Skip to main content
Erschienen in: Surgical and Radiologic Anatomy 1/2017

13.02.2016 | Original Article

Distance between intramuscular nerve and artery in the extraocular muscles: a preliminary immunohistochemical study using elderly human cadavers

verfasst von: Kei Kitamura, Kwang Ho Cho, Hyung Suk Jang, Gen Murakami, Masahito Yamamoto, Shin-ichi Abe

Erschienen in: Surgical and Radiologic Anatomy | Ausgabe 1/2017

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Extraocular muscles are quite different from skeletal muscles in muscle fiber type and nerve supply; the small motor unit may be the most well known. As the first step to understanding the nerve–artery relationship, in this study we measured the distance from the arteriole (25–50 μm in thickness) to the nerve terminal twigs in extraocular muscles.

Materials and methods

With the aid of immunohistochemistry for nerves and arteries, we examined the arteriole–nerve distance at 10–15 sites in each of 68 extraocular muscles obtained from ten elderly cadavers. The oblique sections were nearly tangential to the muscle plate and included both global and orbital aspects of the muscle.

Results

In all muscles, the nerve twigs usually took a course parallel to muscle fibers, in contrast to most arterioles that crossed muscles. Possibly due to polyinnervation, an intramuscular nerve plexus was evident in four rectus and two oblique muscles. The arteriole–nerve distance usually ranged from 300 to 400 μm. However, individual differences were more than two times greater in each of seven muscles. Moreover, in each muscle the difference between sites sometimes reached 1 mm or more. The distance was generally shorter in the rectus and oblique muscles than in the levator palpebrae muscle, which reached statistical significance (p < 0.05).

Conclusions

The differences in arteriole–nerve distances between sites within each muscle, between muscles, and between individuals might lead to an individual biological rhythm of fatigue in oculomotor performance.
Literatur
1.
Zurück zum Zitat Abe S, Fukuda M, Yamane S, Saka H, Katori Y, Rodríguez-Vázquez JF, Murakami G (2013) Fetal anatomy of the upper pharyngeal muscles with special reference to the nerve supply: is it an enteric plexus or simply an intramuscular nerve? Anat Cell Biol 46:141–148CrossRefPubMedPubMedCentral Abe S, Fukuda M, Yamane S, Saka H, Katori Y, Rodríguez-Vázquez JF, Murakami G (2013) Fetal anatomy of the upper pharyngeal muscles with special reference to the nerve supply: is it an enteric plexus or simply an intramuscular nerve? Anat Cell Biol 46:141–148CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Abe S, Kikuchi R, Nakao T, Cho BH, Murakami G, Ide Y (2012) Nerve terminal distribution in the human tongue intrinsic muscles: an immunohistochemical study using mid-term fetuses. Clin Anat 25:189–197CrossRefPubMed Abe S, Kikuchi R, Nakao T, Cho BH, Murakami G, Ide Y (2012) Nerve terminal distribution in the human tongue intrinsic muscles: an immunohistochemical study using mid-term fetuses. Clin Anat 25:189–197CrossRefPubMed
3.
Zurück zum Zitat Asmussen G, Punkt K, Bartsch B, Soukup T (2008) Specific metabolic properties of rat oculorotatory extraocular muscles can be linked to their low force requirements. Invest Ophthalmol Vis Sci 49:4865–4871CrossRefPubMed Asmussen G, Punkt K, Bartsch B, Soukup T (2008) Specific metabolic properties of rat oculorotatory extraocular muscles can be linked to their low force requirements. Invest Ophthalmol Vis Sci 49:4865–4871CrossRefPubMed
4.
Zurück zum Zitat Bishop KN, McClung JR, Goldberg SJ, Shall MS (1985) Anatomic and physiological characteristics of the ferret lateral rectus muscle and abducens nucleus. J Appl Physiol 103:1706–1714CrossRef Bishop KN, McClung JR, Goldberg SJ, Shall MS (1985) Anatomic and physiological characteristics of the ferret lateral rectus muscle and abducens nucleus. J Appl Physiol 103:1706–1714CrossRef
5.
Zurück zum Zitat Chang H, Cho KH, Hayashi S, Kim JH, Abe H, Rodríguez-Vázquez JF, Murakami G (2014) Site-dependent difference in vascular density of the human fetal brain. Childs Nerv Syst 30:399–409CrossRefPubMed Chang H, Cho KH, Hayashi S, Kim JH, Abe H, Rodríguez-Vázquez JF, Murakami G (2014) Site-dependent difference in vascular density of the human fetal brain. Childs Nerv Syst 30:399–409CrossRefPubMed
6.
Zurück zum Zitat Cordier J, Rauber G, Raspiller A, Sirbat D (1980) Arterial vascularization of the rectus medialis and lateralis muscles. J Fr Ophthalmol 3:731–736 Cordier J, Rauber G, Raspiller A, Sirbat D (1980) Arterial vascularization of the rectus medialis and lateralis muscles. J Fr Ophthalmol 3:731–736
7.
Zurück zum Zitat Croes SA, von Bartheld CS (2007) Measurement of contractile force of skeletal and extraocular muscles: effects of blood supply, muscle size and in situ or in vitro preparation. J Neurosci Methods 166:53–65CrossRefPubMedPubMedCentral Croes SA, von Bartheld CS (2007) Measurement of contractile force of skeletal and extraocular muscles: effects of blood supply, muscle size and in situ or in vitro preparation. J Neurosci Methods 166:53–65CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Cruse JP, Edwards DAW, Smith JF, Wyllie JH (1979) The pathology of a cricopharyngeal dysphagia. Histopathology 3:222–232CrossRef Cruse JP, Edwards DAW, Smith JF, Wyllie JH (1979) The pathology of a cricopharyngeal dysphagia. Histopathology 3:222–232CrossRef
9.
Zurück zum Zitat Demer JL, Miller JM, Poukens V, Vinters HV, Glasgow BJ (1995) Evidence for fibromuscular pulleys of the recti extraocular muscles. Investig Ophthalmol Vis Sci 36:1125–1136 Demer JL, Miller JM, Poukens V, Vinters HV, Glasgow BJ (1995) Evidence for fibromuscular pulleys of the recti extraocular muscles. Investig Ophthalmol Vis Sci 36:1125–1136
10.
Zurück zum Zitat Demer JL, Poukens V, Miller JM, Micevych P (1997) Innervation of extraocular pulley smooth muscles in monkeys and humans. Investig Ophthalmol Vis Sci 38:227–240 Demer JL, Poukens V, Miller JM, Micevych P (1997) Innervation of extraocular pulley smooth muscles in monkeys and humans. Investig Ophthalmol Vis Sci 38:227–240
11.
Zurück zum Zitat Dimitrova DM, Allman BL, Shall MS, Goldberg SJ (2009) Polyneuronal innervation of single muscle fibers in cat eye muscle: inferior oblique. J Neurophysiol 101:2815–2821CrossRefPubMedPubMedCentral Dimitrova DM, Allman BL, Shall MS, Goldberg SJ (2009) Polyneuronal innervation of single muscle fibers in cat eye muscle: inferior oblique. J Neurophysiol 101:2815–2821CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Frueh BR, Gregorevic P, Williams DA, Lynch GS (2001) Specific force of the rat extraocular muscles, levator and superior rectus, measured in situ. J Neurophysiol 85:1027–1032PubMed Frueh BR, Gregorevic P, Williams DA, Lynch GS (2001) Specific force of the rat extraocular muscles, levator and superior rectus, measured in situ. J Neurophysiol 85:1027–1032PubMed
13.
Zurück zum Zitat Fujii Y, Abe J, Nunomura S, Moriuchi T, Hizawa K (1990) Immunohistochemical study of fiber types in human extraocular muscles. Acta Pathol Jpn 40:808–814PubMed Fujii Y, Abe J, Nunomura S, Moriuchi T, Hizawa K (1990) Immunohistochemical study of fiber types in human extraocular muscles. Acta Pathol Jpn 40:808–814PubMed
14.
Zurück zum Zitat Hayashi S, Murakami G, Ohtsuka A, Itoh M, Nakano T, Fukuzawa Y (2008) Connective tissue configuration in the human liver hilar region with special reference to the liver capsule and vascular sheath. J Hepatobiliary Pancreat Surg 15:640–647CrossRefPubMed Hayashi S, Murakami G, Ohtsuka A, Itoh M, Nakano T, Fukuzawa Y (2008) Connective tissue configuration in the human liver hilar region with special reference to the liver capsule and vascular sheath. J Hepatobiliary Pancreat Surg 15:640–647CrossRefPubMed
15.
Zurück zum Zitat Hieda K, Cho KH, Arakawa T, Fujimiya M, Murakami G, Matsubara M (2013) Nerves in the intersphincteric space of the human anal canal with special reference to their continuation to the enteric nerve plexus of the rectum. Clin Anat 26:843–854PubMed Hieda K, Cho KH, Arakawa T, Fujimiya M, Murakami G, Matsubara M (2013) Nerves in the intersphincteric space of the human anal canal with special reference to their continuation to the enteric nerve plexus of the rectum. Clin Anat 26:843–854PubMed
16.
Zurück zum Zitat Jang HS, Cho KH, Hieda K, Kim JH, Murakami G, Abe S, Matsubara A (2015) Composite nerve fibers in the hypogastric and pelvic splanchnic nerves: an immunohistochemical study using elderly cadavers. Anat Cell Biol 48:114–123CrossRefPubMedPubMedCentral Jang HS, Cho KH, Hieda K, Kim JH, Murakami G, Abe S, Matsubara A (2015) Composite nerve fibers in the hypogastric and pelvic splanchnic nerves: an immunohistochemical study using elderly cadavers. Anat Cell Biol 48:114–123CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Khanna S, Liao K, Kaminski HJ, Tomsak RL, Joshi A, Leigh RJ (2007) Ocular myasthenia revisited: insights from pseudo-internuclear ophthalmoplegia. J Neurol 254(11):1569–1574CrossRefPubMed Khanna S, Liao K, Kaminski HJ, Tomsak RL, Joshi A, Leigh RJ (2007) Ocular myasthenia revisited: insights from pseudo-internuclear ophthalmoplegia. J Neurol 254(11):1569–1574CrossRefPubMed
18.
Zurück zum Zitat Kjellgren D, Thornell LE, Anderssen J, Pedrosa-Domellőf F (2003) Myosin heavy chain isoforms in human extraocular muscles. Invest Ophthalmol Vis Sci 44:1419–1425CrossRefPubMed Kjellgren D, Thornell LE, Anderssen J, Pedrosa-Domellőf F (2003) Myosin heavy chain isoforms in human extraocular muscles. Invest Ophthalmol Vis Sci 44:1419–1425CrossRefPubMed
20.
Zurück zum Zitat Rashed RM, El-Alfy SH, Mohamed IK (2010) Histochemical analysis of muscle fiber types of rat superior rectus extraocular muscle. Acta Histochem 112:536–545CrossRefPubMed Rashed RM, El-Alfy SH, Mohamed IK (2010) Histochemical analysis of muscle fiber types of rat superior rectus extraocular muscle. Acta Histochem 112:536–545CrossRefPubMed
21.
Zurück zum Zitat Ringel SP, Wilson WB, Barden MT, Kaiser KK (1978) Histochemistry of human extraocular muscle. Arch Ophthalmol 96:1067–1072CrossRefPubMed Ringel SP, Wilson WB, Barden MT, Kaiser KK (1978) Histochemistry of human extraocular muscle. Arch Ophthalmol 96:1067–1072CrossRefPubMed
22.
Zurück zum Zitat Schalén L, Pyykkő I, Juhola M, Magnusson M, Jäntti V, Henriksson N (1984) Intra-individual variation in oculomotor performance in man. Acta Otolaryngol Suppl 406:212–217PubMed Schalén L, Pyykkő I, Juhola M, Magnusson M, Jäntti V, Henriksson N (1984) Intra-individual variation in oculomotor performance in man. Acta Otolaryngol Suppl 406:212–217PubMed
Metadaten
Titel
Distance between intramuscular nerve and artery in the extraocular muscles: a preliminary immunohistochemical study using elderly human cadavers
verfasst von
Kei Kitamura
Kwang Ho Cho
Hyung Suk Jang
Gen Murakami
Masahito Yamamoto
Shin-ichi Abe
Publikationsdatum
13.02.2016
Verlag
Springer Paris
Erschienen in
Surgical and Radiologic Anatomy / Ausgabe 1/2017
Print ISSN: 0930-1038
Elektronische ISSN: 1279-8517
DOI
https://doi.org/10.1007/s00276-016-1642-9

Weitere Artikel der Ausgabe 1/2017

Surgical and Radiologic Anatomy 1/2017 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.