The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord

Journal of Comparative Neurology - Tập 268 Số 4 - Trang 489-507 - 1988
Yoshio Shigenaga1, Masayuki Sera2, Toshikazu Nishimori2, Setsuko Suemune2, Masao Nishimura2, Atsushi Yoshida2, Koichiro Tsuru2
1Department of Oral Anatomy (1st Division), Hiroshima University School of Dentistry, Japan.
2Department of Oral Anatomy (1st Division), Hiroshima University School of Dentistry, Hiroshima 734, Japan

Tóm tắt

AbstractRetrograde and anterograde transport of horseradish peroxidase‐wheat germ agglutinin (HRP‐WGA) conjugate was used to study the organization of primary afferent neurons innervating the masticatory muscles. HRP applied to the nerves of jaw‐closing muscles–the deep temporal (DT), masseter (Ma), and medial pterygoid (MP)–labeled cells in the trigeminal ganglion and the mesencephalic trigeminal nucleus (Vmes), whereas HRP applied to nerves of the jaw‐opening muscles–anterior digastric (AD) and mylohyoid (My)–labeled cells only in the trigeminal ganglion. Cell bodies innervating the jaw‐closing muscles were found with greater frequency in the intermediate region of the mandibular subdivision, while somata supplying the jaw‐opening muscles were predominant posterolaterally. The distribution of their somatic sizes was unimodal and limited to a subpopulation of smaller cells. Projections of the muscle afferents of ganglionic origin to the trigeminal sensory nuclear complex (TSNC) were confined primarily to the caudal half of pars interpolaris (Vi), and the medullary and upper cervical dorsal horns. In the Vi, Ma, MP, AD, and My nerves terminated in the lateral‐most part of the nucleus with an extensive overlap in projections, save for the DT nerve, which projected to the interstitial nucleus or paratrigeminal nucleus. In the medullary and upper cervical dorsal horns, the main terminal fields of individual branches were confined to laminae I/V, but the density of the terminals in lamina V was very sparse. The rostrocaudal extent of the terminal field in lamina I differed among the muscle afferents of origin, whereas in the mediolateral or dorsoventral axis, a remarkable overlap in projections was noted between or among muscle afferents. The terminals of DT afferents were most broadly extended from the rostral level of the pars caudalis to the C3 segment, whereas the MP nerve showed limited projection to the middle one‐third of the pars caudalis. Terminal fields of the Ma, AD, and My nerves appeared in the caudal two‐thirds of the pars caudalis including the first two cervical segments, the caudal half of the pars caudalis and the C1 segment, and in the caudal part of the pars caudalis including the rostral C1 segment, respectively. This rostrocaudal arrangement in the projections of muscle nerves, which corresponds to the anteroposterior length of the muscles and their positions, indicates that representation of the masticatory muscles in lamina I reflects an onion‐skin organization. These results suggest that primary muscle afferent neurons of ganglionic origin primarily mediate muscle pain. In addition, the distribution patterns of the afferent neurons of jaw‐closing muscles in the mesencephalic trigeminal nucleus (Vmes) and their central projections were examined. The Vmes neurons from the DT and Ma nerves were bimo‐dally distributed, with larger numbers in the rostra1 half of the nucleus, whereas those from the MP nerve were sparsely and evenly distributed. Individual central axons of the Vmes neurons innervating the three jaw‐closing muscles projected to the trigeminal motor nucleus (Vmo), supra‐ and intertrigeminal regions, and lateral reticular formation of the medulla extending to the upper spinal cord. There were, however, differences in the caudal extent of the axons from the different muscles.

Từ khóa


Tài liệu tham khảo

Alley K. E., 1974, Morphogenesis of the trigeminal mesencephalic nucleus in the hamster: Cytogenesis and neurone death, J. Embryol. Exp. Morphol., 31, 99

10.1007/BF00235459

Amano N., 1986, Responses of neurons in feline trigeminal subnucleus caudalis (medullary dorsal horn)to cutaneous, intraoral, and muscle afferent stimuli, J. Neurophysiol., 55, 227, 10.1152/jn.1986.55.2.227

10.1113/jphysiol.1978.sp012353

Åstrøm K. E., 1953, On the central course of afferent fibres in the trigeminal, facial, glossopharyngeal, and vagal nerves and their nuclei in the mouse, Acta Physiol. Scand,(Suppl.)., 106, 209, 10.1111/apha.1953.29.s106.209

10.1016/0003-9969(68)90124-6

10.1002/cne.901940407

Bessou P., 1961, Étude des recepteurs musculaires innerves par les fibres afferentes du group III (fibres myelinisees fines)chez le chat, Arch. Ital. Biol., 99, 293

10.1016/0006-8993(79)90680-2

10.1002/cne.901830406

Cervero F., 1982, Somatic and visceral inputs to the thoracic spinal cord of the cat: Effects of noxious stimulation of the biliary system, J. Physiol. (Lond.), 337, 51, 10.1113/jphysiol.1983.sp014611

10.1016/0006-8993(84)91053-9

10.1002/cne.902300108

10.1016/0304-3959(76)90042-7

10.1007/BF01173988

10.1152/jn.1980.44.2.359

10.1152/jn.1980.44.2.349

10.1113/jphysiol.1972.sp009983

Cooper S., 1960, The Structure and Function of Muscle, 381

10.1002/cne.900770302

10.1016/0304-3940(83)90456-1

10.1098/rspb.1955.0039

10.1007/978-1-4757-1682-5

10.1113/jphysiol.1979.sp012614

10.1113/jphysiol.1979.sp012615

10.1002/cne.901830112

10.1016/0006-8993(77)90427-9

Gobel S., 1981, Morphology and synaptic connections of ultrafine primary axons in lamina I of the spinal dorsal horn: Candidates for the terminal axonal arbors of primary neurons with unmyelinated (C)axons, J. Neuroscience., 1, 1163, 10.1523/JNEUROSCI.01-10-01163.1981

10.1002/cne.902280212

Gregg J. M., 1973, Somatotopic organization of the trigeminal ganglion in the rat, Archs. Oral Biol., 18, 457, 10.1016/0003-9969(73)90069-1

Harrison F., 1942, The central pathway for the jaw‐jerk, Brain Res., 135, 439

10.1002/cne.902400106

10.1152/jn.1984.51.5.890

10.1002/aja.1001260408

10.1113/jphysiol.1979.sp012764

Hosokawa H., 1961, Proprioceptive innervation of striated muscles in the territory of cranial nerves, Texas Rep. Biol. Med., 19, 405

10.1002/cne.902180302

10.1002/cne.902150405

10.1152/jn.1963.26.3.379

Jerge C. R., 1963, The function of the nucleus supratrigeminalis, J. Neurophysiol., 26, 393, 10.1152/jn.1963.26.3.393

Kalia M.‐S., 1981, Central projections from ergoreceptors (C fiber) in muscle involved in cardiopulmonary responses to static exercise, Circ. Res., 48, 48

10.3109/00016356509021768

10.3109/00016356909008955

10.1016/0006-8993(68)90018-8

10.1001/archneur.1964.00460240025003

Kidokoro Y., 1968, Reflex organization of cat masticatory muscles, J. Neurophysiol., 31, 695, 10.1152/jn.1968.31.5.695

Kidokoro Y., 1968, Possible interneurons responsible for reflex inhibition of motoneurons of jaw‐closing muscles from the inferior dental nerve, J. Neurophysiol., 31, 709, 10.1152/jn.1968.31.5.709

Kubota K., 1973, Muscle spindle distribution in the masticatory muscles of the squirrel monkey (Saimiri sciurea), Bull. Tokyo Mod. Dent. Univ., 20, 275

10.1113/jphysiol.1977.sp012088

10.1002/cne.902160205

10.1007/BF00495777

10.1152/jn.1948.11.3.199

10.1002/cne.901860203

10.1016/0306-4522(78)90107-0

10.1002/ar.1092010113

10.1016/0304-3940(81)90198-1

10.1016/0003-9969(72)90053-2

10.1113/jphysiol.1977.sp011802

10.1177/26.2.24068

10.1002/cne.902280112

10.1016/0304-3959(81)90003-8

10.1002/cne.901390205

10.1002/cne.902150305

10.1002/cne.902010308

Morimoto T., 1982, Diameter spectra of sensory and motor fibers in nerves to jaw‐closing and jaw‐opening muscles in the cat, Jap Brain Res., 32, 171

Nakamura Y., 1980, Spinal and Supraspinal Mechanisms of Voluntary Motor Control and Locomotion, 181

10.1016/0006-8993(73)90564-7

10.1016/0006-8993(87)90506-3

10.1016/0006-8993(86)91148-0

10.1016/0304-3940(85)90458-6

10.1016/0006-8993(85)91442-8

10.1002/cne.902360109

10.1002/ar.1090550203

10.1113/jphysiol.1960.sp006486

10.1002/cne.900910202

10.1113/jphysiol.1968.sp008666

10.1002/cne.902040107

10.1152/jn.1976.39.5.936

10.1002/cne.901840404

10.1139/y76-043

10.1002/cne.902060308

10.1016/0006-8993(79)90225-7

10.1016/0006-8993(83)90928-9

10.1016/0006-8993(84)90600-0

10.1002/cne.902430309

10.1002/cne.902440102

10.1002/cne.902510303

10.1002/cne.901330408

Stacey M. J., 1969, Free nerve endings in skeletal muscle of the cat, J. Anat., 105, 231

10.1126/science.3764416

Szentágothai J., 1948, Anatomical considerations of monosynaptic reflex arcs, J. Neurophysiol., 11, 445, 10.1152/jn.1948.11.5.445

Takata M., 1980, Jaw Position and Jaw Movement, 248

10.1002/cne.900370108

10.1007/BF00236294

Webber R. H., 1966, Distribution of fibers from nerve cell bodies in ventral roots of spinal nerves, Acta Anat. (Basel)., 65, 579, 10.1159/000142906

10.1002/cne.900460202

10.1001/archneurpsyc.1931.02230100109009

10.1098/rspb.1975.0106

10.1007/BF01181578

10.1002/cne.902200209

10.3171/jns.1978.49.4.0538

10.1002/cne.901830114

10.1016/0006-8993(69)90061-4