Effects of fatigue on the catchlike property in a turtle hindlimb muscle

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 189, Issue 12, 2003, Pages 857-866

  Callister, R J ^a   Reinking, R M ^b,c   Stuart, D G ^b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Catchlike property; Motoneurons; Muscle fatigue; Segmental motor control; Turtle

Indexed keywords

ACTION POTENTIAL; ANIMAL; ARTICLE; BIOLOGICAL MODEL; ELECTROSTIMULATION; HINDLIMB; INNERVATION; MOTONEURON; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE ISOMETRIC CONTRACTION; PHYSIOLOGY; SKELETAL MUSCLE; TURTLE;

ACTION POTENTIALS; ANIMALS; ELECTRIC STIMULATION; HINDLIMB; ISOMETRIC CONTRACTION; MODELS, BIOLOGICAL; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; TURTLES;

EID: 0346403400     PISSN: 03407594     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00359-003-0459-2     Document Type: Article

References (94)

1. Adrian ED, Bronk DW (1929) The discharge impulses in motor nerve fibres. Part II. The frequency of discharge in reflex and voluntary contractions. J Physiol (Lond) 67:119-151
2. Allen DG, Westerblad H (2001) Role of phosphate and calcium stores in muscle fatigue. J Physiol 536:657-665
3. Allen DG, Westerblad H, Lannergren J (1995) The role of interstitial acidosis in muscle fatigue. In: Gandevia SC, Enoka RM, McComas AJ, Stuart DG, Thomas CK (eds) Fatigue-neural and muscular mechanisms. Plenum, New York, pp 57-68
4. Bevan L, Laouris Y, Reinking RM, Stuart DG (1992) The effect of the stimulation pattern on the fatigue of single motor units in adult cats. J Physiol (Lond) 449:85-108
5. Biewener AA (2002) Future directions for the analysis of musculoskeletal design and locomotor performance. J Morphol 252:38-51
6. Binder-Macleod SA (1995) Variable-frequency stimulation patterns for the optimization of force during muscle fatigue: muscle wisdom and the catch-like property. Adv Exp Med Biol 384:227-40
7. Binder-Macleod SA, Barker CB (1991) Use of a catch-like property of human skeletal muscle to reduce fatigue. Muscle Nerve 14:850-857
8. Binder-Macleod SA, Barrish WJ (1992) Force response of rat soleus muscle to variable-frequency train stimulation. J Neurophysiol 68:1068-1078
9. Binder-Macleod SA, Lee SC (1996) Catchlike property of human muscle during isovelocity movements. J Appl Physiol 80:2051-2059
10. Botterman BR, Iwamoto GA, Gonyea J (1986) Gradation of isometric tension by different activation rates in motor units of cat flexor carpi radialis muscle. J Physiol (Lond) 56:494-506
11. Brown IE, Loeb GE (2000) Measured and modeled properties of mammalian skeletal muscle: IV. Dynamics of activation and deactivation. J Muscle Res Cell Motil 21:33-47
12. Brown IE, Loeb GE (2001) Toward the ultimate skeletal muscle model. Soc Neurosci Abstr 31:167.9
13. Buchanan JT, Kasicki S (1995) Activities of spinal neurons during brain stem-dependent fictive swimming in lamprey. J Neurophysiol 73:80-87
14. Burke RE (1981) Motor units: anatomy, physiology, and functional organization. In: Brookhart JM, Mountcastle VB (eds) Handbook of physiology, section 1, vol II, pt 1. The nervous system: motor control (Brooks VB, vol ed). Am Physiol Soc, Bethesda, pp 345-422
15. Burke RE, Rudomin P, Zajac FE (1970) Catch property in single mammalian motor units. Science 168:122-124
16. Burke RE, Rudomin P, Zajac FE (1976) The effect of activation history on tension production by individual muscle units. Brain Res 109:515-529
17. Burkholder TJ, Lieber RL (2001) Sarcomere length operating range of vertebrate muscles during movement. J Exp Biol 204:1529-1536
18. Buss RR, Bourque CW, Drapeau P (2003) Membrane properties related to the firing behavior of zebrafish motoneurons. J Neurophysiol 89:657-664
19. Callister RJ, Callister R, Peterson EH (1989) Histochemical classification of neck and limb muscle fibers in a turtle, Pseudemys scipla: a study using microphotometry and cluster analysis techniques. J Morphol 199:269-286
20. Callister RJ, Laidlaw DH, Reinking RM, Stuart DG (1992) The catch-like property of turtle muscle: effect of shortening, lengthening, and fatiguing isometric contractions. Soc Neurosci Abstr 18:1559
21. Callister RJ, Laidlaw DH, Stuart DG (1995) A commentary on the segmental motor system of the turtle: implications for the study of its cellular mechanisms and interactions. J Morphol 225:213-227
22. Cheng EJ, Brown IE, Loeb GE (2000) Virtual muscle: a computational approach to understanding the effects of muscle properties on motor control. J Neurosci Methods 101:117-130
23. 2+] in the development of low frequency fatigue in mouse single muscle fibres. J Physiol (Lond) 491:813-824
24. Cooper S, Eccles JC (1930) The isometric responses of mammalian muscles. J Physiol (Lond) 69:377-385
25. Curtin NA, Edman KA (1996) Force-velocity relation for frog muscle fibres: effects of moderate muscle fatigue and of intracellular acidosis. J Physiol (Lond) 475:483-494
26. Ding J, Wexler AS, Binder-Macleod SA (2002) A mathematical model that predicts the force-frequency relationship of human skeletal muscle. Muscle Nerve 26:477-485
27. Ding J, Storaska JA, Binder-Macleod SA (2003) Effect of potentiation on the catchlike property of human skeletal muscles. Muscle Nerve 27:312-319
28. 2+ movements in single barnacle muscle fibres. J Muscle Cell Motil 7:18-24
29. Eccles JC, Sherrington CS (1930) Numbers and contraction values of individual motor units examined in some muscles of the limb. Proc Roy Soc (Lond) B 106:326-357
30. Edgerton VR, Bodine-Fowler S. Roy RR, Ishihara A, Hodgson A (1996) Neuromuscular adaptation. In: Rowell LB, Shepherd JT (eds) Handbook of physiology, section 12. Exercise: regulation and integration of multiple systems. Oxford University Press, New York, pp 54-88
31. Ekeberg O, Grillner S (1999) Simulations of neuromuscular control in lamprey swimming. Phil Trans R Soc Lond B Biol Sci 354:895-902
32. Enoka RM, Fuglevand AJ (2001) Motor unit physiology: some unresolved issues. Muscle Nerve 24:4-17
33. Garland SJ, Griffin L (1999) Motor unit double discharges: statistical anomaly or functional entity? Can J Appl Physiol 24:113-130
34. Garland T, Carter PA (1994) Evolutionary physiology. Ann Rev Physiol 56:579-621
35. George DT, Binder-Macleod SA, Delosso TN, Santamore WP (1997) Variable-frequency train stimulation of canine latissimus dorsi muscle during shortening contractions. J Appl Physiol 83:994-1001
36. Gillis GB, Biewener AA (2001) Hindlimb muscle function in relation to speed and gait: in vivo patterns of strain and activation in a hip and knee extensor of the rat (Rattus norvegicus). J Exp Biol 204:2717-2731
37. Gorassini MA, Bennett DJ, Eken T, Kiehn O, Hultborn H (1999) Activation patterns of hindlimb motoneurons in the awake rat and their relation to motoneuron intrinsic properties. J Neurophysiol 82:709-717
38. Heckman CJ, Weytjens JL, Loeb GE (1992) Effect of velocity and mechanical history on the forces of motor units in the cat medial gastrocnemius muscle. J Neurophysiol 68:1503-1515
39. Hennig R, Lómo T (1985) Firing patterns of motor units in normal rats. Nature 314:164-166
40. Hoffer JA, Sugano N, Loeb GE, Marks WB, O'Donovan MJ, Pratt CA (1987) Cat hindlimb motoneurons during locomotion. II. Normal activity patterns. J Neurophysiol 57:530-553
41. Hornby TG, McDonagh JC, Reinking RM, Stuart DG (2002) Electrophysiological properties of spinal motoneurons in the adult turtle. J Comp Physiol A 188:397-408
42. Hounsgaard J, Kiehn O, Mintz I (1988) Response properties of motoneurones in a slice preparation of the turtle spinal cord. J Physiol (Lond) 398:575-589
43. Hoyle G (1983) Forms of modulatable tension in skeletal muscles. Comp Biochem Physiol A 76:203-210
44. Johnston IA (1985) Sustained force development: specializations and variation among the vertebrates. J Exp Biol 115:239-251
45. Josephson R (1997) Power output from a flight muscle of the bumblebee Bombus terrestris. II. Characterisation of the parameters affecting power output. J Exp Biol 200:1227-1239
46. Kebaetse MB, Lee SC, Binder-Macleod SA (2001) A novel stimulation pattern improves performance during repetitive dynamic contractions. Muscle Nerve 24:744-52
47. Kebaetse MB, Turner AE, Binder-Macleod SA (2002) Effects of stimulation frequencies and patterns on performance of repetitive, nonisometric tasks J Appl Physiol 92:109-116
48. Laidlaw DH, Callister RC, Stuart DG (1995) Fiber-type composition of hindlimb muscles in the turtle, Pseudemys (Tachemys) scripta elegans. J Morphol 225:193-211
49. Laouris Y, Stuart, DG (1993) Multiple neuromuscular-strategies for counteracting muscle fatigue. In: Sargeant AJ, Kernell D (eds). Neuromuscular fatigue. North-Holland, Amsterdam, pp 181-183
50. Laouris Y, Bevan L, Reinking RM, Stuart DG (1991) Changes in motoneuron discharge variability during prolonged activation with extracellular stimulation: possible implications for fatigue. In: Atlan G, Beliveau L, Bouissou P (eds) Muscle fatigue: biochemical and physiological aspects. Masson, Paris, p 242
51. Lee SC, Binder-Macleod SA (2000) Effects of activation frequency on dynamic performance of human fresh and fatigued muscles. J Appl Physiol 88:2166-2175
52. Lee SC, Becker CN, Binder-Macleod SA (2000) Activation of human quadriceps femoris muscle during dynamic contractions: effects of load on fatigue. J Appl Physiol 89:926-36
53. Liddell EGT, Sherrington CS (1925) Recruitment and some other forms of reflex inhibition. Proc R Soc Lond B Biol Sci 97:267-283
54. Lindstedt SL, Reich TE, Keim P, LaStayo PC (2002) Do muscles function as adaptable locomotor springs? J Exp Biol 205:2211-2216
55. Lou F, Curtin NA, Woledge RC (1999) Elastic energy storage and release in white muscle from dogfish Scyliorhinus canicula. J Exp Biol 202:135-142
56. McDonagh JC, Gorman RB, Gilliam EE, Hornby TG, Reinking RM, Stuart DG (1998) Properties of spinal motoneurons and interneurons in the adult turtle: provisional classification by cluster analysis. J Comp Neurol 400:544-570
57. McLean DL, McDearmid JR, Sillar KT (2003) Induction of a non-rhythmic motor pattern by nitric oxide in hatchling Rana temporaria embryos. J Exp Biol 204:1307-1317
58. Moll EO, Legler JM (1971) The life history of a neotropical slider turtle, Pseudemys scripta (Schoepff), in Panama. Bull Los Angeles County Mus Nat Hist Sci 11:1-102
59. Nasledov GA, Katina IE, Zhitnikova IuV (2002) Characteristics of functioning of electromechanical coupling in striated muscles of higher and lower vertebrates (in Russian). Biofizika 47:716-27
60. 2+ release channels between rabbit and frog skeletal muscles. Mol Cell Biochem 190:191-201
61. Orlovsky GN, Deliagina TG, Grillner S (1999) Neuronal control of locomotion - from mollusc to man. Oxford University Press, New York, 322 pp
62. Paggett KC, Gupta V, McClellan AD (1998) Adaptive variations of undulatory behaviors in larval lamprey: comparison of swimming and burrowing. Exp Brain Res 119:213-223
63. Parmiggiani F, Stein RB (1981) Nonlinear summation of contractions in cat muscles. II. Later facilitation and stiffness changes. J Gen Physiol 78:295-311
64. Perreault EJ, Day SJ, Hulliger M. Heckman CJ, Sandercock TG (2003) Summation of forces from multiple motor units in the cat soleus muscle. J Neurophysiol 89:738-744
65. Person RS (1974) Rhythmic activity of a group of human motoneurones during contraction of a muscle. EEG Clin Neurophysiol 36:585-595
66. Piazzesi G, Linari M, Reconditi M, Vanzi F, Lombardi V (1997) Cross-bridge detachment and attachment following a step stretch imposed on active single frog muscle fibres. J Physiol (Lond) 498:3-15
67. Powers RK, Binder MD (2000) Relationship between the time course of the afterhyperpolarization and discharge variability in cat spinal motoneurones. J Physiol (Lond) 528:131-150
68. Proske U, Morgan DL, Gregory JE (1993) Thixotropy in skeletal muscle and in muscle spindles: a review. Prog Neurobiol 41:705-721
69. Reinking RM, Stuart DG (1974) A servo-regulated electromagnetic device for muscle stretch and vibration. Am J Phys Med 53: 1-28
70. Reinking RM, Stuart DG (1993a) Structured programming for data acquisition and system calibration using LabVIEW. In: Gross R, Duncan M (eds) SEAM '92 Conf MacSciTech, Worcester, MA, CD-ROM
71. Reinking RM, Stuart DG (1993b) LabVIEW structured programming code. In: Gross R, Duncan M (eds) SEAM'92 Conf, MacSciTech, Worcester MA, CD_ROM
72. Robertson GA, Stein PSG (1998) Synaptic control of hindlimb motoneurons during three forms of the fictive scratch reflex in the turtle. J Physiol (Lond) 404:101-128
73. Rome LC (1998) Some advances in integrative muscle physiology. Comp Biochem Physiol B Biochem Mol Biol 20:51-72
74. Rome LC, Lindstedt SL (1998) The quest for speed: muscles built for high-frequency contractions. News Physiol Sci 13: 261-268
75. Samosudova NV, Lebedinskaya II, Nasledov GA, Skorobovichuk NF (1987) Ultrastructural organisation and the sites of calcium localization in the lamprey striated muscle. Gen Physiol Biophys 6:479-489
76. Sandercock TG, Heckman CJ (1997) Doublet potentiation during eccentric and concentric contractions of cat soleus muscle. J Appl Physiol 82:1219-1228
77. Seidel ME, Smith HM (1986) Chrysemys, Pseudemys, Trachemys (Testudines: emydidae): did Agaswsiz have it right? Herpetol 42:242-248
78. Shupliakov O, Wallen P, Grillner S (1992) Two types of motoneurons supplying dorsal fin muscles in lamprey and their activity during fictive locomotion. J Comp Neurol 321:112-123
79. Silber G (1977) A behavioral study of backflipping and backstroking in the turtle. Senior Honors Thesis, Washington University, St. Louis, MO, USA
80. Stein PSG (1999) Central pattern generators and interphyletic awareness. Prog Brain Res 123:259-271
81. Stein PSG, McCullough ML, Currie SN (1998) Spinal motor patterns in the turtle. Ann NY Acad Sci 860:142-154
82. Stein RB, Parmiggiani F (1979) Optimal motor patterns for activating mammalian muscle. Brain Res 175:372-376
83. Stevens ED (1996) The pattern of stimulation influences the amount of oscillatory work done by frog muscle. J Physiol (Lond) 494:279-285
84. Stephenson DG, Lamb GD, Stephenson GMM, Fryer MW (1995) In: Gandevia SC, Enoka RM, McComas AJ, Stuart DG, Thomas CK (eds). Fatigue - neural and muscular mechanisms. Plenum, New York, pp 45-56
85. Stephenson DG, Lamb GD, Stephenson GM (1998) Events of the excitation-contraction-relaxation (E-C-R) cycle in fast- and slow-twitch mammalian muscle fibres relevant to muscle fatigue. Acta Physiol Scand 162:229-245
86. Stokes D, Josephson R (1994) Contractile properties of a high-frequency muscle from a crustacen - contraction kinetics. J Exp Biol 187:275-293
87. Stuart DG, Callister JC (1993) Afferent and spinal reflex aspects of muscle fatigue. In: Sargeant AJ, Kernell D (eds) Neuromuscular fatigue. North-Holland, Amsterdam pp 169-180
88. Stuart DG, McDonagh JC, Pierce PA, Dalponte D, Abraham KA (1998) Turtle non-twitch muscle fibers and their potential innervation. Soc Neurosci Abstr 24:914
89. Svirskis G, Rinzel J (2000) Influence of temporal correlation of synaptic input on the rate and variability of firing in neurons. Biophys J 79:629-37
90. Tameyasu T, Sugi H (1999) The series elastic component and the force-velocity reaction in the anterior byssal retractor muscle of Mytilus edulis during active and catch contractions. J Exp Biol 64:497-510
91. i in the slowing of relaxation in fatigued fibres from mouse muscle. J Physiol (Lond) 434:323-336
92. Westerblad H, Allen DG, Lannergren J (2002) Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci 17:17-21
93. Williams T, Grillner S, Smoljaninov V, Wallén P, Kashin S, Rossignol S (1989) Locomotion in lamprey and trout: the relative timing of activation and movement. J Exp Biol 143:559-566
94. Zajac FE, Young JL (1980) Properties of stimulus trains producing maximum tension-time area per pulse from single motor units in medial gastrocnemius muscle of the cat. J Neurophysiol 43:1206-1220