Characterization of muscle spindle afferents in the adult mouse using an in vitro muscle-nerve preparation

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Wilkinson, Katherine A ^a   Kloefkorn, Heidi E ^b   Hochman, Shawn ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; EVOKED RESPONSE; EXTENSOR DIGITORUM LONGUS MUSCLE; IN VITRO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; MUSCLE STRETCHING; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NERVE POTENTIAL; NONHUMAN; ROOM TEMPERATURE; VIBRATION;

ANIMALS; MALE; MICE; MICE, INBRED C57BL; MUSCLE SPINDLES; NEUROMUSCULAR JUNCTION; NEURONS, AFFERENT;

EID: 84862639344     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039140     Document Type: Article

References (71)

1. Mense S, (2008) Muscle pain: mechanisms and clinical significance. Deutsches Arzteblatt International 105: 214-219.
2. Lund JP, Sadeghi S, Athanassiadis T, Caram Salas N, Auclair F, et al. (2010) Assessment of the potential role of muscle spindle mechanoreceptor afferents in chronic muscle pain in the rat masseter muscle. PloS One 5: e11131.
3. Kim GH, Suzuki S, Kanda K, (2007) Age-related physiological and morphological changes of muscle spindles in rats. The Journal of Physiology 582: 525-538.
4. Miwa T, Miwa Y, Kanda K, (1995) Dynamic and static sensitivities of muscle spindle primary endings in aged rats to ramp stretch. Neuroscience Letters 201: 179-182.
5. Winarakwong L, Muramoto T, Soma K, Takano Y, (2004) Age-related changes and the possible adaptability of rat jaw muscle spindles: immunohistochemical and fine structural studies. Archives of Histology and Cytology 67: 227-240.
6. Rosant C, Nagel MD, Perot C, (2007) Aging affects passive stiffness and spindle function of the rat soleus muscle. Experimental Gerontology 42: 301-308.
7. Muller KA, Ryals JM, Feldman EL, Wright DE, (2008) Abnormal muscle spindle innervation and large-fiber neuropathy in diabetic mice. Diabetes 57: 1693-1701.
8. van Deursen RW, Sanchez MM, Ulbrecht JS, Cavanagh PR, (1998) The role of muscle spindles in ankle movement perception in human subjects with diabetic neuropathy. Exp Brain Res 120: 1-8.
9. Edin BB, Vallbo AB, (1990) Dynamic response of human muscle spindle afferents to stretch. Journal of Neurophysiology 63: 1297-1306.
10. Hagbarth KE, Vallbo AB, (1967) Afferent response to mechanical stimulation of muscle receptors in man. Acta Societatis Medicorum Upsaliensis 72: 102-104.
11. Edin BB, (1991) The 'initial burst' of human primary muscle spindle afferents has at least two components. Acta Physiologica Scandinavica 143: 169-175.
12. Kakuda N, Nagaoka M, (1998) Dynamic response of human muscle spindle afferents to stretch during voluntary contraction. The Journal of Physiology 513 (Pt 2): 621-628.
13. Ribot-Ciscar E, Rossi-Durand C, Roll JP, (2000) Increased muscle spindle sensitivity to movement during reinforcement manoeuvres in relaxed human subjects. The Journal of Physiology 523 Pt 1: 271-282.
14. Harvey RJ, Matthews PBC, (1961) The response of de-efferented muscle spindle endings in the cat's soleus to slow extension of the muscle. The Journal of Physiology 157: 370-392.
15. Matthews PBC, Watson JD, (1981) Action of vibration on the response of cat muscle spindle Ia afferents to low frequency sinusoidal stretching. The Journal of Physiology 317: 365-381.
16. Rack PM, Westbury DR, (1966) The effects of suxamethonium and acetylcholine on the behaviour of cat muscle spindles during dynamics stretching, and during fusimotor stimulation. The Journal of Physiology 186: 698-713.
17. Richmond FJ, Abrahams VC, (1979) Physiological properties of muscle spindles in dorsal neck muscles of the cat. Journal of Neurophysiology 42: 604-617.
18. Taylor A, Durbaba R, Rodgers JF, (1992) The classification of afferents from muscle spindles of the jaw-closing muscles of the cat. The Journal of Physiology 456: 609-628.
19. Pickar JG, Wheeler JD, (2001) Response of muscle proprioceptors to spinal manipulative-like loads in the anesthetized cat. Journal of Manipulative and Physiological Therapeutics 24: 2-11.
20. Angel A, Clarke KA, (1980) Effect of catechol on the discharge of muscle spindle afferents from the hind limb of the rat. Electroencephalography and Clinical Neurophysiology 49: 373-381.
21. De-Doncker L, Picquet F, Petit J, Falempin M, (2003) Characterization of spindle afferents in rat soleus muscle using ramp-and-hold and sinusoidal stretches. Journal of Neurophysiology 89: 442-449.
22. Fang X, McMullan S, Lawson SN, Djouhri L, (2005) Electrophysiological differences between nociceptive and non-nociceptive dorsal root ganglion neurones in the rat in vivo. The Journal of Physiology 565: 927-943.
23. Boada MD, Woodbury CJ, (2008) Myelinated skin sensory neurons project extensively throughout adult mouse substantia gelatinosa. The Journal of Neuroscience 28: 2006-2014.
24. Boada MD, Woodbury CJ, (2007) Physiological properties of mouse skin sensory neurons recorded intracellularly in vivo: temperature effects on somal membrane properties. Journal of Neurophysiology 98: 668-680.
25. Nakanishi ST, Whelan PJ, (2012) A decerebrate adult mouse model for examining the sensorimotor control of locomotion. Journal of Neurophysiology 107: 500-515.
26. Hunt CC, Ottoson D, (1977) Responses of primary and secondary endings of isolated mammalian muscle spindles to sinusoidal length changes. Journal of Neurophysiology 40: 1113-1120.
27. Hunt CC, Ottoson D, (1975) Impulse activity and receptor potential of primary and secondary endings of isolated mammalian muscle spindles. The Journal of Physiology 252: 259-281.
28. Fischer M, Schafer SS, (2005) Effects of changes in pH on the afferent impulse activity of isolated cat muscle spindles. Brain Research 1043: 163-178.
29. Fischer M, Schafer SS, (1999) Temperature effects on the discharge frequency of primary and secondary endings of isolated cat muscle spindles recorded under a ramp-and-hold stretch. Brain Research 840: 1-15.
30. Lippold OC, Nicholls JG, Redfearn JW, (1960) A study of the afferent discharge produced by cooling a mammalian muscle spindle. The Journal of Physiology 153: 218-231.
31. Simon A, Shenton F, Hunter I, Banks RW, Bewick GS, (2010) Amiloride-sensitive channels are a major contributor to mechanotransduction in mammalian muscle spindles. The Journal of Physiology 588: 171-185.
32. Ganguly DK, Nath DN, Ross HG, Vedasiromoni JR, (1978) Rat isolated phrenic nerve-diaphragm preparation for pharmacological study of muscle spindle afferent activity: effect of oxotremorine. British Journal of Pharmacology 64: 47-52.
33. Barclay CJ, (2005) Modelling diffusive O(2) supply to isolated preparations of mammalian skeletal and cardiac muscle. Journal of Muscle Research and Cell Motility 26: 225-235.
34. Close R, (1965) Force: velocity properties of mouse muscles. Nature 206: 718-719.
35. McCully KK, Faulkner JA, (1985) Injury to skeletal muscle fibers of mice following lengthening contractions. Journal of Applied Physiology 59: 119-126.
36. Brooks SV, Faulkner JA, (1988) Contractile properties of skeletal muscles from young, adult and aged mice. The Journal of Physiology 404: 71-82.
37. Warren GL, Hayes DA, Lowe DA, Williams JH, Armstrong RB, (1994) Eccentric contraction-induced injury in normal and hindlimb-suspended mouse soleus and EDL muscles. Journal of Applied Physiology 77: 1421-1430.
38. Duchen LW, Tonge DA, (1973) The effects of tetanus toxin on neuromuscular transmission and on the morphology of motor end-plates in slow and fast skeletal muscle of the mouse. The Journal of Physiology 228: 157-172.
39. Leonard JP, Salpeter MM, (1979) Agonist-induced myopathy at the neuromuscular junction is mediated by calcium. The Journal of Cell Biology 82: 811-819.
40. Taguchi T, Sato J, Mizumura K, (2005) Augmented mechanical response of muscle thin-fiber sensory receptors recorded from rat muscle-nerve preparations in vitro after eccentric contraction. Journal of Neurophysiology 94: 2822-2831.
41. Koltzenburg M, Stucky CL, Lewin GR, (1997) Receptive properties of mouse sensory neurons innervating hairy skin. Journal of Neurophysiology 78: 1841-1850.
42. Banks RW, Hulliger M, Saed HH, Stacey MJ, (2009) A comparative analysis of the encapsulated end-organs of mammalian skeletal muscles and of their sensory nerve endings. Journal of Anatomy 214: 859-887.
43. Johnson MI, Ovalle WK, (1986) A comparative study of muscle spindles in slow and fast neonatal muscles of normal and dystrophic mice. American Journal of Anatomy 175: 413-427.
44. Larsson L, Edstrom L, (1986) Effects of age on enzyme-histochemical fibre spectra and contractile properties of fast- and slow-twitch skeletal muscles in the rat. Journal of the Neurological Sciences 76: 69-89.
45. Hunt CC, Kuffler SW, (1951) Stretch receptor discharges during muscle contraction. The Journal of Physiology 113: 298-315.
46. Matthews BHC, (1933) Nerve endings in mammalian muscle. The Journal of Physiology 78: 1-53.
47. Matthews PBC, (1963) The response of de-efferented muscle spindle receptors to stretching at different velocities. The Journal of Physiology 168: 660-678.
48. Jansen JK, Matthews PBC, (1962) The central control of the dynamic response of muscle spindle receptors. The Journal of Physiology 161: 357-378.
49. Boyd IA, (1981) The action of the three types of intrafusal fibre in isolated cat muscle spindles on the dynamic and length sensitivities of primary and secondary sensory endings. In: Taylor A, Prochazka A, editors. pp. 17-32 editors. Muscle Receptors and Movement. London: Macmillan.
50. Matthews PBC, editor (1981) Muscle spindles: their messages and their fusimotor supply. Bethesda, MD: American Physiological Society. 189-228 p.
51. Haftel VK, Bichler EK, Nichols TR, Pinter MJ, Cope TC, (2004) Movement reduces the dynamic response of muscle spindle afferents and motoneuron synaptic potentials in rat. Journal of Neurophysiology 91: 2164-2171.
52. Houk JC, Singer JJ, Henneman E, (1971) Adequate stimulus for tendon organs with observations on mechanics of ankle joint. Journal of Neurophysiology 34: 1051-1065.
53. Houk J, Henneman E, (1967) Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. Journal of Neurophysiology 30: 466-481.
54. Szumski AJ, Burg D, Struppler A, Velho F, (1974) Activity of muscle spindles during muscle twitch and clonus in normal and spastic human subjects. Electroencephalography and Clinical Neurophysiology 37: 589-597.
55. Granit R, Kellerth J-O, Szumski AJ, (1966) Intracellular autogenetic effects of muscular contraction on extensor motoneurones. The silent period. The Journal of Physiology 182: 484-503.
56. Kindig AE, Hayes SG, Hanna RL, Kaufman MP, (2006) P2 antagonist PPADS attenuates responses of thin fiber afferents to static contraction and tendon stretch. American Journal of Physiology Heart and Circulatory Physiology 290: H1214-1219.
57. Miwa T, Miwa Y, Kanda K, (1995) Dynamic and static sensitivities of muscle spindle primary endings in aged rats to ramp stretch. Neuroscience Letters 201: 179-182.
58. Matthews PBC, (1964) Muscle spindles and their motor control. Physiological Reviews 44: 219-288.
59. Fallon JB, Macefield VG, (2007) Vibration sensitivity of human muscle spindles and Golgi tendon organs. Muscle & Nerve 36: 21-29.
60. Ottoson D, (1965) The effects of temperature on the isolated muscle spindle. The Journal of Physiology 180: 636-648.
61. Bell KR, Lehmann JF, (1987) Effect of cooling on H- and T-reflexes in normal subjects. Archives of Physical Medicine and Rehabilitation 68: 490-493.
62. Michalski WJ, Seguin JJ, (1975) The effects of muscle cooling and stretch on muscle spindle secondary endings in the cat. The Journal of Physiology 253: 341-356.
63. Beam KG, Donaldson PL, (1983) A quantitative study of potassium channel kinetics in rat skeletal muscle from 1 to 37 degrees C. The Journal of General Physiology 81: 485-512.
64. Rodriguez BM, Sigg D, Bezanilla F, (1998) Voltage gating of Shaker K+ channels. The effect of temperature on ionic and gating currents. The Journal of General Physiology 112: 223-242.
65. Peloquin JB, Doering CJ, Rehak R, McRory JE, (2008) Temperature dependence of Cav1.4 calcium channel gating. Neuroscience 151: 1066-1083.
66. Hunt CC, (1954) Relation of function to diameter in afferent fibers of muscle nerves. The Journal of General Physiology 38: 117-131.
67. Ruffini A, (1898) On the minute anatomy of the neuromuscular spindles of the cat, and on their physiological significance. The Journal of Physiology 23: 190-208 193.
68. Bianconi R, van der Meulen J, (1963) The response to vibration of the end organs of mammalian muscle spindles. Journal of Neurophysiology 26: 177-190.
69. Wenk HN, McCleskey EW, (2007) A novel mouse skeletal muscle-nerve preparation and in vitro model of ischemia. Journal of Neuroscience Methods 159: 244-251.
70. Cody FW, Lee RW, Taylor A, (1972) A functional analysis of the components of the mesencephalic nucleus of the fifth nerve in the cat. The Journal of Physiology 226: 249-261.
71. Bullinger KL, Nardelli P, Wang Q, Rich MM, Cope TC, (2011) Oxaliplatin neurotoxicity of sensory transduction in rat proprioceptors. Journal of Neurophysiology 106: 704-709.