Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Internal Organization of the Motor Cortex for Input‐Output Arrangements

R. Porter

10.1002/cphy.cp010222

Source: Supplement 2: Handbook of Physiology, The Nervous System, Motor Control

Originally published: 1981

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Overview
2 Arrangement of Cells in Motor Cortex
2.1 Input of Thalamic Afferents to Cortex
2.2 Stratification of Output Elements
2.3 Output Cells With Separate Axonal Destinations
2.4 Complex Local Interactions Affecting Output Cells
2.5 Dynamic Input‐Output Relations for Individual Output Elements
3 Electrical Stimulation Studies in Motor Cortex
3.1 Cortical Distribution of Output Elements
3.2 Contributions of Different Output Elements to Response Produced
4 Influences of Natural Activation of Peripheral Receptors
4.1 Projection From Peripheral Afferents to Motor Cortex
4.2 Relation Between Afferent Input Zone and Motor Effect Field
4.3 Influence of Peripheral Afferent Input to Individual Cortical Elements
4.4 Input from Peripheral Receptors to Pyramidal Tract Neurons
5 Pathways for Afferent Projections
5.1 Thalamic Relay for Inputs to Motor Cortex
6 Modification of Cortical Responses to Peripheral Stimuli
7 Summary
Figure 1. Figure 1.

Diagram of basic circuitry of neocortex. Outlined areas, monosynaptic target cells of specific afferent or other thalamic inputs. Lightly stippled, assumed second‐order excitatory cells. Shaded areas, putative inhibitory interneurons that could be activated monosynaptically by specific sensory afferents (spec. sens. aff.). Darkly stippled, other inhibitory interneurons, either later order relative to specific sensory input, or directly contacted by corticocortical afferents (corticocortic. aff.). Extents of axon arborizations in different dimensions are indicated by number (microns).

From Szentágothai 102
Figure 2. Figure 2.

Simplified schematic diagram showing lamination of efferent pyramidal cells with axonal destinations in different situations. Distributions of neuron sizes in area 4 indicated in parentheses (mean ± SD).

Data from Jones and Wise 49 and Jones et al. 48


Figure 1.

Diagram of basic circuitry of neocortex. Outlined areas, monosynaptic target cells of specific afferent or other thalamic inputs. Lightly stippled, assumed second‐order excitatory cells. Shaded areas, putative inhibitory interneurons that could be activated monosynaptically by specific sensory afferents (spec. sens. aff.). Darkly stippled, other inhibitory interneurons, either later order relative to specific sensory input, or directly contacted by corticocortical afferents (corticocortic. aff.). Extents of axon arborizations in different dimensions are indicated by number (microns).

From Szentágothai 102


Figure 2.

Simplified schematic diagram showing lamination of efferent pyramidal cells with axonal destinations in different situations. Distributions of neuron sizes in area 4 indicated in parentheses (mean ± SD).

Data from Jones and Wise 49 and Jones et al. 48
References
 1. Adey, W. R., R. Porter, and I. D. Carter. Temporal dispersion in cortical afferent volleys as a factor in perception: an evoked potential study of deep somatic sensibility in the monkey. Brain 77: 325–344, 1954.
 2. Adrian, E. D. Afferent discharges to the cerebral cortex from peripheral sense organs. J. Physiol. London 100: 159–191, 1941.
 3. Albe‐Fessard, D., Y. Lamarre, and A. Pimpaneau. Sur l'origine fusoriale de certaines afferences somatiques atteignant le cortex moteur du singe. J. Physiol. Paris 58: 443–444, 1966.
 4. Albe‐Fessard, D., and J. Liebeskind. Origine des messages somatosensitifs activant les cellules du cortex moteur chez le singe. Exp. Brain Res. 1: 127–146, 1966.
 5. Andersen, P., P. J. Hagan, C. G. Phillips, and T. P. S. Powell. Mapping by microstimulation of overlapping projections from area 4 to motor units of the baboon's hand. Proc. R. Soc. London Ser. B. 188: 31P–36P, 1975.
 6. Armstrong, D. M. Synaptic excitation and inhibition of Betz cells by antidromic pyramidal volleys. J. Physiol. London 178: 37–38P, 1965.
 7. Asanuma, H. Recent developments in the study of the columnar arrangement of neurons within the motor cortex. Physiol. Rev. 55: 143–156, 1975.
 8. Asanuma, H., and I. Rosén. Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey. Exp. Brain Res. 14: 243–256, 1972.
 9. Bernhard, C. G., and E. Bohm. Cortical representation and functional significance of the cortico‐motoneuronal system. Arch. Neurol. Psychiatry 72: 473–502, 1954.
 10. Berrevoets, C. E., and H. G. J. M. Kuypers. Pericruciate cortical neurons projecting to brain stem reticular formation, dorsal column nuclei and spinal cord in the cat. Neurosci. Letters 1: 257–262, 1975.
 11. Brinkman, J., B. M. Bush, and R. Porter. Deficient influences of peripheral stimuli on precentral neurones in monkeys with dorsal column lesions. J. Physiol. London 276: 27–48, 1978.
 12. Brooks, V. B., and S. D. Stoney, Jr.. Motor mechanisms: the role of the pyramidal system in motor control. Annu. Rev. Physiol. 33: 337–392, 1971.
 13. Burns, B. D. The mammalian cerebral cortex. Monogr. Physiol. Soc. 5, 1958.
 14. Conrad, B., K. Matsunami, J. Meyer‐Lohmann, M. Wiesendanger, and V. B. Brooks. Cortical load compensation during voluntary elbow movements. Brain Res. 71: 507–514, 1974.
 15. Coulter, J. D., and E. G. Jones. Differential distribution of corticospinal projections from individual cytoarchitectonic fields in the monkey. Brain Res. 129: 335–340, 1977.
 16. Devanandan, M. S., and P. D. Heath. A short latency pathway from forearm nerves to area 4 of the baboon's cerebral cortex. J. Physiol. London 248: 43P–44P, 1975.
 17. Dreyer, D. A., R. J. Schneider, C. B. Metz, and B. L. Whitsel. Differential contributions of spinal pathways to body representation in postcentral gyrus of Macaca mulatto. J. Neurophysiol. 37: 119–145, 1974.
 18. Endo, K., T. Araki, and N. Yagi. The distribution and pattern of axon branching of pyramidal tract cells. Brain Res. 57: 484–491, 1973.
 19. Evarts, E. V. Pyramidal tract activity associated with a conditioned hand movement in the monkey. J. Neurophysiol. 29: 1011–1027, 1966.
 20. Evarts, E. V. Relation of pyramidal tract activity to force exerted during voluntary movement. J. Neurophysiol. 31: 14–27, 1968.
 21. Evarts, E. V. Motor cortex reflexes associated with learned movement. Science 179: 501–503, 1973.
 22. Evarts, E. V., and J. Tanji. Gating of motor cortex reflexes by prior instruction. Brain Res. 71: 479–494, 1974.
 23. Evarts, E. V., and J. Tanji. Reflex and intended responses in motor cortex pyramidal tract neurons of monkey. J. Neurophysiol. 39: 1069–1080, 1976.
 24. Fetz, E. E., and M. A. Baker. Response properties of precentral neurons in awake monkeys. Physiologist 12: 223, 1969.
 25. Fetz, E. E., and M. A. Baker. Operantly conditioned patterns of precentral unit activity and correlated responses in adjacent cells and contralateral muscles. J. Neurophysiol. 36: 179–204, 1973.
 26. Fetz, E. E., M. A. Baker, D. V. Finocchio, and M. J. Soso. Responses of precentral “motor” cells during passive and active joint movements. Program and Abstracts, Society of Neuro‐sciences, 4th Meeting, St. Louis, MO, Oct. 20–24, 1974, p. 208.
 27. Fetz, E. E., and P. D. Cheney. Muscle fields of primate corticomotoneuronal cells. J. Physiol. Paris 74: 239–245, 1978.
 28. Fetz, E. E., and D. V. Finocchio. Correlations between activity of motor cortex cells and arm muscles during operantly conditioned response patterns. Exp. Brain Res. 23: 217–240, 1975.
 29. Gatter, K. C., and T. P. S. Powell. The intrinsic connections of the cortex of area 4 of the monkey. Brain 101: 513–541, 1978.
 30. Gatter, K. C., J. J. Sloper, and T. P. S. Powell. An electron microscopic study of the termination of intracortical axons upon Betz cells in area 4 of the monkey. Brain 101: 543–553, 1978.
 31. Goldring, S., and R. Ratcheson. Human motor cortex: sensory input data from single neuron recordings. Science 175: 1493–1495, 1972.
 32. Gorman, A. L. F. Differential patterns of activation of the pyramidal system elicited by surface anodal and cathodal cortical stimulation. J. Neurophysiol. 29: 547–564, 1966.
 33. Hammond, P. H. The influence of prior instruction to the subject on an apparently involuntary neuro‐muscular response. J. Physiol. London 132: 17P–18P, 1956.
 34. Heath, C. J., J. Hore, and C. G. Phillips. Inputs from low threshold muscle and cutaneous afferents of hand and forearm to areas 3a and 3b of baboon's cerebral cortex. J. Physiol. London 257: 199–227, 1976.
 35. Hern, J. E. C., S. Landgren, C. G. Phillips, and R. Porter. Selective excitation of corticofugal neurones by surface‐anodal stimulation of the baboon's motor cortex. J. Physiol. London 161: 73–90, 1962.
 36. Hern, J. E. C., C. G. Phillips, and R. Porter. Electrical thresholds of unimpaled corticospinal cells in the cat. Q. J. Exp. Physiol. 47: 134–140, 1962.
 37. Hore, J., and R. Porter. The role of the pyramidal tract in the production of cortically evoked movement in the brush‐tailed possum Trichosurus vulpecula. Brain Res. 30: 232–234, 1971.
 38. Hore, J., J. B. Preston, R. G. Durkovic, and P. D. Cheney. Responses of cortical neurons (areas 3a and 4) to ramp stretch of hindlimb muscles in the baboon. J. Neurophysiol. 39: 484–500, 1976.
 39. Horne, M. K., and D. J. Tracey. The afferents and projections of the ventroposterolateral thalamus of the monkey. Exp. Brain Res. 36: 129–141, 1979.
 40. Hubel, D. H., and T. N. Weisel. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. London 160: 106–154, 1962.
 41. Humphrey, D. R., and W. S. Corrie. Properties of pyramidal tract neuron system within a functionally defined subregion of primate motor cortex. J. Neurophysiol. 41: 216–243, 1978.
 42. Humphrey, D. R., W. S. Corrie, and R. R. Rietz. Properties of the pyramidal tract neuron system within the precentral wrist and hand area of primate motor cortex. J. Physiol. Paris 74: 215–226, 1978.
 43. Humphrey, D. R., and R. R. Rietz. Cells of origin of corticocorubral projections from the arm area of primate motor cortex and their synaptic actions in the red nucleus. Brain Res. 110: 162–169, 1976.
 44. Jankowska, E., Y. Padel, and R. Tanaka. The mode of activation of pyramidal tract cells by intracortical stimuli. J. Physiol. London 249: 617–636, 1975.
 45. Jankowska, E., Y. Padel, and R. Tanaka. Projections of pyramidal tract cells to α‐motoneurones innervating hind‐limb muscles in the monkey. J. Physiol. London 249: 637–667, 1975.
 46. Jones, E. G. Lamination and differential distribution of thalamic afferents within the sensory‐motor cortex of the squirrel monkey. J. Comp. Neurol. 160: 167–204, 1975.
 47. Jones, E. G. Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey. J. Comp. Neurol. 160: 205–268, 1975.
 48. Jones, E. G., J. D. Coulter, H. Burton, and R. Porter. Cells or origin and terminal distribution of corticostriatal fibers arising in the sensory‐motor cortex of monkeys. J. Comp. Neurol. 173: 53–80, 1977.
 49. Jones, E. G., and S. P. Wise. Size, laminar and columnar distribution of efferent cells in the sensory‐motor cortex of monkeys. J. Comp. Neurol. 175: 391–438, 1977.
 50. Jones, E. G., S. P. Wise, and J. D. Coulter. Differential thalamic relationships of sensory‐motor and parietal cortical fields in monkeys. J. Comp. Neurol. 183: 833–882, 1979.
 51. Kelly, J. P., and D. C. Van Essen. Cell structure and function in the visual cortex of the cat. J. Physiol. London 238: 515–547, 1974.
 52. Kernell, D., and W. U. Chien‐Ping. Responses of the pyramidal tract to stimulation of the baboon's motor cortex. J. Physiol. London 191: 653–672, 1967.
 53. Kievit, J., and H. G. J. M. Kuypers. Organization of the thalamo‐cortical connexions to the frontal lobe in the rhesus monkey. Exp. Brain Res. 29: 299–322, 1977.
 54. Kuypers, H. G. J. M. Central cortical projections to motor and somato‐sensory cell groups. (An experimental study in the Rhesus monkey.) Brain 83: 161–184, 1960.
 55. Landau, W. M., G. H. Bishop, and M. H. Clare. Site of excitation in stimulation of the motor cortex. J. Neurophysiol. 28: 1206–1222, 1965.
 56. Landgren, S., C. G. Phillips, and R. Porter. Cortical fields of origin of the mono‐synaptic pyramidal pathways to some alpha motoneurones of the baboon's hand and forearm. J. Physiol. London 161: 112–125, 1962.
 57. Lemon, R. N., J. A. Hanby, and R. Porter. Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys. Proc. R. Soc. London Ser. B 194: 341–373, 1976.
 58. Lemon, R. N., and R. Porter. Afferent input to movement‐related precentral neurones in conscious monkeys. Proc. R. Soc. London Ser. B 194: 313–339, 1976.
 59. Lemon, R. N., and R. Porter. Short latency peripheral afferent inputs to pyramidal and other neurones in the precentral cortex of conscious monkeys. In: Active Touch, edited by G. Gordon. Oxford: Pergamon, 1978, p. 91–103.
 60. Lemon, R. N., and J. van der Burg. Short latency peripheral inputs to thalamic neurones projecting to the motor cortex. Exp. Brain Res. 36: 445–462, 1979.
 61. Lewis, M. McD., and R. Porter. Pyramidal tract discharge in relation to movement performance in monkeys with partial anaesthesia of the moving hand. Brain Res. 71: 245–251, 1974.
 62. Liddell, E. G. T. The brain and muscle management. Q. J. Exp. Physiol. 38: 125–137, 1953.
 63. Liddell, E. G. T., and C. G. Phillips. Thresholds of cortical representation. Brain 73: 125–140, 1950.
 64. Livingston, A., and C. G. Phillips. Maps and thresholds for the sensorimotor cortex of the cat. Q. J. Exp. Physiol. 42: 190–205, 1957.
 65. Lloyd, D. P. C. The spinal mechanism of the pyramidal system in cats. J. Neurophysiol. 4: 525–546, 1941.
 66. Lucier, G. E., D. C. Rüegg, and M. Wiesendanger. Responses of neurones in the motor cortex and in area 3a to controlled stretches of forelimb muscles in cebus monkeys. J. Physiol. London 251: 833–853, 1975.
 67. Lund, J. S. Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatto). J. Comp. Neurol. 147: 455–496, 1973.
 68. Maendly, R., D. G. Rüegg, J. Lagowska, M. Chofflon, and M. Wiesendanger. Projection sur le thalamus des afférences musculaires à bas sevill chez le singe (Abstract). J. Physiol. Paris 73: 79A, 1977.
 69. Malis, L. I., K. H. Pribram, and L. Kruger. Action potentials in “motor” cortex evoked by peripheral nerve stimulation. J. Neurophysiol. 16: 161–167, 1953.
 70. Marsden, C. D., P. A. Merton, and H. B. Morton. Servo action in human voluntary movement. Nature London 238: 140–143, 1972.
 71. Marsden, C. D., P. A. Merton, H. B. Morton, and J. Adam. The effect of lesions of the sensorimotor cortex and the capsular pathways on servo responses from the human long thumb flexor. Brain 100: 503–526, 1977.
 72. Matthews, P. B. C. Mammalian Muscle Receptors and Their Central Actions. Arnold: London, 1972.
 73. Mountcastle, V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20: 408–434, 1957.
 74. Mountcastle, V. B., Some functional properties of the somatic afferent system. In: Sensory Communication, edited by W. A. Rosenblith. Cambridge: MIT Press, 1961, p. 405–436.
 75. Mountcastle, V. B., G. F. Poggio, and G. Werner. The relation of thalamic cell response to peripheral stimuli varied over an intensive continuum. J. Neurophysiol. 26: 807–834, 1963.
 76. Murphy, J. T., Y. C. Wong, and H. C. Kwan. Afferent‐efferent linkages in motor cortex for single forelimb muscles. J. Neurophysiol. 38: 990–1014, 1975.
 77. Patton, H. D., and V. E. Amassian. The pyramidal tract: its excitation and functions. In: Handbook of Physiology. Neurophysiology, edited by J. Field. Washington, DC: Am. Physiol. Soc., 1960, sect. 1, vol. II, chapt. 34, p. 837–861.
 78. Phillips, C. G. Intracellular records from Betz cells in the cat. Q. J. Exp. Physiol. 41: 58–69, 1956.
 79. Phillips, C. G. Cortical motor threshold and the thresholds and distribution of excited Betz cells in the cat. Q. J. Exp. Physiol. 41: 70–84, 1956.
 80. Phillips, C. G. Actions of antidromic pyramidal volleys on single Betz cells in the cat. Q. J. Exp. Physiol. 44: 1–25, 1959.
 81. Phillips, C. G. Motor apparatus of the baboon's hand. Proc. R. Soc. London Ser. B 173: 141–174, 1969.
 82. Phillips, C. G., and R. Porter. Unifocal and bifocal stimulation of the motor cortex. J. Physiol. London 162: 532–538, 1962.
 83. Phillips, C. G., and R. Porter. Corticospinal Neurones: Their Role in Movement. London: Academic, 1977.
 84. Phillips, C. G., T. P. S. Powell, and M. Wiesendanger. Projection from low‐threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. J. Physiol. London 217: 419–446, 1971.
 85. Porter, R. Relationship of the discharges of cortical neurones to movement in free‐to‐move monkeys. Brain Res. 40: 39–43, 1972.
 86. Porter, R., Functions of the mammalian cerebral cortex in movement. In: Progress in Neurobiology, edited by G. A. Kerkut and J. W. Phillis. New York: Pergamon, 1973, p. 3–51.
 87. Porter, R. Influences of movement detectors on pyramidal tract neurons in primates. Annu. Rev. Physiol. 38: 121–137, 1976.
 88. Porter, R., and P. M. H. Rack. Timing of the responses in the motor cortex of monkeys to an unexpected disturbance of finger position. Brain Res. 103: 201–213, 1976.
 89. Preston, J. B., M. C. Shende, and K. Uemura. The motor cortex‐pyramidal system: patterns of facilitation and inhibition on motoneurons innervating limb musculature of cat and baboon and their possible adaptive significance. In: Neurophysiological Basis of Normal and Abnormal Motor Activities, edited by M. D. Yahr and D. P. Purpura. New York: Raven, 1967, p. 61–72. (Symp. Parkinson's Disease, 3rd, Columbia Univ., 1966.).
 90. Renaud, L. P., J. S. Kelly, and L. Provini. Observations on the functional identification and synaptic organization of pericruciate inhibitory neurons in the cat. Exp. Brain Res. 1 (Suppl.): 380–383, 1976.
 91. Rockel, A. J., R. W. Hiorns, and T. P. S. Powell. Proceedings: numbers of neurons through full depth of neocortex. J. Anat. 118: 371, 1974.
 92. Rosén, I., and H. Asanuma. Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input‐output relations. Exp. Brain Res. 14: 257–273, 1972.
 93. Shapovalov, A. I. Neuronal organization and synaptic mechanisms of supraspinal motor control in vertebrates. Rev. Physiol. Biochem. Pharmacol. 72: 2–54, 1975.
 94. Sherrington, C. S. The Integrative Action of the Nervous System (2nd ed.). New Haven: Yale Univ. Press, 1947.
 95. Sloper, J. J. Dendro‐dendritic synapses in the primate motor cortex. Brain Res. 34: 186–192, 1971.
 96. Sloper, J. J. Gap junctions between dendrites in the primate neocortex. Brain Res. 44: 641–646, 1972.
 97. Sloper, J. J. An electron microscopic study of the neurons of the primate motor and somatic sensory cortices. J. Neurocytol. 2: 351–359, 1973.
 98. Sloper, J. J. An electron microscope study of the termination of afferent connections to the primate motor cortex. J. Neurocytol. 2: 361–368, 1973.
 99. Strick, P. L. Anatomical analysis of ventrolateral thalamic input to primate motor cortex. J. Neurophysiol. 39: 1020–1031, 1976.
 100. Strick, P. L., and P. Sterling. Synaptic termination of afferents from the ventrolateral nucleus of the thalamus in the cat motor cortex. A light and electron microscope study. J. Comp. Neurol. 153: 77–106, 1974.
 101. Szentágothai, J. The “module‐concept” in cerebral cortex architecture. Brain Res. 95: 475–496, 1975.
 102. Szentágothai, J. Basic circuitry of the neocortex. Exp. Brain Res. Supp. 1: 282–287, 1976.
 103. Takahashi, K., K. Kubota, and M. Uno. Recurrent facilitation in cat pyramidal tract cells. J. Neurophysiol. 30: 22–34, 1967.
 104. Tsumoto, T., S. Nakumura, and K. Iwama. Pyramidal tract control over cutaneous and kinaesthetic sensory transmission in the cat thalamus. Exp. Brain Res. 22: 281–294, 1975.
 105. Uchizono, K. Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature London 207: 642–643, 1965.
 106. Wiesendanger, M. Input from muscle and cutaneous nerves of the hand and forearm to neurones of the precentral gyrus of baboons and monkeys. J. Physiol. London 228: 203–219, 1973.
 107. Woolsey, C. N., Organization of somatic sensory and motor areas of the cerebral cortex. In: Biological and Biochemical Bases of Behavior, edited by H. F. Harlow and C. N. Woolsey. Madison: Univ. Wisconsin Press, 1958, p. 63–81.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Internal Organization of the Motor Cortex for Input‐Output Arrangements
 

How to Cite

R. Porter. Internal Organization of the Motor Cortex for Input‐Output Arrangements. Compr Physiol 2011, Supplement 2: Handbook of Physiology, The Nervous System, Motor Control: 1063-1081. First published in print 1981. doi: 10.1002/cphy.cp010222