1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Neuroscience
  4. Volume 44, 2021
  5. Article

Annual Review of Neuroscience

Volume 44, 2021

The Cortical Motor Areas and the Emergence of Motor Skills: A Neuroanatomical Perspective

Abstract

What changes in neural architecture account for the emergence and expansion of dexterity in primates? Dexterity, or skill in performing motor tasks, depends on the ability to generate highly fractionated patterns of muscle activity. It also involves the spatiotemporal coordination of activity in proximal and distal muscles across multiple joints. Many motor skills require the generation of complex movement sequences that are only acquired and refined through extensive practice. Improvements in dexterity have enabled primates to manufacture and use tools and humans to engage in skilled motor behaviors such as typing, dance, musical performance, and sports. Our analysis leads to the following synthesis: The neural substrate that endows primates with their enhanced motor capabilities is due, in part, to () major organizational changes in the primary motor cortex and () the proliferation of output pathways from other areas of the cerebral cortex, especially from the motor areas on the medial wall of the hemisphere.

Keyword(s): corticomotoneuronal, corticospinal, dexterity, motor cortex, rabies virus, transneuronal transport
Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-070918-050216
2021-07-08
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/neuro/44/1/annurev-neuro-070918-050216.html?itemId=/content/journals/10.1146/annurev-neuro-070918-050216&mimeType=html&fmt=ahah

Literature Cited

  1. Akkal D, Bioulac B, Audin J, Burbaud P. 2002. 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
     [Google Scholar]
  2. Alstermark B, Isa T. 2012. Circuits for skilled reaching and grasping. Annu. Rev. Neurosci. 35:559–78
     [Google Scholar]
  3. Alstermark B, Isa T, Pettersson L-G, Sasaki S. 2007. The C3-C4 propriospinal system in the cat and monkey: a spinal pre-motoneuronal centre for voluntary motor control. Acta Physiol 189:123–40
     [Google Scholar]
  4. Alstermark B, Ogawa J, Isa T 2004. Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurones and polysynaptic EPSPs via segmental interneurons. J. Neurophysiol. 91:1832–39
     [Google Scholar]
  5. Armand J, Edgley SA, Lemon RN, Olivier E 1994. Protracted postnatal development of corticospinal projections from the primary motor cortex to hand motoneurones in the macaque monkey. Exp. Brain Res. 101:178–82
     [Google Scholar]
  6. Armand J, Olivier E, Edgley SA, Lemon RN. 1997. The postnatal development of corticospinal projections from motor cortex to the cervical enlargement in the macaque monkey. J. Neurosci. 17:251–66
     [Google Scholar]
  7. Backus DA, Ye S, Russo GS, Crutcher MD. 2001. Neural activity correlated with the preparation and execution of visually guided arm movements in the cingulate motor area of the monkey. Exp. Brain Res. 140:182–89
     [Google Scholar]
  8. Barthas F, Kwan AC. 2017. Secondary motor cortex: where “sensory” meets “motor” in the rodent frontal cortex. Trends Neurosci 40:181–93
     [Google Scholar]
  9. Beckmann M, Johansen-Berg H, Rushworth MF. 2009. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J. Neurosci. 29:1175–90
     [Google Scholar]
  10. Bennett KMB, Lemon RN. 1996. Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey. J. Neurophysiol. 75:1826–42
     [Google Scholar]
  11. Bernhard CG, Bohm E, Petersen I. 1953. New investigations on the pyramidal system in Macaca mulatta. Experientia 9:111–12
     [Google Scholar]
  12. Bonini L, Ugolotti Serventi F, Bruni S, Maranesi M, Bimbi M et al. 2012. Selectivity for grip type and action goal in macaque inferior parietal and ventral premotor grasping neurons. J. Neurophysiol. 108:1607–19
     [Google Scholar]
  13. Bonini L, Ugolotti Serventi F, Simone L, Rozzi S, Ferrari PF, Fogassi L 2011. Grasping neurons of monkey parietal and premotor cortices encode action goals at distinct levels of abstraction during complex action sequences. J. Neurosci. 31:5876–86
     [Google Scholar]
  14. Borra E, Belmalih A, Gerbella M, Rozzi S, Luppino G. 2010. Projections of the hand field of the macaque ventral premotor area F5 to the brainstem and spinal cord. J. Comp. Neurol. 518:2570–91
     [Google Scholar]
  15. Bortoff GA, Strick PL. 1993. Corticospinal terminations in two New-World primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. J. Neurosci. 13:5105–18
     [Google Scholar]
  16. Buys EJ, Lemon RN, Mantel GW, Muir RB. 1986. Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. J. Physiol. 381:529–49
     [Google Scholar]
  17. Cadoret G, Smith AM. 1997. Comparison of the neuronal activity in the SMA and the ventral cingulate cortex during prehension in the monkey. J. Neurophysiol. 77:153–66
     [Google Scholar]
  18. Clough JFM, Kernell D, Phillips CG. 1968. The distribution of monosynaptic excitation from the pyramidal tract and from primary spindle afferents to motoneurones of the baboon's hand and forearm. J. Physiol. 198:145–66
     [Google Scholar]
  19. Cona G, Semenza C. 2017. Supplementary motor area as key structure for domain-general sequence processing: a unified account. Neurosci. Biobehav. Rev. 72:28–42
     [Google Scholar]
  20. Davidson AG, Chan V, O'Dell R, Schieber MH 2007. Rapid changes in throughput from single motor cortex neurons to muscle activity. Science 318:1934–37
     [Google Scholar]
  21. de la Vega A, Chang LJ, Banich MT, Wager TD, Yarkoni T. 2016. Large-scale meta-analysis of human medial frontal cortex reveals tripartite functional organization. J. Neurosci. 36:6553–62
     [Google Scholar]
  22. Dum RP, Levinthal DJ, Strick PL 2016. Motor, cognitive, and affective areas of the cerebral cortex influence the adrenal medulla. PNAS 113:9922–27
     [Google Scholar]
  23. Dum RP, Levinthal DJ, Strick PL 2019. The mind-body problem: circuits that link the cerebral cortex to the adrenal medulla. PNAS 116:26321–28
     [Google Scholar]
  24. Dum RP, Strick PL. 1991. The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 11:667–89
     [Google Scholar]
  25. Dum RP, Strick PL. 1996. Spinal cord terminations of the medial wall motor areas in macaque monkeys. J. Neurosci. 16:6513–25
     [Google Scholar]
  26. Dum RP, Strick PL. 2002. Motor areas in the frontal lobe of the primate. Physiol. Behav. 77:677–82
     [Google Scholar]
  27. Ebbesen CL, Insanally MN, Kopec CD, Murakami M, Saiki A, Erlich JC. 2018. More than just a “motor”: recent surprises from the frontal cortex. J. Neurosci. 38:9402–13
     [Google Scholar]
  28. Esposito MS, Capelli P, Arber S. 2014. Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature 508:7496351–56
     [Google Scholar]
  29. Eyre JA. 2007. Corticospinal tract development and its plasticity after perinatal injury. Neurosci. Biobehav. Rev. 31:1136–49
     [Google Scholar]
  30. Eyre JA, Miller S, Clowry GJ, Conway EA, Watts C. 2000. Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres. Brain 123:51–64
     [Google Scholar]
  31. Fetz EE, Cheney PD. 1980. Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J. Neurophysiol. 44:751–72
     [Google Scholar]
  32. Firmin L, Field P, Maier MA, Kraskov A, Kirkwood PA et al. 2014. Axon diameters and conduction velocities in the macaque pyramidal tract. J. Neurophysiol. 112:1229–40
     [Google Scholar]
  33. Fluet MC, Baumann MA, Scherberger H. 2010. Context-specific grasp movement representation in macaque ventral premotor cortex. J. Neurosci. 30:15175–84
     [Google Scholar]
  34. Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L, Rizzolatti G. 2001. Cortical mechanism for the visual guidance of hand grasping movements in the monkey: a reversible inactivation study. Brain 124:571–86
     [Google Scholar]
  35. Fragaszy DM. 1983. Preliminary quantitative studies of prehension in squirrel monkeys (Saimiri sciureus). Brain Behav. Evol. 23:81–92
     [Google Scholar]
  36. Galea MP, 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 4:166–94
     [Google Scholar]
  37. Galea MP, Darian-Smith I. 1995. Postnatal maturation of the direct corticospinal projections in the macaque monkey. Cereb. Cortex 5:518–40
     [Google Scholar]
  38. Galea MP, Darian-Smith I. 1997. Corticospinal projection patterns following unilateral section of the cervical spinal cord in the newborn and juvenile macaque monkey. J. Comp. Neurol. 381:282–306
     [Google Scholar]
  39. Gardner EP, Babu KS, Reitzen SD, Ghosh S, Brown AS et al. 2007a. Neurophysiology of prehension. I. Posterior parietal cortex and object-oriented hand behaviors. J. Neurophysiol. 97:387–406
     [Google Scholar]
  40. Gardner EP, Debowy DJ, Ro JY, Ghosh S, Babu KS. 2002. Sensory monitoring of prehension in the parietal lobe: a study using digital video. Behav. Brain Res. 135:213–24
     [Google Scholar]
  41. Gardner EP, Ro JY, Babu KS, Ghosh S. 2007b. Neurophysiology of prehension. II. Response diversity in primary somatosensory (S-I) and motor (M-I) cortices. J. Neurophysiol. 97:1656–70
     [Google Scholar]
  42. Gentner R, Classen J. 2006. Modular organization of finger movements by the human central nervous system. Neuron 52:731–42
     [Google Scholar]
  43. Giszter SF, Mussa-Ivaldi FA, Bizzi E 1993. Convergent force fields organized in the frog's spinal cord. J. Neurosci. 13:467–91
     [Google Scholar]
  44. Griffin DM, Hoffman DS, Strick PL. 2015. Corticomotoneuronal cells are “functionally tuned. .” Science 350:6261667–70
     [Google Scholar]
  45. Griffin DM, Strick PL. 2020. The motor cortex uses active suppression to sculpt movement. Sci. Adv. 6:eabb8395
     [Google Scholar]
  46. Gu Z, Kalambogias J, Yoshioka S, Han W, Li Z et al. 2017. Control of species-dependent cortico-motoneuronal connections underlying manual dexterity. Science 357:6349400–4
     [Google Scholar]
  47. Hardwick RM, Rottschy C, Miall RC, Eickhoff SB 2013. A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67:283–97
     [Google Scholar]
  48. Harel R, Asher I, Cohen O, Israel Z, Shalit U et al. 2008. Computation in spinal circuitry: lessons from behaving primates. Behav. Brain Res. 194:119–28
     [Google Scholar]
  49. He SQ, Dum RP, Strick PL. 1993. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J. Neurosci. 13:952–80
     [Google Scholar]
  50. He SQ, Dum RP, Strick PL. 1995. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J. Neurosci. 15:3284–306
     [Google Scholar]
  51. Heffner RS, Masterton RB. 1975. Variation in form of the corticospinal tract and its relationship to digital dexterity. Brain Behav. Evol. 12:161–200
     [Google Scholar]
  52. Heffner RS, Masterton RB. 1983. The role of the corticospinal tract in the evolution of human digital dexterity. Brain Behav. Evol. 23:165–83
     [Google Scholar]
  53. Heilbronner SR, Hayden BY. 2016. Dorsal anterior cingulate cortex: a bottom-up view. Annu. Rev. Neurosci. 39:149–70
     [Google Scholar]
  54. Hoffstaedter F, Grefkes C, Caspers S, Roski C, Palomero-Gallagher N et al. 2014. The role of anterior midcingulate cortex in cognitive motor control: evidence from functional connectivity analyses. Hum. Brain Mapp. 35:2741–53
     [Google Scholar]
  55. Holmes G, May WP. 1909. On the exact origin of the pyramidal tracts in man and other mammals. Proc. R. Soc. Med. 2:92–100
     [Google Scholar]
  56. Isa T, Ohki Y, Alstermark B, Pettersson LG, Sasaki S. 2007. Direct and indirect corticomotoneuronal pathways and control of hand/arm movements. Physiology 22:145–52
     [Google Scholar]
  57. Jankowska E, Padel Y, Tanaka R. 1976. Projections of pyramidal tract cells to alpha-motoneurones innervating hind-limb muscles in the monkey. J. Physiol. 249:637–67
     [Google Scholar]
  58. Jenny AB, Saper CB. 1987. Organization of the facial nucleus and corticofacial projection in the monkey: a reconsideration of the upper motor neuron facial palsy. Neurology 37:930–39
     [Google Scholar]
  59. Jürgens U, Alipour M. 2002. A comparative study on the cortico-hypoglossal connections in primates, using biotin dextranamine. Neurosci. Lett. 328:245–48
     [Google Scholar]
  60. Kaas JH. 2004. Evolution of somatosensory and motor cortex in primates. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 281:1148–56
     [Google Scholar]
  61. Kamiyama T, Kameda H, Murabe N, Fukuda S, Yoshioka N et al. 2015. Corticospinal tract development and spinal cord innervation differ between cervical and lumbar targets. J. Neurosci. 35:1181–91
     [Google Scholar]
  62. Kondo T, Yoshihara Y, Yoshino-Saito K, Sekiguchi T, Kosugi A et al. 2015. Histological and electrophysiological analysis of the corticospinal pathway to forelimb motoneurons in common marmosets. Neurosci. Res. 98:35–44
     [Google Scholar]
  63. Kraskov A, Baker S, Soteropoulos D, Kirkwood P, Lemon R. 2019. The corticospinal discrepancy: Where are all the slow pyramidal tract neurons?. Cereb. Cortex 29:3977–81
     [Google Scholar]
  64. Kuypers HGJM. 1962. Corticospinal connections: postnatal development in the rhesus monkey. Science 138:678–80
     [Google Scholar]
  65. Kuypers HGJM. 1981. Anatomy of the descending pathways. Handbook of Physiology, Section 1: The Nervous System, Vol. II, Motor Control, Part I VB Brooks 597–666 Bethesda, MD: Am. Physiol. Soc.
     [Google Scholar]
  66. Kuypers HGJM, Brinkman J. 1970. Precentral projections to different parts of the spinal intermediate zone in the rhesus monkey. Brain Res 24:29–48
     [Google Scholar]
  67. Landgren S, Phillips CG, Porter R. 1962. Cortical fields of origin of the monosynaptic pyramidal pathways to some alpha motoneurones of the baboon's hand and forearm. J. Physiol. 161:112–25
     [Google Scholar]
  68. Lassek AM. 1954. The Pyramidal Tract: Its Status in Medicine. Springfield, IL: Charles C. Thomas
  69. Latash ML. 2010. Motor synergies and the equilibrium-point hypothesis. Motor Control 14:294–322
     [Google Scholar]
  70. Latash ML, Scholz JP, Schoner G. 2007. Toward a new theory of motor synergies. Motor Control 11:276–308
     [Google Scholar]
  71. Lawrence DG, Hopkins DA. 1976. The development of motor control in the rhesus monkey: evidence concerning the role of corticomotoneuronal connections. Brain 99:235–54
     [Google Scholar]
  72. Lawrence DG, Kuypers HGJM. 1968a. The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 91:1–14
     [Google Scholar]
  73. Lawrence DG, Kuypers HGJM. 1968b. The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathway. Brain 91:15–36
     [Google Scholar]
  74. Lemon RN. 2008. Descending pathways in motor control. Annu. Rev. Neurosci. 31:195–218
     [Google Scholar]
  75. Lemon RN. 2019. Recent advances in our understanding of the primate corticospinal system. F1000Res 8:274
     [Google Scholar]
  76. Leo A, Handjaras G, Bianchi M, Marino H, Gabiccini M et al. 2016. A synergy-based hand control is encoded in human motor cortical areas. eLife 5:e13420
     [Google Scholar]
  77. Maier MA, Armand J, Kirkwood PA, Yang HW, Davis JN, Lemon RN 2002. Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study. Cereb. Cortex 12:281–96
     [Google Scholar]
  78. Maier MA, Olivier E, Baker SN, Kirkwood PA, Morris T, Lemon RN. 1997. Direct and indirect corticospinal control of arm and hand motoneurons in the squirrel monkey (Saimiri sciureus). J. Neurophysiol. 78:721–33
     [Google Scholar]
  79. Martin GF, Beattie MS, Bresnahan JC, Henkel CK, Hughes HC. 1975. Cortical and brain stem projections to the spinal cord of the American opossum (Didelphis marsupialis virginiana). Brain Behav. Evol. 12:270–289
     [Google Scholar]
  80. McKiernan BJ, Marcario K, Karrer JH, Cheney PD. 1998. Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. J. Neurophysiol. 80:1961–80
     [Google Scholar]
  81. McNeal DW, Darling WG, Ge J, Stilwell-Morecraft KS, Solon KM et al. 2010. Selective long-term reorganization of the corticospinal projection from the supplementary motor cortex following recovery from lateral motor cortex injury. J. Comp. Neurol. 518:586–621
     [Google Scholar]
  82. Morecraft RJ, Ge J, Stilwell-Morecraft KS, Rotella DL, Pizzimenti MA, Darling WG. 2019. Terminal organization of the corticospinal projection from the lateral premotor cortex to the cervical enlargement (C5-T1) in rhesus monkey. J. Comp. Neurol. 527:2761–89
     [Google Scholar]
  83. Morecraft RJ, Louie JL, Herrick JL, Stilwell-Morecraft KS. 2001. Cortical innervation of the facial nucleus in the non-human primate: a new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression. Brain 124:176–208
     [Google Scholar]
  84. Morecraft RJ, Stilwell-Morecraft KS, Rossing WR 2004. The motor cortex and facial expression: new insights from neuroscience. Neurologist 10:235–49
     [Google Scholar]
  85. Muir RB, Lemon RN. 1983. Corticospinal neurons with a special role in precision grip. Brain Res 261:312–16
     [Google Scholar]
  86. Muir RB, Porter R. 1973. The effect of a preceding stimulus on temporal facilitation at corticomotoneuronal synapses. J. Physiol. 228:749–63
     [Google Scholar]
  87. Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G. 1997. Object representation in the ventral premotor cortex (area F5) of the monkey. J. Neurophysiol. 78:2226–30
     [Google Scholar]
  88. Nachev P, Kennard C, Husain M. 2008. Functional role of the supplementary and pre-supplementary motor areas. Nat. Rev. Neurosci. 9:856–69
     [Google Scholar]
  89. Nakajima K, Maier MA, Kirkwood PA, Lemon RN. 2000. Striking differences in transmission of corticospinal excitation to upper limb motoneurons in two primate species. J. Neurophysiol. 84:698–709
     [Google Scholar]
  90. Napier JR. 1961. Prehensility and opposability in the hands of primates. Symp. Zool. Soc. Lond. 5:115–32
     [Google Scholar]
  91. Nudo RJ, Masterton RB. 1990a. Descending pathways to the spinal cord, III: sites of origin of the corticospinal tract. J. Comp. Neurol. 296:559–83
     [Google Scholar]
  92. Nudo RJ, Masterton RB. 1990b. Descending pathways to the spinal cord, IV: some factors related to the amount of cortex devoted to the corticospinal tract. J. Comp. Neurol. 296:584–97
     [Google Scholar]
  93. Overduin SA, d'Avella A, Carmena JM, Bizzi E. 2012. Microstimulation activates a handful of muscle synergies. Neuron 76:1071–77
     [Google Scholar]
  94. Overduin SA, d'Avella A, Roh J, Carmena JM, Bizzi E. 2015. Representation of muscle synergies in the primate brain. J. Neurosci. 35:12615–24
     [Google Scholar]
  95. Palmer E, Ashby P. 1992. Corticospinal projections to upper limb motoneurones in humans. J. Physiol. 448:397–412
     [Google Scholar]
  96. Park MC, Belhaj-Saif A, Gordon M, Cheney PD 2001. Consistent features in the forelimb representation of primary motor cortex in rhesus macaques. J. Neurosci. 21:2784–92
     [Google Scholar]
  97. Phillips CG, Powell TP, Wiesendanger M. 1971. Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. J. Physiol. 217:419–46
     [Google Scholar]
  98. Phillips KA. 1998. Tool use in wild capuchin monkeys. Am. J. Primatol. 46:259–61
     [Google Scholar]
  99. Picard N, Strick PL. 1996. Motor areas of the medial wall: a review of their location and functional activation. Cereb. Cortex 6:342–53
     [Google Scholar]
  100. Picard N, Strick PL. 2001. Imaging the premotor areas. Curr. Opin. Neurobiol. 11:6663–72
     [Google Scholar]
  101. Porter R, Lemon RN. 1993. Corticospinal Function and Voluntary Movement Oxford, UK: Oxford Univ. Press
  102. Pouydebat E, Gorce P, Coppens Y, Bels V. 2009. Biomechanical study of grasping according to the volume of the object: human versus non-human primates. J. Biomech. 42:266–72
     [Google Scholar]
  103. Prabhu G, Shimazu H, Cerri G, Brochier T, Spinks RL et al. 2009. Modulation of primary motor cortex outputs from ventral premotor cortex during visually guided grasp in the macaque monkey. J. Physiol. 587:1057–69
     [Google Scholar]
  104. Rathelot JA, Dum RP, Strick PL 2017. Posterior parietal cortex contains a command apparatus for hand movements. PNAS 114:4255–60
     [Google Scholar]
  105. Rathelot JA, Nwankwo A, Strick PL. 2016. Origin of descending commands from the cerebral cortex to hand motoneurons in the rat. Neurosci. Meet. Plan. Program 534:1 Abstr .)
     [Google Scholar]
  106. Rathelot JA, Strick PL 2006. Muscle representation in the macaque motor cortex: an anatomical perspective. PNAS 103:8257–62
     [Google Scholar]
  107. Rathelot JA, Strick PL 2009. Subdivisions of primary motor cortex based on cortico-motoneuronal cells. PNAS 106:918–23
     [Google Scholar]
  108. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S. 2004a. The role of the medial frontal cortex in cognitive control. Science 306:5695443–47
     [Google Scholar]
  109. Ridderinkhof KR, van den Wildenberg WP, Segalowitz SJ, Carter CS. 2004b. Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn 56:129–40
     [Google Scholar]
  110. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M. 1988. Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp. Brain Res. 71:491–507
     [Google Scholar]
  111. Rolls ET. 2019. The cingulate cortex and limbic systems for emotion, action, and memory. Brain Struct. Funct. 224:3001–18
     [Google Scholar]
  112. Rosenbaum D. 1991. Human Motor Control. San Diego, CA: Academic Press, 1st ed..
  113. Rouiller EM, Moret V, Tanne J, Boussaoud D. 1996. Evidence for direct connections between the hand region of the supplementary motor area and cervical motoneurons in the macaque monkey. Eur. J. Neurosci. 8:1055–59
     [Google Scholar]
  114. Russell JR, DeMeyer W. 1961. The quantitative cortical origin of pyramidal axons of Macaca mulatta. Neurology 11:96–108
     [Google Scholar]
  115. Russo GS, Backus DA, Ye S, Crutcher MD. 2002. Neural activity in monkey dorsal and ventral cingulate motor areas: comparison with the supplementary motor area. J. Neurophysiol. 88:2612–29
     [Google Scholar]
  116. Saslow JM. 1991. The Poetry of Michelangelo: An Annotated Translation New Haven, CT: Yale Univ. Press
  117. Schieber MH. 2001. Constraints on somatotopic organization in the primary motor cortex. J. Neurophysiol. 86:2125–43
     [Google Scholar]
  118. Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ. 2011. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 12:154–67
     [Google Scholar]
  119. Shalit U, Zinger N, Joshua M, Prut Y 2012. Descending systems translate transient cortical commands into a sustained muscle activation signal. Cereb. Cortex 22:1904–14
     [Google Scholar]
  120. Shinoda Y, Yokota J, Futami T. 1981. Divergent projection of corticospinal axons to motoneurons of multiple muscles in the monkey. Neurosci. Lett. 23:7–12
     [Google Scholar]
  121. Touroutoglou A, Andreano J, Dickerson BC, Barrett LF. 2020. The tenacious brain: how the anterior mid-cingulate contributes to achieving goals. Cortex 123:12–29
     [Google Scholar]
  122. Toyoshima K, 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. 23:257–69
     [Google Scholar]
  123. Ueno M, Nakamura Y, Li J, Gu Z, Niehaus J et al. 2018. Corticospinal circuits from the sensory and motor cortices differentially regulate skilled movements through distinct spinal interneurons. Cell Rep 23:1286–300
     [Google Scholar]
  124. Umilta MA, Brochier T, Spinks RL, Lemon RN. 2007. Simultaneous recording of macaque premotor and primary motor cortex neuronal populations reveals different functional contributions to visuomotor grasp. J. Neurophysiol. 98:488–501
     [Google Scholar]
  125. Westergaard GC, Fragaszy DM. 1987. The manufacture and use of tools by capuchin monkeys (Cebus apella). J. Comp. Psychol. 101:159–68
     [Google Scholar]
  126. Whishaw IQ, Coles BL. 1996. Varieties of paw and digit movement during spontaneous food handling in rats: postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions. Behav. Brain Res. 77:135–48
     [Google Scholar]
  127. Widener GL, Cheney PD. 1997. Effects on muscle activity from microstimuli applied to somatosensory and motor cortex during voluntary movement in the monkey. J. Neurophysiol. 77:2446–65
     [Google Scholar]
  128. Witham CL, Fisher KM, Edgley SA, Baker SN. 2016. Corticospinal inputs to primate motoneurons innervating the forelimb from two divisions of primary motor cortex and area 3a. J. Neurosci. 36:2605–16
     [Google Scholar]
  129. Yang H-W, Lemon RN. 2003. An electron microscopic examination of the corticospinal projection to the cervical spinal cord in the rat: lack of evidence for cortico-motoneuronal synapses. Exp. Brain Res. 149:458–69
     [Google Scholar]
  130. Yoshino-Saito K, Nishimura Y, Oishi T, Isa T 2010. Quantitative inter-segmental and inter-laminar comparison of corticospinal projections from the forelimb area of the primary motor cortex of macaque monkeys. Neuroscience 171:1164–79
     [Google Scholar]
  131. Zander SL, Weiss DJ, Judge PG. 2013. The interface between morphology and action planning: a comparison of two species of New World monkeys. Anim. Behav. 86:1251–58
     [Google Scholar]
/content/journals/10.1146/annurev-neuro-070918-050216
Loading
The Cortical Motor Areas and the Emergence of Motor Skills: A Neuroanatomical Perspective
Annual Review of Neuroscience 44, 425 (2021); https://doi.org/10.1146/annurev-neuro-070918-050216
/content/journals/10.1146/annurev-neuro-070918-050216
/content/journals/10.1146/annurev-neuro-070918-050216
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error