Physiologic and morphologic properties of motoneurons and spindle afferents innervating the temporal muscle in the cat

Journal of Comparative Neurology

Volumn 406, Issue 1, 1999, Pages 29-50

  Yoshida, Atsushi ^a   Mukai, Norifumi ^a   Moritani, Masayuki ^a   Nagase, Yoshitaka ^a   Hirose, Yohsuke ^a   Honma, Shiho ^a   Fukami, Hideyuki ^a   Takagi, Kazunori ^a   Matsuya, Tokuzo ^a   Shigenaga, Yoshio ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

HRP; Intracellular; Jaw reflex; SCh; Stretch response

Indexed keywords

BIOTINIDASE; HORSERADISH PEROXIDASE; SUXAMETHONIUM;

ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CAT; DENDRITE; JAW OPENING REFLEX; LATENT PERIOD; MICROSCOPY; MOTONEURON; MOTOR NERVE CONDUCTION; MUSCLE INNERVATION; MUSCLE SPINDLE AFFERENT NERVE; MYOTATIC REFLEX; NERVE CELL NETWORK; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; TEMPORALIS MUSCLE; TRIGEMINAL NUCLEUS;

EID: 0033614293     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990329)406:1<29::AID-CNE3>3.0.CO;2-0     Document Type: Article

References (96)

1. Adams JC. 1977. Technical consideration on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2:141-145.
2. Appenteng K, O'Donovan MJ, Somjen G, Stephens JA, Taylor A. 1978. The projection of jaw elevator muscle spindle afferents to fifth nerve motoneurones in the cat. J Physiol (Lond) 279:409-423.
3. Bae YC, Nakagawa S, Yabuta NH, Yoshida A, Pil PK, Moritani M, Chen K, Takemura M, Shigenaga Y. 1996. Electron microscopic observations of synaptic connections of jaw-muscle spindle and periodontal afferent terminals in the trigeminal motor and supratrigeminal nuclei in the cat. J Comp Neurol 374:421-435.
4. Bossy J. 1958. A propos de Iinnervation proprioceptive du muscle stylohyoid et du ventre postieur du muscle digastrique. Arch Anat Histol Embryol 41:37-44.
5. Boyd IA. 1985. Review. In: Boyd IA, Gladden MH, editors. The muscle spindle. London: Macmillan. p 129-150.
6. Brown AG, Fyffe REW. 1981. Direct observations on the contacts made between Ia afferent fibres and α-motoneurones in the cat's lumbosacral spinal cord. J Physiol (Lond) 313:121-140.
7. Browne JS. 1975. The responses of muscle spindles in sheep extraocular muscles. J Physiol (Lond) 251:483-496.
8. Burke RE. 1967. The composite nature of the monosynaptic excitatory postsynaptic potentials. J Neurophysiol 30:1114-1137.
9. Burke RE, Rudomin P. 1977. Spinal neurons synapses. Handbook of physiology. The nervous system. Cellular biology of neurons. Bethesda, MD: Am Physiol Soc, sect. 1, vol. 1, p 877-944.
10. Burke RE, Walmsley B, Hodgson JA. 1979. HRP anatomy of group Ia afferent contacts on alpha motoneurones. Brain Res 160:347-352.
11. Burke RE, Dum RP, Fleshman JW, Glenn LL, Lev-tov A, O'Donovan MJ, Pinter MJ. 1982, An HRP study of the relation between cell size and motor unit type in cat ankle extensor motoneurons. J Comp Neurol 209:17-28.
12. Burke RF, Glenn LL. 1996. Horseradish peroxidase study of the spatial and electrotonic distribution of group Ia synapses on type-identified ankle extensor motoneurons in the cat. J Comp Neurol 372:465-485.
13. Cameron WE, Averill DB, Berger AJ. 1985. Quantitative analysis of the dendrites of cat phrenic motoneurons stained intracellularly with horseradish peroxidase. J Comp Neurol 230:91-101.
14. Carr RW, Morgan DL, Proske U. 1996. Impulse initiation in the mammalian muscle spindle during combined fusimotor stimulation and succinyl choline infusion. J Neurophysiol 75:1703-1713.
15. Cheney PD, Preston JB. 1976. Classification and response characteristics of muscle spindle afferents in the primate. J Neurophysiol 39:1-8.
16. Cody FWJ, Lee RWH, Taylor A. 1972. A functional analysis of the components of the mesencephalic nucleus of the fifth nerve in the cat. J Physiol (Lond) 226:249-261.
17. Cody FWJ, Harrison LM, Taylor A. 1975. Analysis of activity of muscle spindles of the jaw-closing muscles during normal movements in the cat. J Physiol (Lond) 253:565-582.
18. Cooper S. 1961. The response of the primary and secondary endings of muscle spindles with intact motor innervation during applied stretch. Q J Exp Physiol 46:389-398.
19. Crowe A, Matthews PBC. 1964. The effects of stimulation of static and dynamic fusimotor fibers on the response to stretching of the primary endings of muscle spindles. J Physiol (Lond) 174:109-131.
20. Cullheim S, Kellerth J-O. 1978a. A morphological study of the axons and recurrent axon collaterals of cat sciatic α-motoneurons after intracellular staining with horseradish peroxidase. J Comp Neurol 178:537-558.
21. Cullheim S, Kellerth J-O. 1978b. A morphological study of the axons and recurrent axon collaterals of cat α-motoneurons supplying different hind-limb muscles. J Physiol (Lond) 281:285-299.
22. Cullheim S, Ulfhake B. 1979. Observations on the morphology of intracellularly stained γ-motoneurons in relation to their axon conduction velocity. Neurosci Lett 13:47-50.
23. Dessem D, Taylor A. 1989. Morphology of jaw-muscle spindle afferents in the rat. J Comp Neurol 282:389-403.
24. Dessem D, Donga R, Luo P. 1997. Primary-and secondary-like jaw-muscle spindle afferents have characteristic topographic distributions. J Neurophysiol 77:2925-2944.
25. Dmytruk RJ. 1974. Neuromuscular spindles and depressor masticatory muscles of monkey. Am J Anat 141:147-153.
26. Donga R, Dessem D. 1995. Central terminations of intra-axonally labeled jaw-elevator muscle spindle afferents in the rat. In: Taylor A, Gladden M, Durbaba R, editors. Alpha and gamma motor systems. New York and London: Plenum Press. p 60-62.
27. Egger MD, Freeman NCG, Proshansky E. 1980. Morphology of spinal motoneurones mediating a cutaneous spinal reflex in the cat. J Physiol (Lond) 306:349-363.
28. Evinger C, Graf WM, Baker R. 1987. Extra-and Intra-cellular HRP analysis of the organization of extraocular motoneurons and internuclear neurons in the guinea pig and rabbit. J Comp Neurol 262:429-445.
29. Friauf E, Baker R. 1985. An intracellular HRP-study of cat tensor tympani motoneurons. Exp Brain Res 57:499-511.
30. Fukunishi Y, Nagase Y, Yoshida A, Moritani M, Honma S, Hirose Y, Shigenaga Y. 1999. Quantitative analysis of the dendritic architectures of cat hypoglossal motoneurons stained with intracellularly with horse-radish peroxidase. J Comp Neurol 405:345-358.
31. Gladden MH. 1976. Structural features relative to the function of intrafusal muscle fibres in the cat. Prog Brain Res 44:51-59.
32. Gladden MH, McWilliam PN. 1977. The activity of intrafusal muscle fibres during cortical stimulation in the cat. J Physiol (Lond) 273:28-29.
33. Highstein SM, Karabelas A, Baker R, McCrea RA. 1982. Comparison of the morphology of physiologically identified abducens motor and internuclear neurons in the cat: a light microscopic study employing the intracellular injection of horseradish peroxidase. J Comp Neurol 208: 369-381.
34. Hunt CC. 1951. The reflex activity of mammalian small-nerve fibers. J Physiol (Lond) 115:456-469.
35. Iansek R, Redman SJ. 1973. The amplitude, time course and charge of unitary excitatory post-synaptic potentials evoked in spinal motoneurone dendrites. J Physiol (Lond) 234:665-688.
36. Inoue H, Morimoto T, Kawamura Y. 1981. Response characteristics and classification of muscle spindles of the masseter muscle in the cat. Exp Neurol 74:548-560.
37. Jack JJB, Miller S, Porter R, Redman SJ. 1971. The time course of minimal excitatory post-synaptic potentials evoked in spinal motoneurones by group Ia afferent fibres. J Physiol (Lond) 215:353-380.
38. Jack JJ, Redman ST, Wong K. 1981. The components of synaptic potentials evoked in cat spinal motoneurons by impulses in single group Ia afferents. J Physiol (Lond) 321:65-96.
39. Kernell D, Zwaagstra G. 1989. Size and remoteness: two relatively independent parameters of dendrites, as studied for spinal motoneurones of the cat. J Physiol (Lond) 413:233-254.
40. Kidokoro Y, Kubota K, Shuto S, Sumino R. 1968a. Reflex organization of cat masticatory muscles. J Neurophysiol 31:695-708.
41. Kidokoro Y, Kubota K, Shuto S, Sumino R. 1968b. Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve. J Neurophysiol 31:709-716.
42. Kirkwood PA, Sears TA. 1974. Monosynaptic excitation of motoneurons from secondary endings of muscle spindles. Nature 252:243-244.
43. Kishimoto H, Bae YC, Yoshida A, Moritani M, Takemura M, Nakagawa S, Nagase Y, Wada T, Sessle BJ, Shigenaga Y. 1998. Central distribution of synaptic contacts of primary and secondary jaw muscle spindle afferents in the trigeminal motor nucleus of the cat. J Comp Neurol 391:50-63.
44. Koeze TH. 1968. The response to stretch of muscle spindle afferents of baboon's tibialis anticus and the effect of fusimotor stimulation. J Physiol (Lond) 197:107-121.
45. Koeze TH. 1973. Muscle spindle afferent studies in the baboon. J Physiol (Lond) 229:297-317.
46. Kubota K, Masegi T, Osanai K. 1974. Muscle spindle in masticatory muscle and its trigeminal mesencephalic nucleus. Bull Tokyo Med Dent Univ 21:3-6.
47. Kuffler SW, Hunt CC, Quilliam JP. 1951. Function of medullated small-nerve fibers in mammalian ventral root: efferent muscle spindle innervation. J Neurophysiol 14:29-54.
48. Lennerstrand G. 1968. Position and velocity sensitivity of muscle spindles in the cat: IV. Interaction between two fusimotor fibres converging on the same spindle ending. Acta Physiol Scand 74:257-273.
49. Lingenhöl K, Friauf E. 1991. Sensory neurons and motoneurons of the jaw-closing reflex pathway in rats: a combined morphological and physiological study using the intracellular horseradish peroxidase technique. Exp Brain Res 83:385-396.
50. Luo P, Dessem D. 1995. Inputs from identified jaw-muscle spindle afferents to trigeminothalamic neurons in the rat: a double-labeling study using retrograde HRP and intracellular biotinamide. J Comp Neurol 353:50-66.
51. Luo P, Wong R, Dessem D. 1995a. Ultrastructural basis for synaptic transmission between jaw-muscle spindle afferents and trigeminothalamic neurons in the rostral trigeminal sensory nuclei of the cat. J Comp Neurol 363:109-128.
52. Luo P, Wong R, Dessem D. 1995b. Projection of jaw-muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide. J Comp Neurol 358:63-78.
53. Matesz C. 1981. Peripheral and central distribution of fibers of the mesencephalic trigeminal root in the rat. Neurosci Lett 27:13-17.
54. Matsuda K, Uemura M, Kume M, Matsushima R, Mizuno N. 1978. Topographical representation of masticatory muscles in the motor trigeminal nucleus in the rabbit: an HRP study. Neurosci Lett 8:1-4.
55. Matthews PBC. 1963. The response of de-efferented muscle spindle receptors to stretching at different velocity. J Physiol (Lond) 168:660-678.
56. Matthews PBC. 1972. Mammalian muscle receptors and their central actions. London: Edward Arnold.
57. Matthews PBC, Stein RB. 1969. The regularity of primary and secondary muscle spindle afferent discharges. J Physiol (Lond) 202:59-82.
58. Meessen H, Olszewski J. 1949. A cytoarchitectonic atlas of the rhombencephalon of the rabbit. Basel: Karger.
59. Mendell LM, Henneman E. 1968a. Terminals of single Ia fibers: distribution within a pool of 300 homonymous motor neurons. Science 160:96-98.
60. Mendell LM, Henneman E. 1968b. Terminals of single Ia fibers: location, density, and distribution within a pool of 300 homonymous motoneurons. J Neurophysiol 34:171-187.
61. Mendell LM, Weiner R. 1976. Analysis of pairs of individual Ia-E.P.S.Ps in single motoneurons. J Physiol (Lond) 255:81-104.
62. Mizuno N, Konishi A, Sato M. 1975. Localization of masticatory motoneurons in the cat and rat by means of retrograde axonal transport of horseradish peroxidase. J Comp Neurol 164:105-116.
63. Moschovakis AK, Burke RE, Fyffe REW. 1991. The size and dendritic structure of HRP-labeled gamma motoneurons in the cat spinal cord. J Comp Neurol 311:531-545.
64. Munson JB, Sypert GW. 1979. Properties of single central Ia afferent fibers projecting to motoneurones. J Physiol (Lond) 296:315-327.
65. Munson JB, Fleshman JW, Sypert GW. 1980. Properties of single-fiber spindle group II EPSPs in triceps surae motoneurons. J Neurophysiol 44:713-725.
66. Nagase Y, Moritani M, Nakagawa S, Yoshida A. Takemura M, Zhang L-F, Kida H, Shigenaga Y. 1997. Serotonergic axonal contacts on identified cat trigeminal motoneurons and their correlation with medullary raphe nucleus stimulation. J Comp Neurol 384:443-455.
67. Nakagawa S, Kurata S, Yoshida A, Nagase Y, Moritani M, Takemura M, Bae YC, Shigenaga Y. 1997. Ultrastructural observations of synaptic connections of vibrissa afferent terminals in cat principal sensory nucleus and morphometry of related synaptic element. J Comp Neurol 389:12-33.
68. Nomura S, Mizuno N. 1985. Differential distribution of cell bodies and central axons of mesencephalic trigeminal nucleus neurons supplying the jaw-closing muscles and periodontal tissue: a transganglionic tracer study in the cat. Brain Res 359:311-319.
69. Price RF, Dutia MB. 1987. Properties of cat neck muscle spindles and their excitation by succinylcholine. Exp Brain Res 68:619-630.
70. Rack PMH, Westbury DR. 1966. The effects of suxamethonium and acetylcholine on the behavior of cat muscle spindles during dynamic stretching and during fusimotor stimulation. J Physiol (Lond) 186:698-713.
71. Rakhawy MT, Shehata SH, Badawy ZH. 1971. The proprioceptive innervation of the lateral pterygoid muscle in man and some other mammals. Acta Anat 79:581-598.
72. Rall W, Burke RE, Smith TG, Nelson PG, Frank K. 1967. Dendritic location of synapses and possible mechanisms for the monosynaptic EPSPs in motoneurons. J Neurophysiol 30:1169-1193.
73. Redman S, Walmsley B. 1983. The time course of synaptic potentials evoked in cat spinal motoneurones at identified group Ia synapses. J Physiol (Lond) 343:117-133.
74. Richmond FJ, Abrahams VC. 1979. Physiological properties of muscle spindles in dorsal neck muscles of the cat. J Neurophysiol 42:604-617.
75. Rose PK, Keirstesd SA, Vanner SJ. 1985. A quantitative analysis of the geometry of cat motoneurons innervating neck and shoulder muscles. J Comp Neurol 239:89-107.
76. Russell-Mergenthal H, McClung JR, Goldberg SJ. 1986. The determination of dendrite morphology on lateral rectus motoneurons in cat. J Comp Neurol 245:116-122.
77. Scott JJA. 1990. Classification of muscle spindle afferents in the peroneus brevis muscle of the cat. Brain Res 509:62-70.
78. Shigenaga Y, Mitsuhiro Y, Yoshida A, Cao CQ, Tsuru H. 1988a. Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat. Brain Res 445:392-399.
79. Shigenaga Y, Sera M, Nishimori T, Suemune S, Nishimura M, Yoshida A, Tsuru K. 1988b. The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J Comp Neurol 268:489-507.
80. Shigenaga Y, Yoshida A, Tsuru K, Mitsuhiro Y, Otani K, Cao CQ. 1988c. Physiological and morphological characteristics of cat masticatory motoneurons: intracellular injection of HRP. Brain Res 461:238-256.
81. Shigenaga Y, Mitsuhiro Y, Shirana Y, Tsuru H. 1990. Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP. Brain Res 514:219-237.
82. Stauffer EK, Watt DGD, Taylor A, Reinking RM, Stuart DG. 1976. Analysis of muscle receptor connections by spike-triggered averaging. 2. spindle group II afferents. J Neurophysiol 39:1393-1402.
83. Takata M. 1979. Postsynaptic potentials in the jaw-opening motoneurons by stimulation of the trigeminal nerves. Brain Res 163:161-164.
84. Takata M, Fujita S. 1979. The properties of lingually induced IPSPs in the masseteric motoneurons. Brain Res 168:648-651.
85. Taylor A, Durbaba R, Rodgers JF. 1992a. The classification of afferents from muscle spindles of the jaw-closing muscles of the cat. J Physiol (Lond) 456:609-628.
86. Taylor A, Rodgers JF, Fowle AJ, Durbaba R. 1992b. The effect of succinylcholine on cat gastrocnemius muscle spindle afferents of different types. J Physiol (Lond) 456:629-644.
87. Uemura-Sumi M, Takahashi O, Matsushima R, Takada M, Yasui Y, Mizuno N. 1982. Localization of masticatory motoneurons in the trigeminal motor nucleus of the guinea pig. Neurosci Lett 29:219-224.
88. Ulfhake B, Cullheim S. 1981. A quantitative light microscopic study of the dendrites of cat spinal γ-motoneurons after intracellular staining with horseradish peroxidase. J Comp Neurol 202:585-596.
89. Ulfhake B, Kellerth J-O. 1981. A quantitative light microscopic study of the dendrites of cat spinal α-motoneurons after intracellular staining with horseradish peroxidase. J Comp Neurol 202:571-583.
90. Ulfhake B, Kellerth J-O. 1983. A quantitative morphological study of HRP-labeled cat α-motoneurons supplying different hindlimb muscles. Brain Res 264:1-19.
91. Wei JK, Kripke BR, Burgess PR. 1986. Classification of muscle spindle receptors. Brain Res 370:119-126.
92. Westbury DR. 1982. A comparison of the structure of α-and γ-spinal motoneurons of the cat. J Physiol (Lond) 325:79-91.
93. Yabuta NH, Yasuda K, Nagase Y, Yoshida A, Fukunishi Y, Shigenaga Y. 1996. Light microscopic observation of the contacts made between two spindle afferent types and α-motoneurons in the cat trigeminal motor nucleus. J Comp Neurol 374:436-450.
94. Yoshida A, Yasuda K, Dostrovsky JO, Bae YC, Takemura M, Shigenaga Y, Sessle BJ. 1994. Two major types of premotoneurons in the feline trigeminal nucleus oralis neurons as demonstrated by intracellular staining with HRP. J Comp Neurol 347:495-514.
95. Yoshida A, Bae YC, Shigenaga Y, Sessle BJ 1995. Physiology and morphology of the neuronal circuits of jaw reflexes in cats. In: Taylor A, Gladden M, Durbaba R, editors. Alpha and gamma motor systems. New York and London: Plenum Press. p 57-59.
96. Yoshida A, Hiraga T, Moritani M, Chen K, Takatsuki Y, Hirose Y, Bae YC, Shigenaga Y. 1998. Morphological characteristics of physiologically defined neurons in the cat trigeminal nucleus principalis. J Comp Neurol 401:308-328.