×

Somatic and intramuscular distribution of muscle spindles and their relation to muscular angiotypes. (English) Zbl 1440.92021

Summary: The distribution pattern of muscle spindles in the skeletal musculature has been reviewed in a large number of muscles (using the literature data especially from cat and man), and the relation of spindle content to muscle mass was quantitatively examined in 36 cat and 140 human muscles. In both species, the number of spindles increases with increasing muscle mass in a power law fashion of the form \(y=bx +a\), whereby \(y\) denotes the logarithm of spindle content within a muscle, and \(x\) is the logarithm of muscle mass. For the cat, slope \(b\) and intercept \(a\) were estimated as 0.39 and 1.53, and for man as 0.48 and 1.33, respectively. The results show that the spindle content of a muscle may be related to its mass, confirming a similar analysis made previously by R. W. Banks and M. Stacey [Mechano receptors. New York, NY: Plenum Press. 263–269 (1988)] in a different data set. With regard to the histological profile of muscle fibers, (as it is already well documented by many groups) muscle spindles tend to be located in deeper muscle regions where oxidative fibers predominate, and are far scarcer in superficial and flat muscle regions where glycolytic fibers predominate. These discrete muscle regions differ also in the properties of the vessel tree supplying them, for which the term oxidative and glycolytic “angiotype” has been used. The results from these three aspects of analysis (relation to muscle mass, relation to muscle regions with high oxidative index and relation to muscle regions with dense vascular supply) were combined with histological findings showing that spindles may be in systematic anatomical contact to intramuscular vessels. Based on these data a hypothesis is proposed according to which, both the number and intramuscular placement of muscle spindles are related to the oxidative angiotype supplying the muscle territories rich in oxidative fibers. The hypothesis is discussed.

MSC:

92C30 Physiology (general)
62P10 Applications of statistics to biology and medical sciences; meta analysis
PDFBibTeX XMLCite
Full Text: DOI

References:

[1] Abuel-Atta, A.; DeSantis, M.; Wong, A., Encapsulated sensory receptors within intraorbital skeletal muscles of a camel, Anat. Rec., 248, 189-198 (1997)
[2] Acosta, L.; Roy, R. R., Fiber-type composition of skeletal hindlimb muscles of a primate (Cynomolgus monkey), Anat. Rec., 218, 136-141 (1987)
[3] Adair, T. H.; Gay, W. L.; Montani, J. P., Growth regulation of the vascular systemevidence for a metabolic hypothesis, Am. J. Physiol., 259, R393-R404 (1990)
[4] Adal, M. N.; Chew-Cheng, S. B., The blood supply of duck muscle spindles, Cell Tissue Res., 212, 2, 233-239 (1980)
[5] Backsai, T.; Matesz, C., Primary afferent fibers establish dye-coupled connections in the frog central nervous system, Brain Res. Bull., 57, 3-4, 237-564 (2002)
[6] Ballard, K., Typical sympathetic noradrenergic endings in a muscle spindle of the cat, J. Physiol. (Lond.), 285, 61P-62P (1978)
[7] Banks, R. W.; Stacey, M., Quantitative studies on mammalian muscle spindles and their sensory innervation, (Hnik, P.; Soukup, T.; Vejsada, R.; Zelena, J., Mechanoreceptors (1988), Plenum Press: Plenum Press New York), 263-269
[8] Barker, D., The structure and distribution of muscle receptors, (Barker, D., Muscle Receptors (1962), Hong Kong University Press: Hong Kong University Press Hong-Kong), 227-240
[9] Barker, D., The morphology of muscle receptors, (Hunt, C. C., Handbook of sensory physiology. III/2 Muscle receptors (1974), Springer: Springer Berlin, Heidelberg, New York), 1-190
[10] Barker, D.; Banks, R. W., The muscle spindle, (Engel, A.; Franzini-Armstrong, C., Myology (1994), McGraw-Hill: McGraw-Hill New York), 333-360, (Chapter 11)
[11] Barker, D.; Saed, H. H., Adrenergic innervation of rat jaw muscles, J. Physiol. (Lond. ), 391, 114P (1987)
[12] Barker, D.; Saito, M., Autonomic innervation of receptors and muscle fibers in cat skeletal muscle, Proc. R. Soc. Lond., 212, 317 (1981)
[13] Bates, D.; Taylor, G. I.; Newgreen, D. F., The pattern of neurovascular development in the forelimb of the quail embryo, Dev. Biol., 249, 300-320 (2002)
[14] Berkinblit, M. B.; Feldman, A. G.; Fukson, O., Adaptability of innate motor patterns and motor control mechanisms, Behav. Brain Sci., 9, 585-638 (1986)
[15] Bessou, P.; Laporte, Y., Responses from primary and secondary endings of the same neuromuscular spindle of the tenuissimus muscle of the cat, (Barker, D., Muscle Receptors (1962), Hong Kong University Press: Hong Kong University Press Hong-Kong), 105-119
[16] Blumer, R.; Lukas, J. R.; Aigner, M.; Bittner, R.; Baumgartner, I.; Mayr, R., Fine structural analysis of extraoccular muscle spindles of a two-year-old human infant, Invest. Ophthalmol. Vis. Sci., 40, 1, 55-64 (1999)
[17] Botterman, B.; Binder, M.; Stuart, D., Functional anatomy of the association between motor units and muscle receptors, Am. Zool., 18, 135-152 (1978)
[18] Boyd, I. A., The behavior of isolated mammalian muscle spindles with intact innervation, J. Physiol. (Lond.), 186, 109P-110P (1966)
[19] Boyd, I. A.; Ward, J., The response of isolated cat muscle spindles to passive stretch, J. Physiol. (Lond.), 200, 104P-105P (1969)
[20] Boyd-Clark, L. C.; Briggs, C. A.; Galea, M. P., Muscle spindle distribution, morphology and density in longus colli and multifidus muscles of the cervical spine, Spine, 27, 7, 694-701 (2002)
[21] Bredman, J. J.; Weijs, W. A.; Brugman, P., Relationships between spindle density, muscle architecture and fiber type composition in different parts of the rabbit masseter, Eur. J. Morphol., 29, 4, 297-307 (1991)
[22] Bridgman, C. F.; Eldred, E., Hypothesis for a pressure-sensitive mechanism in muscle spindles, Science, 143, 481-482 (1964)
[23] Bridgman, C. F.; Shumpert, E. E.; Eldred, E., Insertions of intrafusal fibers in muscle spindles of the cat and other mammals, Anat. Rec., 164, 391-402 (1969)
[24] Brown, A. G., Organization in the Spinal Cord (1981), Springer: Springer Berlin, Heidelberg, New York
[25] Brown, M.; Cotter, M.; Hudlicka, O.; Vrbova, G., The effects of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles, Pflügers Arch., 361, 241-250 (1976)
[26] Brzezinski, D. K.von, Untersuchungen zur histochemie der muskelspindeln, II Mitteilung. Zur Topochemie und Funktion des Spindelraumes und der Spindelkapsel. Acta Histochem., 12, 277-288 (1961)
[27] Burhanudin, R.; McDonald, F.; Rowlerson, A., Muscle spindles in the jaw-closer muscles of the domestic cat, J. Anat., 188, 2, 299-309 (1996)
[28] Burke, D.; Skuse, N. F.; Stuart, D. G., The regularity of muscle spindle discharge in man, J. Physiol. (Lond.), 291, 277-290 (1979)
[29] Chin, N. K.; Cope, M.; Pang, M., Number and distribution of spindle capsules in seven hindlimb muscles of the cat, (Barker, D., Muscle Receptors (1962), Hong Kong University Press: Hong Kong University Press Hong-Kong), 241-248
[30] Cooper, S.; Daniel, P. M., Muscle spindles in human extrinsic eye muscles, Brain, 72, 1-24 (1949)
[31] Cooper, S.; Daniel, P. M., Muscle spindles in man; their morphology in the lumbricals and the deep muscles of the neck, Brain, 86, 563-586 (1963)
[32] Desaki, J.; Kawakita, S.; Yamagata, T., Existence of a muscle spindle on the posterior cricoarytenoid muscle of the guinea pig, J. Electron. Microsc. (Tokyo), 46, 3, 257-261 (1997)
[33] Diwan, F. H.; Milburn, A., The effects of temporary ischemia on rat muscle spindles, J. Embryol. Exp. Morphol., 92, 223-254 (1986)
[34] Dow, P. R.; Shinn, S. I.; Ovalle, W. K., Ultrastructural study of a blood-muscle spindle barrier after systemic administration of horseradish peroxidase, Am. J. Anat., 157, 375-388 (1980)
[35] Egginton, S., Temperature and angiogenesisthe possible role of mechanical factors in capillary growth, Compar. Biochem. Physiol. (A; Molec. and Integr.), 80, 1, 365-376 (2002)
[36] Eldred, E.; Bridgman, C. F.; Swett, J. E.; Eldred, B., Quantitative comparisons of muscle receptors of the cat’s medial gastrocnemius, soleus, and extensor digitorum brevis muscles, (Barker, D., Muscle Receptors (1962), Hong Kong University Press: Hong Kong University Press Hong-Kong), 207-213
[37] Eldred, E.; Yung, L.; Roy, R. R., Spindle representation relative to distribution of muscle fiber types in the cat capsularis muscle, Acta Anat., 159, 114-126 (1997)
[38] Eriksson, P. O.; Thornell, L. E., Relation to extrafusal fiber-type composition in muscle-spindle structure and location in the human masseter muscle, Arch. Oral Biol., 32, 7, 483-491 (1987)
[39] Feldman, A. G.; Levin, M. F., The origin and use of positional frames of reference in motor control, Behav. Brain Sci., 18, 723-806 (1995)
[40] Fuentes, I.; Cobos, A. R.; Segade, L. A.G, Muscle fiber types and their distribution in the biceps and triceps brachii of the rat and rabbit, J. Anat., 192, 203-210 (1998)
[41] Gladden, M. H.; Jankowska, E.; Czarkowska-Bauch, J., New observations on coupling between group II muscle afferents and feline gamma-motoneurons, J. Physiol. (Lond.), 512, 2, 507-520 (1998)
[42] Gonyea, W. J.; Eriksson, G. C., Morphological and histochemical organization of the flexor carpi radialis muscle in the cat, Am. J. Anat., 148, 329-344 (1977)
[43] Gordon, T.; Patullo, M., Plasticity of muscle fiber and motor unit types, Exerc. Sport Sci. Rev., 21, 331-362 (1993)
[44] Gray, S. D.; McDonagh, P. F.; Gore, R. W., Comparison of functional and total capillary densities in fast and slow muscles of the chicken, Pflügers Arch., 397, 209-213 (1983)
[45] Gregor, A., Ueber die verheilung der muskelspindel n in der musculatur des menschlichen fetus, Arch. Anat Physiol, Anat Abst (Hefte II und III),, 112-196 (1904)
[46] Gregory, J. E.; Wise, A. K.; Wood, S. A.; Prochazka, A.; Proske, U., Muscle history, fusimotor activity and the human stretch reflex, J. Physiol. (Lond.), 513, 3, 927-934 (1998)
[47] Hansen-Smith, F. M., Capillary network patterning during angiogenesis, Clin. Exp. Pharmacol. Physiol., 27, 10, 830-835 (2000)
[48] Hennig, R.; Lömo, T., Firing patterns of motor units in normal rats, Nature, 314, 164-166 (1985)
[49] Holtz, J., Peripheral circulationfundamental concepts, comparative aspects of control in specific vascular sections, and lymph flow, (Greger, R.; Windhorst, U., Comprehensive human physiology (1996), Springer: Springer Berlin, Heidelberg, New York), 1865-1915, (Chapter 94)
[50] Hoppeler, H.; Kayar, S. R., Capillarity and oxidative capacity of muscles, News Physiol. Sci., 3, 113-116 (1988)
[51] Houk, C., Regulation of stiffness by skeletomotor reflexes, Annu. Rev. Physiol., 41, 99-114 (1979)
[52] Houk, J. C.; Rymer, W. Z., Neural control of muscle length and tension, (Brooks, V. B., Handbook of Physiology, Motor control (1981), The American Physiological Society: The American Physiological Society Bethesda), 257-323
[53] Hulliger, M., The mammalian muscle spindle and its central control, Rev. Physiol. Biochem. Pharmacol., 101, 1-110 (1984)
[54] Jankowska, E.; Gladden, M. H., A positive feedback circuit involving muscle spindle secondaries and gamma motoneurons in the cat, Prog. Brain Res., 123, 149-156 (1999)
[55] Johnson, M. I.; Ovalle, W. K., A comparative study of muscle spindles in slow and fast neonatal muscles of normal and dystrophic mice, Am. J. Anat., 175, 413-427 (1986)
[56] Karch, R.; Neumann, F.; Neuman, M.; Schreiner, W., A three-dimensional model for arterial tree representation, generated by constrained constructive optimization, Comput. Biol. Med., 29, 19-38 (1999)
[57] Karch, R.; Neumann, F.; Neuman, M.; Schreiner, W., Functional characteristics of optimized arterial tree models perfusing volumes of different thickness and shape, J. Vasc. Res., 37, 250-264 (2000)
[58] Kierner, A. C.; Zelenka, I.; Lukas, J. R.; Aigner, M.; Mayr, R., Observations on the number, distribution and morphological peculiarities of muscle spindles in the tensor tympani and stapedius muscle in man, Hear Res., 135, 71-77 (1999)
[59] Kokkorogiannis, T., Kyriazi, L., 2001. On the distribution of muscle spindles in the human skeletal musculature. Proceedings of the 16th Congress of the Hellenic Society of Neuroscientists, HSN, Thessalonica, pp. 70-71.
[60] Lackner, J. R.; DiZio, P. A., Aspects of body self-calibration, Trends Cogn. Sci., 4, 7, 279-288 (2000)
[61] Lincoln, J.; Harb, R., Postnatal development of nitric oxide synthase activity in fast and slow muscles of the rat, Muscle Nerve, 21, 10, 1344-1346 (1998)
[62] Maeda, N.; Miyoshi, S.; Toh, H., First observation of a muscle spindle in fish, Nature, 302, 3, 61-62 (1983)
[63] Mai, J. V.; Edgerton, V. R.; Barnard, R. J., Capillarity of red, white and intermediate muscle fibers in trained and untrained guinea-pigs, Experientia, 26, 1222-1223 (1970)
[64] Maier, A., The avian muscle spindle, Anat. Embryol. (Berlin), 186, 1, 1-25 (1992)
[65] Maier, A., Proportions of slow myosin heavy chain-positive fibers in muscle spindles and adjoining extrafusal fascicles, and the positioning of spindles relative to these fascicles, J. Morphol., 242, 2, 157-165 (1999)
[66] Maier, A.; Mayne, R., Distribution of connective tissue proteins in chick muscle spindles as revealed by monoclonal antibodiesa unique distribution of brachinectin/tenascin, Am. J. Anat., 180, 226-236 (1987)
[67] Matthews, P. B.C, Mammalian Muscle Receptors and their Central Action (1972), Edward Arnold Ltd: Edward Arnold Ltd London
[68] Matthews, P. B.C, Evolving views on the internal operation and functional role of the muscle spindle, J. Physiol. (Lond.), 320, 1-30 (1981)
[69] Matthews, P. B.C, Proprioceptors and their contribution to somatosensory mappingcomplex messages require complex processing, Can. J. Physiol. Pharmacol., 66, 430-438 (1988)
[70] Matthews, P. B.C; Stein, R. B., The sensitivity of muscle spindle afferents to small sinusoidal changes in length, J. Physiol. (Lond.), 200, 723-743 (1969)
[71] Maxwell, L. C.; Barclay, J. K.; Mohrman, D. E.; Faulkner, J. A., Physiological characteristics of skeletal muscle of dogs and cats, Am. J. Physiol., 233, C14-C18 (1977)
[72] Merrillees, N.C.R., 1962. Some observations on the fine structure of a Golgi tendon organ of a rat. In: Barker D. (Ed.), Muscle receptors Hong Kong University Press, pp. 199-206.
[73] Milburn, A., Stages in the development of cat muscle spindle, J. Embryol. Exp. Morphol., 82, 177-216 (1984)
[74] Mittelstaedt, H., Somatic vs. vestibular gravity reception in man, Ann. N. Y. Acad. Sci., 656, 124-139 (1992)
[75] Myrhage, R., Capillary supply of the muscle fiber population in hindlimb muscles of the cat, Acta Physiol. Scand., 103, 19-30 (1978)
[76] Myrhage, R.; Eriksson, E., Vascular arrangements in hind limb muscles of the cat, J. Anat., 131, 1, 1-17 (1980)
[77] Nahirney, C. P.; Dow, P. R.; Ovalle, W. K., Quantitative morphology of mast cells in skeletal muscle of normal and genetically dystrophic mice, Anat. Rec., 247, 341-349 (1997)
[78] Nieuwenhuys, R.; Voogd, V.; van Huijzen, C., The Human Central Nervous System (1988), Springer: Springer Berlin, Heidelberg, New York
[79] Ovalle, W. K.; Dow, P. R.; Nahirney, P. C., Structure, distribution and innervation of muscle spindles in avian fast and slow skeletal muscle, J. Anat., 194, 3, 381-394 (1999)
[80] Pallot, D. J.; Ridge, R. M.A. P., The fine structure of the short capsule muscle spindles in snakes of Natrix sp, J. Anat., 114, 1, 13-24 (1973)
[81] Passatore, M., Filippi, G.M., Grassi, C., 1985. Cervical sympathetic nerve stimulation can induce an intrafusal muscle fiber contraction in the rabbit. In: Boyd, I.A., Gladden, M.H. (Eds.), The Muscle Spindle, Stockton Press.
[82] Passatore, M.; Deriu, F.; Grassi, C.; Roatta, S., A comparative study of changes operated by sympathetic nervous system activation on spindle afferent discharge and on tonic vibration reflex in rabbit jaw muscles, J. Auton. Nerv. Syst., 57, 163-167 (1996)
[83] Pedrosa-Domellof, F.; Virtanen, I.; Thornell, L. E., Tenascin is present in human muscle spindles and neuromuscular junctions, Neurosci. Lett., 198, 3, 173-176 (1995)
[84] Plyley, M. J.; Groom, A. C., Geometrical distribution of capillaries in mammalian striated muscle, Am. J. Physiol., 228, 5, 1376-1383 (1975)
[85] Prochazka, A.; Hulliger, M., The continuing debate about CNS control of proprioception, J. Physiol. (Lond.), 513, 2, 315 (1998)
[86] Proske, U.; Morgan, D. L.; Gregory, E., Thixotropy in muscle and in muscle spindlesa review, Prog. Neurobiol., 41, 705-721 (1993)
[87] Richmond, F. J.; Abrahams, V. C., Morphology and enzyme histochemistry of dorsal muscles of the cat neck, J. Neurophysiol., 38, 1312-1321 (1975)
[88] Richmond, F. J.; Abrahams, V. C., Morphology and distribution of muscle spindles in dorsal muscles of the cat neck, J. Neurophysiol., 38, 1322-1339 (1975)
[89] Richmond, F.J., Stacey, M.J., Bakker, G.J., Bakker, D.A., 1985. Gaps in spindle physiology: why the tandem spindle? In: Boyd, I.A., Gladden, M.H. (Eds.), The Muscle Spindle, Stockton Press, pp. 75-81.
[90] Roatta, S.; Windhorst, U.; Ljubisavljevic, M.; Johansson, H.; Passatore, M., Sympathetic modulation of muscle spindle afferent sensitivity to stretch in rabbit jaw closing muscles, J. Physiol. (Lond.), 540, 1, 237-248 (2002)
[91] Romanul, F., Distribution of capillaries in relation to oxidative metabolism of skeletal muscle fibers, Nature, 201, 307-308 (1964)
[92] Roy, R. R.; Kim, J. A.; Monti, R. J.; Zhong, H.; Edgerton, V. R., Architectural and histochemical properties of cat hip “cuff” muscles, Acta Anat., 159, 136-146 (1997)
[93] Sanes, J. R., The extracellular matrix, (Engel, A.; Franzini-Armstrong, C., Myology (1994), McGraw-Hill: McGraw-Hill New York), 242-260
[94] Santini, M.; Ibata, Y., The fine structure of thin unmyelinated axons within muscle spindles, Brain Res., 33, 289-302 (1971)
[95] Schmidt-Schönebein, G. W., Microlympahtics and lymph flow, Physiol. Rev., 70, 1, 987-1028 (1990)
[96] Schreiner, W.; Karch, R.; Neumann, M.; Neumann, F.; Roedler, S.; Heinze, G., Heterogeneous perfusion is a consequence of uniform shear stress in optimized arterial tree models, J. Theor. Biol., 220, 285-301 (2003) · Zbl 1464.92079
[97] Sciote, J. J.; Rowlerson, A., Skeletal fiber types and spindle distribution in limb and jaw muscles of the adult and neonatal opossum. Monodelphis domestica, Anat. Rec., 251, 4, 548-562 (1998)
[98] Scott, J. J.A; Young, H., The number and distribution of muscle spindles and tendon organs in the peroneal muscles of the cat, J. Anat., 151, 143-155 (1987)
[99] Shorey, C. D.; Cleland, K. W., Morphometric analysis of frozen transverse sections of human skeletal muscle taken post-mortem, Acta Anat., 131, 30-34 (1988)
[100] Siegel, G., Connective Tissuemore than just a Matrix for Cells, (Greger, R.; Windhorst, U., Comprehensive human physiology (1995), Springer: Springer Berlin, Heidelberg, New York), 173-224, (Chapter 9)
[101] Stein, R. B., What muscle variable(s) does the nervous system control in limb movements? Behav, Brain Sci., 5, 535-577 (1982)
[102] Stephens, H.R., 1985. Distribution and 3-D reconstruction of muscle spindles in mouse skeletal muscles. In: Boyd, I.A., Gladden, M.H. (Eds.), The Muscle Spindle, Stockton Press, pp. 83-93.
[103] Suzuki, J.; Kobayashi, T.; Uruma, T.; Koyama, T., Strength training with partial ischemia stimulates microvascular remodeling in rat calf muscles, Eur. J. Appl. Physiol., 82, 215-222 (2000)
[104] Swash, M., Fox, K.P., 1985. Adrenergic innervation of baboon and human muscle spindles. In: Boyd, I.A., Gladden, M.H. (Eds.), The Muscle Spindle, Stockton Press, pp. 121-126.
[105] Swett, J. E.; Eldred, E., Distribution and number of stretch receptors in medial gastrocnemius and soleus muscles, Anat. Rec., 137, 453-460 (1960)
[106] Thompson, D. A., On Growth and Form (1961), Cambridge University Press: Cambridge University Press Cambridge
[107] Vallbo, A. B., Discharge patterns in human spindle afferents during isometric voluntary contractions, Acta Physiol. Scand., 80, 552-566 (1970)
[108] Vallbo, A. B.; Hagbarth, K. E.; Torebjörk, H. E.; Wallin, B. G., Somatosensory, proprioceptive and sympathetic activity in human peripheral nerves, Physiol. Rev., 59, 919-957 (1979)
[109] Voss, H., Tabelle der absoluten und relativen muskelspindelzahlen der menschlichen skelettmuskulatur, Anat. Anz., 129, 562-572 (1971)
[110] Watanabe, K.; Suzuki, A., Distribution, density, and structure of muscle spindles in the vastus intermedius and the peroneus longus of sheep, Okajimas Folia Anatomica Japonica, 76, 203-220 (1999)
[111] Windhorst, U., How Brain Like is the Spinal Cord (1988), Springer: Springer Berlin, Heidelberg, New York, London, Paris, Tokyo
[112] Windhorst, U.; Hamm, T. M.; Stuart, D. G., On the function of muscle and reflex partitioning, Behav. Brain Sci., 12, 629-645 (1989)
[113] Yellin, H., A histochemical study of muscle spindles and their relationship to extrafusal fiber types in the rat, Am. J. Anat., 125, 31-46 (1969)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.