Differential responses of fast- and slow-conducting pyramidal tract neurons to changes in accuracy demands during locomotion

Journal of Physiology

Volumn 591, Issue 10, 2013, Pages 2647-2666

  Stout, Erik E ^a   Beloozerova, Irina N ^a  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CAT; CONTROLLED STUDY; FEMALE; LOCOMOTION; MALE; MOTOR CORTEX; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; STANDING; TASK PERFORMANCE; WALKING;

ANIMALS; CATS; FEMALE; LOCOMOTION; MALE; NEURONS; PYRAMIDAL TRACTS;

EID: 84877828588     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.232538     Document Type: Article

References (100)

1. Amos A, Armstrong DM & Marple-Horvat DE (1990). Changes in the discharge patterns of motor cortical neurons associated with volitional changes in stepping in the cat. Neuroscience Letters 109, 107-112 .
2. Antal M (1984). Termination areas of corticobulbar and corticospinal fibres in the rat. J Hirnforsch 25, 647-659.
3. Armstrong DM & Drew T (1984a). Discharges of pyramidal tract and other motor cortical neurones during locomotion in the cat. J Physiol 346, 471-495.
4. Armstrong DM & Drew T (1984b). Locomotor-related neuronal discharges in cat motor cortex compared with peripheral receptive fields and evoked movements. J Physiol 346, 497-517.
5. Armstrong DM & Drew T (1985). Electromyographic responses evoked in muscles of the forelimb by intracortical stimulation in the cat. J Physiol 367, 309-326.
6. Baranyi A, Szente MB & Woody CD (1993). Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. II. Membrane parameters, action potentials, current-induced voltage responses and electrotonic structures. J Neurophysiol 69, 1865-1879.
7. Bastian AJ, Zackowski KM & Thach WT (2000). Cerebellar ataxia: torque deficiency or torque mismatch between joints? J Neurophysiol 83(5): 3019-3030.
8. Batshelet E (1981). Circular Statistics in Biology . Academic Press, New York .
9. Beer RF, Dewald JP & Rymer WZ (2000). Deficits in the coordination of multijoint arm movements in patients with hemiparesis: evidence for disturbed control of limb dynamics. Exp Brain Res 131(3): 305-319.
10. Beloozerova IN & Sirota MG (1985). Activity of neurons of the motosensory cortex during natural locomotion in the cat. Neirofiziologia 17, 406-408.
11. Beloozerova IN & Sirota MG (1988). The role of motor cortex in control of locomotion. In Stance and Motion. Facts and Concepts, ed. Gurfinkel VS, Ioffe ME, Massion J & Roll JP, pp. 163-176, Plenum Press, New York .
12. Beloozerova IN & Sirota MG (1993a). The role of the motor cortex in the control of accuracy of locomotor movements in the cat. J Physiol 461, 1-25.
13. Beloozerova IN & Sirota MG (1993b). The role of the motor cortex in the control of vigour of locomotor movements in the cat. J Physiol 461, 27-46.
14. Beloozerova IN, Sirota MG & Swadlow HA (2003). Activity of different classes of neurons of the motor cortex during locomotion. J Neurosci 23, 1087-1097.
15. Beloozerova IN, Sirota MG, Orlovsky GM & Deliagina TG (2005). Activity of pyramidal tract neurons in the cat during postural corrections. J Neurophysiol 93, 1831-1844.
16. Beloozerova IN, Wettenstein P & Sirota MG (2007). Integration of motor and visual information in the motor cortex during locomotion. Program No. 292.16; 2007 Neuroscience Meeting Planner . Society for Neuroscience, San Diego, CA, USA . Online.
17. Beloozerova IN, Farrell BJ, Sirota MG & Prilutsky BI (2010). Differences in movement mechanics, electromyographic, and motor cortex activity between accurate and non-accurate stepping. J Neurophysiol 103, 2285-2300.
18. Bishop PO, Jeremy D & Lance JW (1953). Properties of pyramidal tract. J Physiol 5, 537-549.
19. Bishop PO, Burke W & Davis R (1962). The identification of single units in central visual pathways. J Physiol 162, 409-431.
20. Brookhart JM & Morris RE (1948). Antidromic potential recordings from the bulbar pyramid of the cat. J Neurophysiol 11, 387-398.
21. Brookhart JM (1952). A study of corticospinal activation of motoneurones. Res Publ Ass Nerv Ment Dis 30, 157-173.
22. Calvin WH & Sypert GW (1976). Fast and slow pyramidal tract neurons: An intracellular analysis of their contrasting repetitive firing properties in the cat. J Physiol 39, 420-434.
23. Canedo A (1997). Primary motor cortex influences on the descending and ascending systems. Progress in Neurobiol 51, 287-335.
24. Chambers WWV & Liu CN (1957). Corticospinal tract of the cat. An attempt to correlate the pattern of degeneration with deficit in reflex act following neocortical lesions. J Com Neurol 108, 23-26.
25. Cheney PD & Fetz EE (1980). Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44, 773-791.
26. Crammond DJ & Kalaska JF (1994) Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. J Neurophysiol 71, 1281-1284.
27. Criado JM, de la Fuente A, Heredia M, Riolobos AS & Yajeya J (1997). Electrophysiological study of prefrontal neurones of cats during a motor task. Pflugers Arch 434, 91-96.
28. Deschênes M & Labelle A (1979). Differential distribution of spines on the apical dendrites of slow and fast pyramidal tract cells in the cat. Brain Res 164, 309-313.
29. Deschênes M, Labelle A & Landry P (1979). Morphological characterization of slow and fast pyramidal tract cells in the cat. Brain Res 178(2-3): 251-274.
30. Deschênes M, Landry P & Clercq M (1982). A reanalysis of the ventrolateral input in slow and fast pyramidal tract neurons of the cat motor cortex. Neuroscience 7, 2149-2157.
31. Dounskaia N (2005). The internal model and the leading joint hypothesis: implications for control of multi-joint movements. Exp Brain Res 166, 1-16.
32. Dounskaia N, Wisleder D & Johnson T (2005). Influence of biomechanical factors on substructure of pointing movements. Exp Brain Res 164, 505-516.
33. Drew T (1993). Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. J Neurophysiol 70, 179-199.
34. Drew T, Andujar JE, Lajoie K & Yakovenko S (2008). Cortical mechanisms involved in visuomotor coordination during precision walking. Brain Res Rev 57, 199-211.
35. Drew T & Doucet S (1991). Application of circular statistics to the study of neuronal discharge during locomotion. J Neurosci Methods 38, 171-181.
36. Drew T, Jiang W, Kably B & Lavoie S (1996). Role of the motor cortex in the control of visually triggered gait modifications. Can J Physiol Pharmacol 74, 426-442.
37. Dyachkova LN, Kostyuk PG & Pogorelaya NC (1971). An electron microscopic analysis of pyramidal tract termination nn the spinal cord of the cat. Exp Brain Res 12, 105-119.
38. Efron B & Tibshirani RJ (1993). An Introduction to the Bootstrap . Chapman & Hall, New York .
39. Evarts EV (1965). Relation of discharge frequency to conduction velocity in pyramidal tract neurons. J Neurophysiol 28, 216-228.
40. Fetz EE & Cheney PD (1980). Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J Neurophysiol 44(4): 751-772.
41. Fisher NI (1993). Statistical Analysis of Circular Data. Cambridge University Press, Cambridge, MA, USA .
42. Friel KM, Drew T & Martin JH (2007). Differential activity-dependent development of corticospinal control of movement and final limb position during visually guided locomotion. J Neurophysiol 97, 3396-3406.
43. Fromm C & Evarts EV (1977). Relation of motor cortex neurons to precisely controlled and ballistic movements. Neurosci Lett 5, 259-265.
44. Fromm C & Evarts EV (1981). Relation of size and activity of motor cortex pyramidal tract neurons during skilled movements in the monkey. J Neurosci 1, 453-460.
45. Fromm C, Wise SP & Evarts EV (1984). Sensory response properties of pyramidal tract neurons in the precentral motor cortex and postcentral gyrus of the rhesus monkey. Exp Brain Res 54, 177-185.
46. Fuller JH & Schlag J (1976). Determination of antidromic excitation by the collision test: problems of interpretation. Brain Res 122, 283-298.
47. Galloway JC & Koshland GF (2002). General coordination of shoulder, elbow and wrist dynamics during multijoint arm movements. Exp Brain Res 142, 163-180.
48. Ghosh S (1997a). Identification of motor areas of the cat cerebral cortex based on studies of cortical stimulation and corticospinal connections. J Comp Neurol 380, 191-214.
49. Ghosh S (1997b). Comparison of the cortical connections of areas 4 gamma and 4 delta in the cat cerebral cortex. J Comp Neurol 388, 371-396.
50. Ghosh S & Porter R (1988). Morphology of pyramidal neurones in monkey motor cortex and the synaptic actions of their intracortical axon collaterals. J Physiol 400, 593-615.
51. Gomez JE, Fu Q, Flament D & Ebner TJ (2000). Representation of accuracy in the dorsal premotor cortex. Eur J Neurosci 12, 3748-3760.
52. Goodale MA, Pelisson D & Prablanc C (1986). Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature 320, 748-750.
53. Gordon J, Ghilardi MF & Ghez C (1994). Accuracy of planar reaching movements. I. Independence of direction and extent variability. Exp Brain Res 99, 97-111.
54. Grillner S & Rossignol S (1978). On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res 146, 269-277.
55. Hassler R & Muhs-Clement K (1964). Architektonischer Aufbau des sensorimotorischen und parietalen Cortex der Katz. J Hirnforsch 6, 377-420.
56. Hoff EC & Hoff HE (1934). Spinal terminations of the projection fibers from the motor cortex of primates. Brain 57, 454-474.
57. Humphrey DR & Corrie WS (1978). Properties of pyramidal tract neuron system within a functionally defined subregion of primate motor cortex. J Neurophysiol 41, 216-243.
58. Jones EG, Coulter JD & Hendry SH (1978). Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol 181, 291-347.
59. Kakei S, Hoffman DS & Strick PL (1999). Muscle and movement representation in the primary motor cortex. Science 285, 2136-2139.
60. Lacroix S, Havton LA, McKay H, Yang H, Brant A, Roberts J & Tuszynski MH (2004). Bilateral corticospinal projections arise from each motor cortex in the macaque monkey: a quantitative study. J Comp Neurol 473, 147-161.
61. Lassek AM & Rasmussen GL (1940). A comparative fiber and numerical analysis of the pyramidal tract. J Comp Neurol 72, 417-428.
62. Lemon RN & Porter R (1993). Corticospinal Function and Voluntary Movement . Clarendon Press, Oxford .
63. Liddell EGT & Phillips CG (1944). Pyramidal section in the cat. Brain 67, 1-9.
64. Lloyd DPC (1941). The spinal mechanism of the pyramidal system in cats. J Neurophysiol 4, 525-546.
65. Marconi B, Genovesio A, Battaglia-Mayer A, Ferraina S, Squatrito S, Molinari M, Lacquaniti F & Caminiti R (2001). Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb Cortex 11, 513-527.
66. Marlinski V, Nilaweera WU, Zelenin PV, Sirota MG & Beloozerova IN (2012). Signals from the ventrolateral thalamus to the motor cortex during locomotion. J Neurophysiol 107, 455-472.
67. Marple-Horvat DE, Amos AJ, Armstrong DM & Criado JM (1993). Changes in the discharge patterns of cat motor cortex neurones during unexpected perturbations of on-going locomotion. J Physiol 462, 87-113.
68. Martin JH & Ghez C (1993). Differential impairments in reaching and grasping produced by local inactivation within the forelimb representation of the motor cortex in the cat. Exp Brain Res 94, 429-443.
69. Matsunami K & Hamada I (1980). Antidromic latency of the monkey pyramidal tract neuron related to ipsilateral hand movements. Neurosci Let 16, 245-249.
70. Messier J & Kalaska JF (1999). Comparison of variability of initial kinematics and endpoints of reaching movements. Exp Brain Res 125, 139-152.
71. Metz GA & Whishaw IQ (2002). Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 115, 169-179.
72. Mihaltchev P, Archambault PS, Feldman AG & Levin MF. (2005). Control of double-joint arm posture in adults with unilateral brain damage. Exp Brain Res 163(4): 468-486.
73. Myasnikov AA, Dykes RW & Leclerc SS (1997). Correlating cytoarchitecture and function in cat primary somatosensory cortex: the challenge of individual differences. Brain Res 750, 95-108.
74. Nieoullon A & Rispal-Padel L (1976). Somatotopic localization in cat motor cortex. Brain Res 105, 405-422.
75. Novak KE, Miller LE & Houk JC (2002). The use of overlapping submovements in the control of rapid hand movements. Exp Brain Res 144, 351-364.
76. Prablanc C & Martin O (1992). Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67, 455-469.
77. Prilutsky BI, Sirota MG, Gregor RJ & Beloozerova IN (2005). Quantification of motor cortex activity and full-body biomechanics during unconstrained locomotion. J Neurophysiol 94, 2959-2969.
78. Pryor K (1975). Lads before the Wind . Harper and Row, New York .
79. Reitboeck HJ (1983). Fiber microelectrodes for electrophysiological recordings. J Neurosci Methods 8, 249-262.
80. Rosenzweig ES, Brock JH, Culbertson MD, Lu P, Moseanko R, Edgerton VR, Havton LA & Tuszynski MH (2009). Extensive spinal decussation and bilateral termination of cervical corticospinal projections in rhesus monkeys. J Comp Neurol 513, 151-163.
81. Sakai H (1982). Morphological properties of fast and slow PT cells in the cat revealed by intracellular pressure injection of HRP. Nihon Seirigaku Zassh 44(5), 199-204. Japanese
82. Sirota MG, Swadlow HA & Beloozerova IN (2005). Three channels of corticothalamic communication during locomotion. J Neurosci 25, 5915-5925.
83. Skinner BF (1938). The Behavior of Organisms . Appleton-Century-Crofts Inc, New York .
84. Soechting JF & Flanders M (1989). Errors in pointing are due to approximations in sensorimotor transformations. J Neurophysiol 62, 595-608.
85. Stout EE & Beloozerova IN (2010). The role of slow-conducting pyramidal tract neurons in precision stepping. Program No. 290.15. 2010 Neuroscience Meeting Planner. Society for Neuroscience, San Diego, CA, 2010. Online.
86. Stout EE & Beloozerova IN (2012). Pyramidal tract neurons receptive to different forelimb joints act differently during locomotion. J Neurophysiol 107, 1890-1903.
87. Takahashi K (1965). Slow and fast groups of pyramidal tract cells and their respective membrane properties. J Neurophysiol 28, 908-924.
88. Tanji J, Taniguchi K & Fukushima K (1978). Relation of slowly conducting pyramidal tract neurons to specific aspects of forearm movement. J Physiol (Paris) 74, 293-296.
89. Towe AL., Patton HD & Kennedy TT (1963). Properties of the pyramidal system in the cat. Exp Neurol, 8, 220-238.
90. Towe AL, Whitehorn D & Nyquist JK (1968). Differential activity among wide-field neurons of the cat postcruciate cerebral cortex. Exp Neurol 20, 497-521.
91. 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 fur Hirnforschung 23, 257-269.
92. Trendelenburg W (1911). Untersuchungen uber reizlose vorubergehende Aussaltung am Zentralnervensystem. III. Die extermitaten Region der Grosshirninde. Pflugers Archiv 137, 515-544.
93. Tsukahara N, Fuller DR & Brooks VB (1968). Collateral pyramidal influences on the corticorubrospinal system. J Neurophysiol 31(3): 467-484.
94. Udo M, Kamei H, Matsukawa K & Tanaka K (1982). Interlimb coordination in cat locomotion investigated with perturbation. II. Correlates in neuronal activity of Deiter's cells of decerebrate walking cats. Exp Brain Res 46, 438-447.
95. Vicario DS, Martin JH & Ghez C (1983). Specialized subregions in the cat motor cortex: a single unit analysis in the behaving animal. Exp Brain Res 51, 351-367.
96. Vigneswaran G, Kraskov A & Lemon RN (2011). Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification. J Neurosci 31, 14235-14242.
97. Widajewicz W, Kably B & Drew T (1994). Motor cortical activity during voluntary gait modifications in the cat. II. Cells related to the hindlimbs. J Neurophysiol 72, 2070-2089.
98. Wiesendanger M (1981). The pyramidal tract. Its structure and function. In Handbook of Behavioral Neurobiology 5, 401-491.
99. Wise SP, Di Pellegrino G & Boussaoud D (1992). Primate premotor cortex: dissociation of visuomotor from sensory signals. J Neurophysiol 68, 969-972.
100. Woodworth RS (1899). The accuracy of voluntary movement. Columbia University Press, New York .