Supplementary motor area

Some motor areas in the human cortex. The supplementary motor area is shown in pink. Image by: Paskari

The supplementary motor area (SMA) is a part of the primate cerebral cortex that contributes to the control of movement. It is located on the midline surface of the hemisphere just in front of (anterior to) the primary motor cortex leg representation. In monkeys the SMA contains a rough map of the body. In humans the body map is not apparent. Neurons in the SMA project directly to the spinal cord and may play a role in the direct control of movement. Possible functions attributed to the SMA include the postural stabilization of the body, the coordination of both sides of the body such as during bimanual action, the control of movements that are internally generated rather than triggered by sensory events, and the control of sequences of movements. All of these proposed functions remain hypotheses. The precise role of the SMA is not yet known and it may serve multiple roles.

For the discovery of the SMA and its relationship to other motor cortical areas, see the main article on the motor cortex.

Subregions

At least six areas are now recognized within the larger region once defined as the SMA. These subdivisions have been studied most extensively in the monkey brain. The most anterior portion is now commonly termed pre-SMA.[1][2][3] It has sparse or no connections to the spinal cord or the primary motor cortex and has extensive connectivity with prefrontal areas.[1][4][5][6][7]

The supplementary eye field (SEF) is a relatively anterior portion of the SMA that, when stimulated, evokes head and eye movements and perhaps movements of the limbs and torso.[8][9][10][11]

Dum and Strick[5] hypothesized on the basis of cytoarchitecture and connections to the spinal cord that the portion of SMA in the cingulate sulcus, on the medial part of the hemisphere, can be split into three separate areas, the cingulate motor areas. The functions of the cingulate motor areas have not yet been systematically studied.

SMA proper in monkeys has now been confined to a region on the crown of the hemisphere and extending partly onto the medial wall, just anterior to the primary motor leg representation. SMA proper projects directly to the spinal cord and therefore is one of the primary output areas of the cortical motor system.[5][12][13][14][15][16]

Recently, Zhang et al.[17] investigated the functional subdivisions of the medial SFC on the basis of whole-brain connectivity characterized from a large resting-state fMRI data set. Other than replicating the boundaries between SMA and preSMA, the current results support a functional difference between the posterior and anterior preSMA. In contrast to the posterior preSMA, the anterior preSMA is connected with most of the prefrontal but not somatomotor areas. Overall, the SMA is strongly connected to the thalamus and epithalamus, the posterior preSMA to putamen, pallidum, and STN and anterior preSMA to the caudate, with the caudate showing significant hemispheric asymmetry.

Functions

Penfield and Welch[18] in 1951 first described SMA in the monkey brain and the human brain as a representation of the body on the medial wall of the hemisphere. Woolsey and colleagues[19] in 1952 confirmed SMA in the monkey brain, describing it as a rough somatotopic map with the legs in a posterior location and the face in an anterior location. The representations of different body parts were found to overlap extensively. Stimulation of many sites evoked bilateral movements and sometimes movements of all four limbs. This overlapping somatotopic map in SMA was confirmed by many others.[2][13][20][21][22]

Four main hypotheses have been proposed for the function of SMA: the control of postural stability during stance or walking,[18] coordinating temporal sequences of actions,[23][24][25][26][27][28][29][30] bimanual coordination,[31][32] and the initiation of internally generated as opposed to stimulus driven movement.[3][29][30][33] The data, however, tend not to support an exclusive role of SMA in any one of these functions. Indeed, SMA is demonstrably active during non-sequential, unimanual, and stimulus-cued movements.[34]

For human voluntary movement the role of the SMA has been elucidated: Its activity generates the early component of the Bereitschaftspotential (BP) or readiness potential BP1 or BPearly.[35] The role of the SMA was further substantiated by Cunnington et al. 2003,[36] showing that SMA proper and pre-SMA are active prior to volitional movement or action, as well as the cingulate motor area (CMA) = anterior mid-cingulate cortex (aMCC). Recently is has been shown by integrating simultaneously acquired EEG and fMRI that SMA and aMCC have strong reciprocal connections that act to sustain each other’s activity, and that this interaction is mediated during movement preparation according to the Bereitschaftspotential amplitude.[37]

SMA in the monkey brain may emphasize locomotion, especially complex locomotion such as climbing or leaping.[38][39][40] This suggestion was based on studies in which stimulation on a behaviorally relevant time scale evoked complex, full body movements that resembled climbing or leaping. This hypothesis is consistent with previous hypotheses, including the involvement of SMA in postural stabilization, in internally generated movements, in bimanual coordination, and in the planning of movement sequences, because all of these functions are heavily recruited in complex locomotion. The locomotion hypothesis is an example of interpreting the motor cortex in terms of the underlying behavioral repertoire from which abstract control functions emerge, an approach emphasized by Graziano and colleagues.[38]

References

  1. 1 2 He, S.Q., Dum, R.P. and Strick, P.L (1995). "Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere". J. Neurosci 15: 3284–3306.
  2. 1 2 Luppino, G., Matelli, M., Camarda, R.M., Gallese, V. and Rizzolatti, G (1991). "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 (4): 463–482. doi:10.1002/cne.903110403. PMID 1757598.
  3. 1 2 Matsuzaka, Y., Aizawa, H., and Tanji, J (1992). "A motor area rostrao to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task". J. Neurophysiol 68 (3): 653–662. PMID 1432040.
  4. ↑ Bates, J.F. and Goldman-Rakic, P.S (1993). "Prefrontal connections of medial motor areas in the rhesus monkey". J. Comp. Neurol 336: 211–228. doi:10.1002/cne.903360205.
  5. 1 2 3 Dum, R.P. and Strick, P.L (1991). "The origin of corticospinal projections from the premotor areas in the frontal lobe". J. Neurosci 11: 667–689.
  6. ↑ Lu, M.T., Preston, J.B. and Strick, P.L (1994). "Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe". J. Comp. Neurol 341: 375–392. doi:10.1002/cne.903410308.
  7. ↑ Luppino, G., Matelli, M., Camarda, R. and Rizzolatti, G (1993). "Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey". J. Comp. Neurol 338 (1): 114–140. doi:10.1002/cne.903380109. PMID 7507940.
  8. ↑ Chen, L.L. and Walton, M.M (2005). "Head movement evoked by electrical stimulation in the supplementary eye field of the rhesus monkey". J. Neurophysiol 94: 4502–4519. doi:10.1152/jn.00510.2005.
  9. ↑ Russo, G.S. and Bruce, C.J (2000). "Supplementary eye field: representation of saccades and relationship between neural response fields and elicited eye movements". J. Neurophysiol 84: 2605–2621.
  10. ↑ Schlag, J and Schlag-Rey, M (1987). "Evidence for a supplementary eye field". J. Neurophysiol 57: 179–200.
  11. ↑ Tehovnik, E.J. and Lee, K (1993). "The dorsomedial frontal cortex of the rhesus monkey: topographic representation of saccades evoked by electrical stimulation". Exp. Brain Res 96: 430–442. doi:10.1007/bf00234111.
  12. ↑ Galea, M.P. and Darian-Smith, I (1994). "Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections". Cereb. Cortex 4: 166–194. doi:10.1093/cercor/4.2.166.
  13. 1 2 Macpherson, J., Marangoz, C., Miles, T.S. and Wiesendanger, M (1982). "Microstimulation of the supplementary motor area (SMA) in the awake monkey". Exp. Brain Res 45: 410–416. doi:10.1007/bf01208601.
  14. ↑ Murray, E.A. and Coulter, J.D (1981). "Organization of corticospinal neurons in the monkey". J. Comp. Neurol 195: 339–365. doi:10.1002/cne.901950212.
  15. ↑ Nudo, R.J. and Masterton, R.B (1990). "Descending pathways of the spinal cord, III: Sites of origin of the corticospinal tract". J. Comp. Neurol 296: 559–583. doi:10.1002/cne.902960405.
  16. ↑ Toyoshima, K and Sakai, H (1982). "Exact cortical extent of the origin of the corticospinal tract (CST) and the quantitative contribution to the CST in different cytoarchitectonic areas. A study with horseradish peroxidase in the monkey". J. Hirnforsch 23: 257–269.
  17. ↑ Zhang, S., Ide, J.S., and Li, C.S. (2012). "Resting-State Functional Connectivity of the Medial Superior Frontal Cortex". Cereb. Cortex 22: 99–111. doi:10.1093/cercor/bhr088.
  18. 1 2 Penfield, W. and Welch, K (1951). "The supplementary motor area of the cerebral cortex: A clinical and experimental study". Am. Med. Ass. Arch. Neurol. Psychiat. 66 (3): 289–317. doi:10.1001/archneurpsyc.1951.02320090038004. PMID 14867993.
  19. ↑ Woolsey, C.N., Settlage, P.H., Meyer, D.R., Sencer, W., Hamuy, T.P. and Travis, A.M. (1952). "Pattern of localization in precentral and "supplementary" motor areas and their relation to the concept of a premotor area". Association for Research in Nervous and Mental Disease, Vol. 30 (New York, NY: Raven Press): 238–264.
  20. ↑ Gould, H.J. III, Cusick, C.G., Pons, T.P. and Kaas, J.H (1996). "The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys". J. Comp. Neurol 247 (3): 297–325. doi:10.1002/cne.902470303. PMID 3722441.
  21. ↑ Muakkassa, K.F. and Strick, P.L (1979). "Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized 'premotor' areas". Brain Res 177: 176–182. doi:10.1016/0006-8993(79)90928-4.
  22. ↑ Mitz, A.R. and Wise, S.P (1987). "The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping". J. Neurosci 7: 1010–1021.
  23. ↑ Gaymard, B, Pierrot=Deseilligny, C. and Rivaud, S (1990). "Impairment of sequences of memory-guided saccades after supplementary motor area lesions". Annals of Neurology 28: 622–626. doi:10.1002/ana.410280504.
  24. ↑ Gerloff, C., Corwell, B., Chen, R., Hallett, M. and Cohen, L.G (1997). "Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences". Brain 120: 1587–1602. doi:10.1093/brain/120.9.1587.
  25. ↑ Jenkins, I.H., Brooks, D.J., Nixon, P.D., Frackowiak, R.S. and Passingham, R.E (1994). "Motor sequence learning: a study with positron emission tomography". J. Neurosci 14: 3775–3790.
  26. ↑ Lee, D. and Quessy, S (2003). "Activity in the supplementary motor area related to learning and performance during a sequential visuomotor task". J. Neurophysiol 89: 1039–1056. doi:10.1152/jn.00638.2002.
  27. ↑ Mushiake, H., Inase, M. and Tanjii, J (1990). "Selective coding of motor sequence in the supplementary motor area of the monkey cerebral cortex". Exp. Brain Res 82: 208–210. doi:10.1007/bf00230853.
  28. ↑ Shima, K. and Tanji, J (1998). "Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements". J. Neurophysiol 80 (6): 3247–3260. PMID 9862919.
  29. 1 2 Roland, P.E., Larsen, B., Lassen, N.A. and Skinhoj, E (1980). "Supplementary motor area and other cortical areas in organization of voluntary movements in man". J. Neurophysiol 43: 118–136.
  30. 1 2 Roland, P.E., Skinhoj, E., Lassen, N.A. and Larsen, B. (1980). "Different cortical areas in man in organization of voluntary movements in extrapersonal space". J. Neurophysiol 43: 137–150.
  31. ↑ Brinkman, C (1981). "Lesions in supplementary motor area interfere with a monkey's performance of a bimanual coordination task". Neurosci. Lett 27 (3): 267–270. doi:10.1016/0304-3940(81)90441-9. PMID 7329632.
  32. ↑ Serrien, D.J., Strens, L.H., Oliveiero, A. and Brown, P (2002). "Repetitive transcranial magnetic stimulation of the supplementary motor area (SMA) degrades bimanual movement control in humans". Neurosci. Lett 328: 89–92. doi:10.1016/s0304-3940(02)00499-8.
  33. ↑ Halsband, U., Matsuzaka, Y. and Tanji, J. (1994). "Neuronal activity in the primate supplementary, pre-supplementary and premotor cortex during externally and internally instructed sequential movements". Neurosci. Res 20 (2): 149–155. doi:10.1016/0168-0102(94)90032-9. PMID 7808697.
  34. ↑ Picard, N. and Strick, P.L (September 2003). "Activation of the supplementary motor area (SMA) during performance of visually guided movements". Cereb. Cortex 13 (9): 977–986. doi:10.1093/cercor/13.9.977. PMID 12902397.
  35. ↑ Deecke L, Kornhuber (1978). "supplementary" motor cortex in human voluntary finger movements". Brain Res 159: 473–476. doi:10.1016/0006-8993(78)90561-9.
  36. ↑ Cunnington R, Windischberger C, Deecke L, Moser E (2003). "The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response". NeuroImage 20: 404–412. doi:10.1016/s1053-8119(03)00291-x.
  37. ↑ Nguyen VT, Breakspear M, Cunnington R (2014). "Reciprocal interactions of the SMA and cingulate cortex sustain pre-movement activity for voluntary actions". J Neurosci 34: 16397–16407. doi:10.1523/jneurosci.2571-14.2014.
  38. 1 2 Graziano, M.S.A. (2008). The Intelligent Movement Machine. Oxford, UK: Oxford University Press.
  39. ↑ Graziano, M.S.A. and Aflalo, T.N. (2007). "Mapping behavioral repertoire onto the cortex.". Neuron 56 (2): 239–251. doi:10.1016/j.neuron.2007.09.013. PMID 17964243.
  40. ↑ Graziano, M.S.A., Aflalo, T.N. and Cooke, D.F (2005). "Arm movements evoked by electrical stimulation in the motor cortex of monkeys". J. Neurophysiol 94 (6): 4209–4223. doi:10.1152/jn.01303.2004. PMID 16120657.

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