 1999
18. Diehl B, Dinner DS, Mohamed A, Najm I, Klem G, LaPresto E, et al: Evidence of cingulate motor representation in humans. Neurology 55:725-728, 2000
19. Dinner DS, Lüders HO: Human supplementary sensorimotor area. Electrical stimulation and movement-related potential studies. Adv Neurol 66:261-271, 1995
20. Dum RP, Strick PL: Motor areas in the frontal lobe of the primate. Physiol Behav 77:677-682, 2002
21. Dum RP, Strick PL: The origin of the corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11:667-689, 1991
22. 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 50:297-305, 2002 (Pubitemid 41672583)
23. Fried I, Katz A, McCarthy G, Sass K, Williamson P, Spencer SS, et al: Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 11:3656-3666, 1991
24. Grosbras MH, Lobel E, Van de Moortele PF, LeBihan D, Berthoz A: An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. Cereb Cortex 9:705-711, 1999 (Pubitemid 29514100)
25. Hoshi E, Tanji J: Differential roles of neuronal activity in the supplementary and presupplementary motor areas: from information retrieval to motor planning and execution. J Neurophysiol 92:3482-3499, 2004 (Pubitemid 38649777)
26. Kremer S, Chassagnon S, Hoffmann D, Benabid AL, Kahane P: The cingulate hidden hand. J Neurol Neurosurg Psychiatry 70:264-265, 2001 (Pubitemid 32127873)
27. Krolak-Salmon P, Henaff MA, Vighetto A, Bauchet F, Bertrand O, Mauguiere F: Experiencing and detecting happiness in humans: the role of the supplementary motor area. Ann Neurol 59:196-199, 2006 (Pubitemid 43042889)
28. Laplane D, Talairach J, Meninger V, Bancaud J, Orgogozo JM: Clinical consequences of cortectomies involving the supplementary motor area in man. J Neurol Sci 34:301-314, 1977 (Pubitemid 8230911)
29. Lesser RP, Luders HO, Klem G, Dinner DS, Hahn JF: Extraoperative cortical functional localization in patients with epilepsy. J Clin Neurophysiol 4:27-53, 1987 (Pubitemid 17115705)
30. Lim SH, Dinner DS, Pillay PK, Luders H, Morris HH, Klem G, et al: Functional anatomy of the human supplementary sensory motor area: results of extraoperative electrical stimulation. Electroencephalogr Clin Neurophysiol 91:179-193, 1994 (Pubitemid 24285312)
31. Lobel E, Kahane P, Leonards U, Grosbras M, Lehericy S, Le Bihan D, et al: Localization of human frontal eye fields: anatomical and functional findings of functional magnetic resonance imaging and intracerebral electrical stimulation. J Neurosurg 95:804-815, 2001 (Pubitemid 33043354)
32. Lüders HO, Lesser RP, Dinner DS, Morris HH, Wyllie E, Godoy J, et al: A negative motor response elicited by electri cal stimulation of the human frontal cortex. Adv Neurol 57:149-157, 1992
33. Lüders HO, Dinner DS, Morris HH, Wyllie E, Comair YG: Cortical electrical stimulation in humans. The negative motor areas. Adv Neurol 67:115-129, 1995
34. Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G: Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey. J Comp Neurol 311:463-482, 1991
35. 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 338:114-140, 1993 (Pubitemid 23337260)
36. Matelli M, Luppino G, Rizzolatti G: Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311:445-462, 1991
37. Mitz AR, Wise SP: The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping. J Neurosci 7:1010-1021, 1987
38. Nobili L, Francione S, Mai R, Tassi L, Cardinale F, Castana L, et al: Nocturnal frontal lobe epilepsy: intracerebral recordings of paroxysmal motor attacks with increasing complexity. Sleep 26:883-886, 2003 (Pubitemid 39610636)
39. Penfield W, Welch K: The supplementary motor area in the cerebral cortex of man. Trans Am Neurol Assoc 74:179-185, 1949
40. Penfield W, Welch K: The supplementary motor area of the cerebral cortex. A clinical and experimental study. Arch Neurol Psychiatry 66:289-317, 1951
41. Picard N, Strick PL: Motors areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342-353, 1996 (Pubitemid 26161547)
42. Rizzolatti G, Gentilucci M, Camarda R, Gallese V, Luppino G, Matelli M, et al: Neurons related to reaching-grasping arm movements in the rostral part of area 6 (area 6abeta). Exp Brain Res 82:337-350, 1990 (Pubitemid 20378092)
43. Roland PE, Zilles K: Functions and structures of the motor cortices in human. Curr Opin Neurobiol 6:773-781, 1996
44. Rosenow F, Luders H: Presurgical evaluation of epilepsy. Brain 124:1683-1700, 2001 (Pubitemid 32845431)
45. Shima K, Mushiake H, Saito N, Tanji J: Role for cells in the presupplementary motor area in updating motor plans. Proc Natl Acad Sci U S A 93:8694-8698, 1996 (Pubitemid 26269622)
46. Sperli F, Spinelli L, Pollo C, Seeck M: Contralateral smile and laughter, but no mirth, induced by electrical stimulation of the cingulate cortex. Epilepsia 47:440-443, 2006
47. Talairach J, Bancaud J: The supplementary motor area in man: anatomo-functional findings by stereoencephalography in epilepsy. Int J Neurol 5:330-347, 1966
48. Talairach J, Tournoux P (eds): Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging. Stuttgart: Thieme Medical Publishers, 1988, pp 1-122
49. Tanji J, Kurata K: Changing concepts of motor areas of the cerebral cortex. Brain Dev 11:374-377, 1989 (Pubitemid 20037101)
50. Turken AU, Swick D: Response selection in the human anterior cingulate cortex. Nat Neurosci 2:920-924, 1999
51. Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR: Human cingulate cortex: surfaces features, flat maps, and cytoarchitecture. J Comp Neurol 359:490-506, 1995
52. Vogt C, Vogt O: Allgemeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol 25:279-439, 1919
53. Vorobiev V, Rizzolati G, Matelli M, Luppino G: Parcellation of human mesial area 6: cytoarchitectonic evidence for three separate areas. Eur J Neurosci 10:2199-2203, 1998 (Pubitemid 28327367)
54. Wiesendanger M, Seguin JJ, Kunzle H: The supplementary motor area - a control system for posture? in Stein RB, Pearson KC, Smith RS, et al (eds): Control of Posture and Locomotion. New York: Plenum Press, 1973, pp 331-346
55. Williamson PD, Jobst BC: Frontal lobe epilepsy. Adv Neurol 84:215-242, 2000
56. Yamane F, Muragaki Y, Maruyama T, Okada Y, Iseki H, Ikeda A, et al: Preoperative mapping for patients with supplementary motor area epilepsy: multimodality brain mapping. Psychiatry Clin Neurosci 58:S16-S21, 2004 (Pubitemid 38859025)
57. Zilles K, Schlaug G, Geyer S, Luppino G, Matelli M, Qü M, et al: Anatomy and transmitter receptors of the supplementary motor areas in the human and nonhuman primate brain. Adv Neurol 70:29-43, 1996