Spinal interneurons facilitate coactivation of hand muscles during a precision grip task in monkeys

Journal of Neuroscience

Volumn 30, Issue 50, 2010, Pages 17041-17050

  Takei, Tomohiko ^a,b   Seki, Kazuhiko ^a,b,c  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARM MUSCLE; ARTICLE; ELECTROMYOGRAPHY; GRIP STRENGTH; HAND MUSCLE; MALE; MONKEY; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD NERVE CELL; TASK PERFORMANCE;

ANIMALS; ARM; CERVICAL VERTEBRAE; ELECTROMYOGRAPHY; HAND; HAND STRENGTH; INTERNEURONS; MACACA; MALE; MUSCLE, STRIATED; SPINAL CORD;

EID: 78650319061     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4297-10.2010     Document Type: Article

References (67)

1. Armand J, Olivier E, Edgley SA, Lemon RN (1997) Postnatal development of corticospinal projections from motor cortex to the cervical enlargement in the macaque monkey. J Neurosci 17:251-266.
2. Baker SN, Lemon RN (1998) Computer simulation of post-spike facilitation in spike-triggered averages of rectified EMG. J Neurophysiol 80:1391-1406.
3. Baldissera F, Hultborn H, Illert M (1981) Integration in spinal neuronal systems. In: Handbook of physiology, Sec I, The nervous system, Vol II, Motor control, Part I (Brooks VB, ed), pp 509-595. Bethesda, MD: American Physiological Society.
4. Bell C (1834) The hand, its mechanism and vital endowments, as evincing design. London: William Pickering.
5. Bennett KM, Lemon RN (1996) Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey. J Neurophysiol 75:1826-1842.
6. Bizzi E, Mussa-Ivaldi FA, Giszter S (1991) Computations underlying the execution of movement: a biological perspective. Science 253:287-291.
7. Bizzi E, D'Avella A, Saltiel P, Tresch M (2002) Modular organization of spinal motor systems. Neuroscientist 8:437-442.
8. 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 13:5105-5118.
9. Brochier T, Spinks RL, Umilta MA, Lemon RN (2004) Patterns of muscle activity underlying object-specific grasp by the macaque monkey. J Neurophysiol 92:1770-1782.
10. Buys EJ, Lemon R, Mantel GW, Muir RB (1986) Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. J Physiol 381:529-549. (Pubitemid 17220332)
11. Cheema SS, Rustioni A, Whitsel BL (1984) Light and electron microscopic evidence for a direct corticospinal projection to superficial laminae of the dorsal horn in cats and monkeys. J Comp Neurol 225:276-290.
12. Cullheim S, Kellerth JO (1978) A morphological study of the axons and recurrent axon collaterals of cat alpha-motoneurones supplying different hind-limb muscles. J Physiol 281:285-299. (Pubitemid 9015886)
13. Davidson AG, Schieber MH, Buford JA (2007a) Bilateral spike-triggered average effects in arm and shoulder muscles from the monkey pontomedullary reticular formation. J Neurosci 27:8053-8058.
14. Davidson AG, O'Dell R, Chan V, Schieber MH (2007b) Comparing effects in spike-triggered averages of rectified EMG across different behaviors. J Neurosci Methods 163:283-294.
15. Dum RP, Strick PL (1996) Spinal cord terminations of the medial wall motor areas in macaque monkeys. J Neurosci 16:6513-6525.
16. Fetz EE, Cheney PD (1980) Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J Neurophysiol 44:751-772.
17. Flament D, Fortier PA, Fetz EE (1992) Response patterns and postspike effects of peripheral afferents in dorsal root ganglia of behaving monkeys. J Neurophysiol 67:875-889.
18. Giszter SF, Mussa-Ivaldi FA, Bizzi E (1993) Convergent force fields organized in the frog's spinal cord. J Neurosci 13:467-491.
19. Hahne M, Illert M, Wietelmann D (1988) Recurrent inhibition in the cat distal forelimb. Brain Res 456:188-192.
20. Hart CB, Giszter SF (2010) A neural basis for motor primitives in the spinal cord. J Neurosci 30:1322-1336.
21. Hongo T, Kitazawa S, Ohki Y, Xi MC (1989a) Functional identification of last-order interneurones of skin reflex pathways in the cat forelimb segments. Brain Res 505:167-170.
22. Hongo T, Kitazawa S, Ohki Y, Sasaki M, Xi MC (1989b) A physiological and morphological study of premotor interneurones in the cutaneous reflex pathways in cats. Brain Res 505:163-166.
23. Hörner M, Illert M, Kümmel H (1991) Absence of recurrent axon collaterals in motoneurones to the extrinsic digit extensor muscles of the cat forelimb. Neurosci Lett 122:183-186.
24. Jankowska E (1992) Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38:335-378.
25. Jenny AB, Inukai J (1983) Principles of motor organization of the monkey cervical spinal cord. J Neurosci 3:567-575.
26. Kilner JM, Baker SN, Lemon RN (2002) A novel algorithm to remove electrical cross-talk between surface EMG recordings and its application to the measurement of short-term synchronisation in humans. J Physiol 538:919-930.
27. Kitazawa S, Ohki Y, Sasaki M, Xi M, Hongo T (1993) Candidate premotor neurones of skin reflex pathways to T1 forelimb motoneurones of the cat. Exp Brain Res 95:291-307.
28. Kuypers H (1981) Anatomy of the descending pathways. In: Handbook of physiology, Sec I, The nervous system, Vol II, Motor control, Part I (Brooks V, ed), pp 597-666. Bethesda: American Physiological Society.
29. Kuypers HG, Brinkman J (1970) Precentral projections to different parts of the spinal intermediate zone in the rhesus monkey. Brain Res 24:29-48.
30. Lawrence DG, Kuypers HG (1968) The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 91:1-14.
31. Lemon RN (2008) Descending pathways in motor control. Annu Rev Neurosci 31:195-218.
32. Lemon RN, Mantel GW, Muir RB (1986) Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. J Physiol 381:497-527.
33. Long C 2nd, Conrad PW, Hall EA, Furler SL (1970) Intrinsic-extrinsic muscle control of the hand in power grip and precision handling: an electromyographic study. J Bone Joint Surg Am 52:853-867.
34. Maier MA, Hepp-Reymond MC (1995) EMG activation patterns during force production in precision grip. I. Contribution of 15 finger muscles to isometric force. Exp Brain Res 103:108-122.
35. Maier MA, Bennett KM, Hepp-Reymond MC, Lemon RN (1993) Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. J Neurophysiol 69:772-785.
36. Maier MA, Perlmutter SI, Fetz EE (1998) Response patterns and force relations of monkey spinal interneurons during active wrist movement. J Neurophysiol 80:2495-2513.
37. Mason CR, Gomez JE, Ebner TJ (2001) Hand synergies during reach-to-grasp. J Neurophysiol 86:2896-2910.
38. Mason CR, Theverapperuma LS, Hendrix CM, Ebner TJ (2004) Monkey hand postural synergies during reach-to-grasp in the absence of vision of the hand and object. J Neurophysiol 91:2826-2837.
39. McCurdy ML, Hamm TM (1992) Recurrent collaterals of motoneurons projecting to distal muscles in the cat hindlimb. J Neurophysiol 67:1359-1366.
40. McKiernan BJ, Marcario JK, 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 80:1961-1980.
41. Mewes K, Cheney PD (1991) Facilitation and suppression of wrist and digit muscles from single rubromotoneuronal cells in the awake monkey. J Neurophysiol 66:1965-1977.
42. Moritz CT, Lucas TH, Perlmutter SI, Fetz EE (2007) Forelimb movements and muscle responses evoked by microstimulation of cervical spinal cord in sedated monkeys. J Neurophysiol 97:110-120.
43. Muir RB, Lemon RN (1983) Corticospinal neurons with a special role in precision grip. Brain Res 261:312-316.
44. Mussa-Ivaldi FA, Giszter SF, Bizzi E (1994) Linear combinations of primitives in vertebrate motor control. Proc Natl Acad Sci U S A 91:7534-7538.
45. Napier JR (1956) The prehensile movements of the human hand. J Bone Joint Surg Br 38:902-913.
46. Overduin SA, d'Avella A, Roh J, Bizzi E (2008) Modulation of muscle synergy recruitment in primate grasping. J Neurosci 28:880-892.
47. Perlmutter SI, Maier MA, Fetz EE (1998) Activity of spinal interneurons and their effects on forearm muscles during voluntary wrist movements in the monkey. J Neurophysiol 80:2475-2494.
48. Poliakov AV, Schieber MH (1998) Multiple fragment statistical analysis of post-spike effects in spike-triggered averages of rectified EMG. J Neurosci Methods 79:143-150.
49. Porter R, Lemon R (1993) Corticospinal function and voluntary movement. Oxford: Oxford UP.
50. Ralston DD, Ralston HJ 3rd (1985) The terminations of corticospinal tract axons in the macaque monkey. J Comp Neurol 242:325-337.
51. Rathelot JA, Strick PL (2009) Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci U S A 106:918-923.
52. Riddle CN, Baker SN (2010) Convergence of pyramidal and medial brain stem descending pathways onto macaque cervical spinal interneurons. J Neurophysiol 103:2821-2832.
53. Riddle CN, Edgley SA, Baker SN (2009) Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J Neurosci 29:4993-4999.
54. Robinson FR, Houk JC, Gibson AR (1987) Limb specific connections of the cat magnocellular red nucleus. J Comp Neurol 257:553-577.
55. Saltiel P, Wyler-Duda K, D'Avella A, Tresch MC, Bizzi E (2001) Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J Neurophysiol 85:605-619.
56. Santello M, Flanders M, Soechting JF (1998) Postural hand synergies for tool use. J Neurosci 18:10105-10115.
57. Schieber MH, Rivlis G (2005) A spectrum from pure post-spike effects to synchrony effects in spike-triggered averages of electromyographic activity during skilled finger movements. J Neurophysiol 94:3325-3341.
58. Shim JK, Latash ML, Zatsiorsky VM (2005a) Prehension synergies in three dimensions. J Neurophysiol 93:766-776.
59. Shim JK, Latash ML, Zatsiorsky VM (2005b) Prehension synergies: trial-to-trial variability and principle of superposition during static prehension in three dimensions. J Neurophysiol 93:3649-3658.
60. Sinkjaer T, Miller L, Andersen T, Houk JC (1995) Synaptic linkages between red nucleus cells and limb muscles during a multi-joint motor task. Exp Brain Res 102:546-550.
61. Smith AM (1981) The coactivation of antagonist muscles. Can J Physiol Pharmacol 59:733-747.
62. Takei T, Seki K (2008) Spinomuscular coherence in monkeys performing a precision grip task. J Neurophysiol 99:2012-2020.
63. Takei T, Seki K (2009) Post-spike effects of spinal interneurons on hand muscles in monkeys performing a precision grip. Soc Neurosci Abstr 35:10.19.
64. Theverapperuma LS, Hendrix CM, Mason CR, Ebner TJ (2006) Finger movements during reach-to-grasp in the monkey: amplitude scaling of a temporal synergy. Exp Brain Res 169:433-448.
65. Tresch MC, Saltiel P, Bizzi E (1999) The construction of movement by the spinal cord. Nat Neurosci 2:162-167.
66. Zatsiorsky VM, Gao F, Latash ML (2003) Prehension synergies: effects of object geometry and prescribed torques. Exp Brain Res 148:77-87.
67. Zhang W, Scholz JP, Zatsiorsky VM, Latash ML (2008) What do synergies do? Effects of secondary constraints on multidigit synergies in accurate force-production tasks. J Neurophysiol 99:500-513.