Research article
Early fetal development of hard tissue pulleys for the human superior oblique and tensor veli palatini muscles

https://doi.org/10.1016/j.aanat.2011.01.004Get rights and content

Abstract

The trochlea for the superior oblique muscle as well as the hamulus for the tensor veli palatini muscle is well known as a fibrocartilage-associated, hard tissue pulley that changes the direction of the tendon. However, details of the fetal development of these structures remain obscure. We carried out a histological study of hematoxylin–eosin-stained preparations from 20 human fetuses (7–15 weeks of gestation) and clarified a common rule for the formation of these pulleys: changing in the location of a structure for the muscle insertion. At the early stage, the muscle and insertion exhibit an almost straight course alongside the primitive pulley, but because the structure for insertion later moves away from a straight line along which the muscle acts, the tendon begins to turn around the cartilage by 12 weeks. The posterior shift of the soft palate is clearly evident, but rotation of the sclera or eyeball is difficult to identify in sections. To some degree, the trochlea may originate from a common anlage with the sclera. We hypothesize that, from the evolutionary point of view, the hamulus or trochlea do not form for the pulley itself but as a structure independent of the related muscle function. The fetal topographical anatomy around the tensor veli palatini, as well as its relationship to the tensor tympani, is also described.

Introduction

The presence of a fibrocartilage-associated, hard tissue pulley that reverses the course of a muscle tendon is a well known anatomical feature in both the human palate and orbit (Benjamin et al., 1995, Putz and Kroyer, 1999). The pulley for the superior oblique muscle (SO) is fibrocartilaginous and usually called the “trochlea”, while that for the tensor veli palatini muscle (TV) is bony and termed the “pterygoid hamulus”, representing an inferior extension of the medial pterygoid plate. The hamulus is formed by chondrification within the ectopterygoid elements of the mammalian pterygoid (cf. Presley and Steel, 1978, Sánches-Villagra et al., 2008 and Depew et al., 2005, respectively, for reviews on evolutionary and molecular development aspects). According to the classical description, the medial lamina of the pterygoid process and its extension, the pterygoid hamulus, develop up to the 7th month of gestation as a separate membranous bone (Peter et al., 1938, Sieglbauer, 1927). It remains unclear whether the primitive hamulus pushes the muscle anlage, thus bending it to provide a pulley. Sevel (1986) reported that, in fetuses examined at the earliest stage (CRL 26 mm; almost 7 weeks of gestation), the tendon fans out distal to the trochlea. If the tendon does not form after the appearance of the trochlea, another possibility that could be considered is that the muscle belly and tendon develop independently, and then later combine at an acute angle, thus wedging the primitive hamulus or trochlea. In fact, Rodríguez-Vázquez (2009) has reported such a secondary combination between the human stapedius muscle and its tendon, although the two are arranged at an obtuse angle to each other.

In the famous textbook by Keibel (1912), the SO, like the medial and lateral rectus muscles, is described as growing from the back of the orbit, its terminal tendon gradually passing from the anterior into the posterior portion of the eye ball. Although short, this description suggests to some extent that, in the early stage of development, the SO tendon does not turn around the trochlea but simply passes alongside it, because the anterior insertion does not require a change in tendon direction. Likewise, if the soft palate anlage is located anterior to the hamulus anlage, the same hypothesis is also probably applicable to the early development of the pterygoid hamulus. However, although many studies of the TV have been performed using mid-term or full-term fetuses (Rood, 1973, Rood and Doyle, 1978, Seif and Dellon, 1978, Klueber and Langdon, 1979, Swarts et al., 1986, Spauwen et al., 1991), none of them contain any information on the primitive morphology of the hamulus and its surrounding structures.

Consequently, to provide a better understanding of the pulley morphology, the present study has been conducted to clarify details of the early development of the SO trochlea and pterygoid hamulus using collections of human fetal sections kept at Universidad Complutense (Madrid, Spain) and Chunbuk National University (Jeonju, Korea).

Section snippets

Materials and methods

The study was performed in accordance with the provisions of the Declaration of Helsinki 1995 (as revised in Edinburgh 2000). We conducted histological examinations of paraffin-embedded sections of 20 fetuses at 7–15 weeks of gestation or estimated ovulation ages: 4 specimens each at 7 weeks (20–23 mm crown-rump length or CRL), 9 weeks (32–40 mm CRL), 12 weeks (70–85 mm CRL), 13 weeks (90–100 mm CRL) and 15 weeks (105–120 mm CRL), respectively. All sections were horizontal with a thickness of 8–10 μm

General observations

By 7 weeks, the eyeball exhibited the basic components such as the pigmented layer of the retina, cornea, conjunctiva, lens, extraocular muscles and nerves. However, in the posterior and lateral areas where the conjunctiva was not attached, the sclera could not be clearly discriminated from the surrounding mesenchymal tissues. In fetuses at 9–11 weeks, the cartilaginous nasal capsule, containing the nasal cavity and cartilaginous nasal septum, occupied a large space in the head (Fig. 1). On the

Discussion

The findings of the present study suggested a common rule for the formation of the two fibrocartilage-associated, hard tissue pulleys in the human head region (i.e., the SO trochlea and the pterygoid hamulus): changing in the location of a structure for the muscle insertion away from a straight line along which the muscle acts (Fig. 6). The related muscles, the SO and TV, exhibited an almost straight course alongside the pulley anlage in the early stage but, depending on the change in the

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