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Functional Differences in Corticospinal Projections from Macaque Primary Motor Cortex and Supplementary Motor Area

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Sensorimotor Control of Movement and Posture

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 508))

Abstract

We made a quantitative comparison of the density of macaque corticospinal projections from primary motor cortex (Ml) and supplementary motor area (SMA) to spinal motor nuclei supplying hand and finger muscles. We also compared the action of corticospinal outputs from these two areas on 84 upper limb (mostly hand) motoneurones in chloralose-anaesthetised macaques. The hand representations of Ml and SMA were first identified using MRI and intracortical microstimulation. We made focal injections of WGA-HRP into these representations. Densitometric analysis showed that corticospinal projections from Ml were far denser and occupied a much greater proportion of the hand muscle motor nuclei than did SMA projections. Stimulation of M l and SMA with bipolar intracortical pulses evoked monosynaptic EPSPs. These were significantly larger and more common from MI (88% of motoneurons) than from SMA (48%). The results demonstrate corticomotoneuronal connections from both M I and SMA, some converging upon single motoneurons. Both areas give rise to CM projections but that those from M I are far more numerous and exert stronger excitatory effects than those from the SMA.

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References

  • Alstermark, B., Isa, T., Ohki, Y., and Saito, Y., 1999, isynaptic pyramidal excitation in forelimb motoneurons mediated via C3–C4 propriospinal neurons in the Macaca fuscata, Journal of Neurophysiology, 82, C3–C4.

    PubMed  CAS  Google Scholar 

  • Andersen, P., Hagan, P. J., Phillips, C. G., and Powell, T. P. S., 1975, Mapping by microstimulation of overlapping projections from area 4 to motor units of the baboon’s hand, Proceedings of the Royal Society,188, 31–60

    Article  CAS  Google Scholar 

  • Armand, J., 1982, The origin, course and terminations of corticospinal fibers in various mammals, Progress in Brain Research, 57, 330–360.

    Article  Google Scholar 

  • Armand, J., Olivier, E., Edgley, S. A., and Lemon, R. N., 1997, The postnatal development of corticospinal projections from motor cortex to the cervical enlargement in the macaque monkey, Journal of Neuroscience, 17, 251–266.

    PubMed  CAS  Google Scholar 

  • Baker, S. N., Olivier, E., amd Lemon, R. N., 1995, Task-related variation in corticospinal output evoked by transcranial magnetic stimulation in the macaque monkey, Journal of Physiology, 488, 795–801.

    PubMed  CAS  Google Scholar 

  • Baker, S. N., Philbin, N., Spinks, R., Pinches, E. M., Pauluis, Q., McManus, D., Lemon, R. N., and Wolpert, D. M., 1999, Multiple single unit recording in the cortex of monkeys using independently moveable microelectrodes, Journal of Neuroscience Methods, 94, 5–17.

    Article  PubMed  CAS  Google Scholar 

  • Bortoff, G. A., Strick, P.L., 1993, Corticospinal terminations in two New-World primates: Further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity, Journal of Neuroscience, 13, 5105–5118.

    PubMed  CAS  Google Scholar 

  • Deletis, V., Rodi, Z., and Amassian, V., 2001, Neurophysiological mechanisms underlying motor evoked potentials in anaesthetized humans. Part 2. Relationships between epidural recordings and muscle responses, Clinical Neurophysiology, 112,445–452.

    Article  PubMed  CAS  Google Scholar 

  • Dum, R. P., and Strick, P. L., 1991, The origin of corticospinal projections from the premotor areas in the frontal lobe, Journal of Neuroscience, 11, 667–689.

    PubMed  CAS  Google Scholar 

  • Dum, R. P., and Strick, P. L., 1996, Spinal cord terminations of the medial wall motor areas in macaque monkeys, Journal of Neuroscience, 16, 6513–6525.

    PubMed  CAS  Google Scholar 

  • Edgley, S. A., Eyre, J. A., Lemon, R. N., and Miller, S., 1990, Excitation of the corticospinal tract by electromagnetic and electrical stimulation of the scalp in the macaque monkey, Journal of Physiology, 425, 301–320.

    PubMed  CAS  Google Scholar 

  • Edgley, S. A., Eyre, J. A., Lemon, R. N., and Miller, S., 1997, Comparison of activation of corticospinal neurones and spinal motoneurones by magnetic and electrical stimulation in the monkey, Brain, 129, 839–853.

    Article  Google Scholar 

  • Fetz, EE., 1992, Are movement parameters recognizably coded in activity of single neurons? Behavioural and Brain Sciences, 15, 679–690.

    Google Scholar 

  • Gales, M. P., and Darian-Smith, I., 1994, Multiple corticospinal neuron populations in the Macaque monkey are specified by their unique cortical orgins, spinal terminations, and connections, Cerebral Cortex, 4, 166–194.

    Article  Google Scholar 

  • Huntley, G. W., and Jones, E.G., 1991, Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: A correlative anatomic and physiological study, Journal of Neurophysiology, 66, 390–413.

    PubMed  CAS  Google Scholar 

  • Jankowska, E., Padel, Y., and Tanaka, R., 1975, Projections of pyramidal tract cells to p-motoneurones innervating hind-limb muscles in monkey, Journal of Physiology, 249, 637–667.

    PubMed  CAS  Google Scholar 

  • Jankowska, E., Padel, Y., and Tanaka, R., 1976, Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey, Journal of Physiology, 258, 467–487

    PubMed  CAS  Google Scholar 

  • Kemell, D., and Wu, C-P., 1967, Post-synaptic effects of cortical stimulation on forelimb motoneurones in the baboon, Journal of Physiology, 191, 673–690.

    Google Scholar 

  • Kuypers, H. G. J. M., 1981, Anatomy of the descending pathways, in: Handbook of Physiology - The Nervous System II, Brookhart, J. M., and Mountcastle, V. B., ed., American Physiological Society, Bethesda, pp. 597–666.

    Google Scholar 

  • Lemon, R. N., 1988, The output map of the primate motor cortex, Trends in Neuroscience, 11, 501–506

    Article  CAS  Google Scholar 

  • Lemon, R. N., 1993, Cortical control of the primate hand, Experimental Physiology, 78, 263–301.

    PubMed  CAS  Google Scholar 

  • Lemon, R. N., Muir, R. B., and Mantel, G. W. H., 1987, The effects upon the activity of hand and forearm muscles of intracortical stimulation in the vicinity of corticomotor neurones in the conscious monkey,Experimental Brain Research, 66, 621–637.

    Article  CAS  Google Scholar 

  • 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, Journal of Comparative Neurology, 311, 463–482.

    Article  PubMed  CAS  Google Scholar 

  • Macpherson, J. M., Wiesendanger, M., Marangoz, C., and Miles, TS., 1982, Corticospinal neurones of the supplementary motor area of the monkey, Experimental Brain Research, 48, 81–88.

    Article  CAS  Google Scholar 

  • Maier, M. A., Armand, J., Kirkwood, P. A., Yang, H-W., Davis, J. N., and Lemon, R. N., 2001, Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study, Cerebral Cortex, in press.

    Google Scholar 

  • Maier, M. A., Illert, M., Kirkwood, P. A., Nielsen, J., and Lemon, R. N., 1998, Does a C3–C4 propriospinal system transmit corticospinal excitation in the primate? An investigation in the macaque monkey, Journal of Physiology, 511,C3–C4.

    Article  CAS  Google Scholar 

  • Maier, M. A., Olivier, E., Baker, S. N., Kirkwood, P. A., Morris, T., and Lemon, RN., 1997, Direct and indirect corticospinal control of arm and hand motoneurons in the squirrel monkey (Saimiri sciureus), Journal of Neurophysiology, 78, 721–733.

    PubMed  CAS  Google Scholar 

  • Mitz, A. R., and Wise, S. P., 1987, The somatotopic organization of the supplementary motor area: intracortical microstimulation mappingJournal of Neuroscience, 7, 1010–1021.

    PubMed  CAS  Google Scholar 

  • Muir, R. B., and Porter, R., 1973, The effect of a preceding stimulus on temporal summation at corticomotoneuronal synapses, Journal of Physiology, 228, 749–763.

    PubMed  CAS  Google Scholar 

  • Nakajima, K., Maier, M. A., Kirkwood, P. A., and Lemon, R. N., 2000, Striking differences in the transmission of corticospinal excitation to upper limb motoneurons in two primate species, Journal of Neurophysiology,84,698–709.

    PubMed  CAS  Google Scholar 

  • Patton, H. D., Amassian, VE., 1954, Single-and multiple-unit analysis of cortical stage of pyramidal tract activation, Journal of Neurophysiology,17, 345–363.

    PubMed  CAS  Google Scholar 

  • Perlmutter, S. I., Maier, M. A., and Fetz, E. E., 1998, Activity of spinal interneurons and their effects on forearm muscles during voluntary wrist movements in the monkey, Journal of Neurophysiology, 80, 2475–2494.

    PubMed  CAS  Google Scholar 

  • Phillips, C. G., and Porter, R., 1964, The pyramidal projection to motoneurones of some muscle groups of the baboon’s forelimb, Progress in Brain Research, 12, 222–245.

    Article  PubMed  CAS  Google Scholar 

  • Porter, R., and Lemon, R. N., 1993, Corticospinal Function and Voluntary Movement,Clarendon Press, Oxford.

    Google Scholar 

  • Rouiller, E. M., Yu, X. H., Moret, V., Tempini, A., Wiesendanger, M., and Liang, F.1998 Dexterity in adult monkeys following early lesion of the motor cortical hand area: the role of cortex adjacent to the lesionEuropean Journal of Neuroscience, 10,729–740.

    Article  PubMed  CAS  Google Scholar 

  • Schieber, M. H., Hibbard, L. S., 1993, How somatotopic is the motor cortex hand area? Science, 261, 489–492. Tanji, J., 1994, The supplementary motor area in the cerebral cortex, Neuroscience Research, 19, 489–492.

    Google Scholar 

  • Wise, SP., 1996, Corticospinal efferents of the supplementary sensorimotor area in relation to the primary motor area, in: Advances in Neurology, Luders, H. O., ed., Lippincott-Raven, Philadelphia, pp. 57–69.

    Google Scholar 

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Lemon, R.N., Maier, M.A., Armand, J., Kirkwood, P.A., Yang, HW. (2002). Functional Differences in Corticospinal Projections from Macaque Primary Motor Cortex and Supplementary Motor Area. In: Gandevia, S.C., Proske, U., Stuart, D.G. (eds) Sensorimotor Control of Movement and Posture. Advances in Experimental Medicine and Biology, vol 508. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0713-0_48

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  • DOI: https://doi.org/10.1007/978-1-4615-0713-0_48

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5206-8

  • Online ISBN: 978-1-4615-0713-0

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