A new teaching model for demonstrating the movement of the extraocular muscles

The extraocular muscles consist of the superior, inferior, lateral, and medial rectus muscles and the superior and inferior oblique muscles. This study aimed to create a new teaching model for demonstrating the function of the extraocular muscles. A coronal section of the head was prepared and sutures attached to the levator palpebral superioris muscle and six extraocular muscles. Tension was placed on each muscle from a posterior approach and movement of the eye documented from an anterior view. All movements were clearly seen less than that of the inferior rectus muscle. To our knowledge, this is the first cadaveric teaching model for demonstrating the movements of the extraocular muscles. Clin. Anat. 30:733–735, 2017. © 2017Wiley Periodicals, Inc.     

滑车组织在眼球内旋运动时维持眼外肌力学优势的模拟研究

目的 研究眼外肌滑车系统在眼球大幅度内旋时的生物力学作用。方法 结合文献报道的眼外肌坐标参数,根据眼球运动的力学平衡原理,建立主动滑车力学模型,并以无滑车模型作为对照,模拟眼球在30°~45°范围内的内旋运动。结果 在内直肌对眼球内旋运动的贡献方面,无滑车模型的内直肌提供的作用力大于主动滑车模型,且内直肌力值明显大于生理安全极限值（约0.5 N）。在模拟眼球内旋的最大角度45°处,主动滑车模型和无滑车模型模拟得到的内直肌力分别为0.508、0.782 N,后者超过生理阈值约56%。在控制眼球运动方面,主动滑车模型消耗的能量远小于无滑车模型。结论 滑车组织的存在,使得眼外肌能够以较低的耗能控制眼球运动,加强了眼外肌对眼球的牵引作用。而且,在眼球大幅度内旋运动时,主动滑车模型维持着内直肌的力学优势。     

Comparative Study of Fibrillar Collagen Arrangement in the Corneas of Primates and Other Mammals

This study is a comparative study of the relationship between corneal structure, morphology, and function in a range of mammalian species. X‐ray scattering patterns were gathered at regular spatial intervals over the excised cornea (and in most cases also the scleral rim) of humans, marmosets, horses, cows, pigs, rabbits, and mice. All patterns were analyzed to produce quantitative information regarding the predominant orientation of fibrillar collagen throughout the tissue. The predominant direction of corneal collagen varies between mammals. This variation is not related to the size, shape, or thickness of the cornea or the frequency with which the animal blinks. A relationship does, however, appear to exist between corneal collagen arrangement and visual acuity. An excess of collagen directed toward one or both sets of opposing rectus muscles is a feature of animals that have an intermediate to high level of visual acuity. There is a significant variation in the arrangement of corneal collagen between different mammalian species. This finding may be related to differences in the frequency of action and the forces generated by the various extraocular muscles during eye movement and image fixation. Anat Rec, 2007. © 2007 Wiley‐Liss, Inc.     

Acetylcholine Receptor Organization at the Dystrophic Extraocular Muscle Neuromuscular Junction

Spared extraocular muscles of dystrophic mice are not subjected to regeneration process and can be used to verify whether the lack of dystrophin per se could cause changes in acetylcholine receptor (AChR) distribution. In the present study, rectus and oblique (spared) and retractor bulbi (nonspared) muscles were dissected from adult control (C57Bl/10) and mdx mice. AChRs and nerve terminals were labeled with rhodamine–α‐bungarotoxin and anti–NF200‐IgG‐FITC, respectively, and visualized by confocal microscopy. Rectus and oblique muscles presented 0.5% central nucleation, while retractor bulbi had central nucleation in 45% of muscle fibers. In mdx rectus, AChRs were distributed in branches in 99% of the junctions examined (n = 200), similar to that observed for controls. Nerve terminals covered the AChR branches in 100% of the junctions examined. In control retractor bulbi, AChRs were distributed in regular branches. In mdx retractor bulbi, multiple fragmented islands of receptors were seen in 56% of the endplates examined (n = 200). These results suggest that the lack of dystrophin per se does not influence the distribution of acetylcholine receptors at the neuromuscular junction of spared extraocular muscles. Anat Rec, 2007. © 2007 Wiley‐Liss, Inc.     

Contractile properties and temperature sensitivity of the extraocular muscles, the levator and superior rectus, of the rabbit.

1. Contractile and fatigue-resistance characteristics, temperature sensitivity (10-37 degrees C) of contraction, and histochemical fibre types were determined for two of the extraocular muscles, the superior rectus and levator palpebrae superioris (levator), of the rabbit. 2. The levator displayed similar contractile characteristics (time to peak, half-relaxation time of twitch response, and twitch-tetanus force ratio) to mammalian fast-twitch limb muscle at room temperature (20 degrees C). However, normalized twitch and tetanic force levels were significantly less than those found in limb muscle. The superior rectus displayed the characteristics of even faster contraction than the levator at 20 degrees C, but generated lower maximum force levels than the levator. 3. The twitch response of the superior rectus showed a biphasic relaxation phase. This response was not due to non-twitch (tonic) fibres present in the superior rectus as it was unaffected by propranolol application during muscle stimulation. 4. The superior rectus and levator displayed significantly less fatigue in the tetanic force response than fast-twitch limb muscles did in response to a fatiguing electrical stimulation protocol. The levator was significantly more fatigue resistant than the superior rectus. 5. The force responses of both extraocular muscles displayed a similar dependence on temperature (10-37 degrees C) to limb skeletal muscles. 6. The superior rectus and levator exhibited a high proportion of fast-twitch muscle fibres (type II) as shown by myosin ATPase staining. Succinate dehydrogenase activity indicated that these muscles showed a high oxidative capacity, with a staining intensity typical of type I or type II A fibres of limb muscles. 7. The results emphasize the morphological and functional complexity of mammalian extraocular muscles. The combination of very fast contractile properties with high oxidative capacity make these muscles well suited to their role in eye/eyelid movement.     

Motoneuronal innervation and mechanical properties of extraocular muscles in the catfish, (Ictalurus punctatus)

Mechanical characteristics and electrical activity were studied in the extraocular muscles of the catfish, Ictalurus punctatus. The contractile properties were determined by stimulation of the individual muscle nerve branches to lateral and medial rectii and the superior and inferior oblique muscles. The speed of contraction was higher than in most other fish muscle, with a twitch contraction time of about 12 ms and a tetanus fusion frequency of 150–170 Hz in all four eye muscles. The fatigue resistance was also high. These properties were the same in fully innervated and partially innervated muscle, largely irrespective of what part of the muscle that was activated. Although different fibre types are known to exist in fish extraocular muscle, it was not possible to obtain functional separation of the mechanical force profile even in the lateral rectus with two distinct motoneuronal innervations. We suggest that polyneuronal innervation of the muscle fibres produces the mechanical responses. Since EMG activity during spontaneous eye movements was similar in the global and the orbital parts of the muscle, all types of fibres in fish extraocular muscle are probably recruited for all types of eye movements.     

The vestibuloocular reflex of the adult flatfish. I. Oculomotor organization

The flatfish species constitute a natural paradigm for investigating adaptive changes in the vertebrate central nervous system. During metamorphosis all species of flatfish experience a 90 degree change in orientation between their vestibular and extraocular coordinate axes. As a result, the optic axes of both eyes maintain their orientation with respect to earth horizontal, but the horizontal semicircular canals become oriented vertically. Since the flatfish propels its body with the same swimming movements when referenced to the body as a normal fish, the horizontal canals are exposed to identical accelerations, but in the flatfish these accelerations occur in a vertical plane. The appropriate compensatory eye movements are simultaneous rotations of both eyes forward or backward (i.e., parallel), in contrast to the symmetric eye movements in upright fish (i.e., one eye moves forward, the other backward). Therefore, changes in the extraocular muscle arrangement and/or the neuronal connectivity are required. This study describes the peripheral and central oculomotor organization in the adult winter flounder, Pseudopleuronectes americanus. At the level of the peripheral oculomotor apparatus, the sizes of the horizontal extraocular muscles (lateral and medial rectus) were considerably smaller than those of the vertical eye muscles, as quantified by fiber counts and area measurements of cross sections of individual muscles. However, the spatial orientations and the kinematic characteristics of all six extraocular muscles were not different from those described in comparable lateral-eyed animals. There were no detectable asymmetries between the left and the right eye. Central oculomotor organization was investigated by extracellular horseradish peroxidase injections into individual eye muscles. Commonly described distributions of extraocular motor neurons in the oculomotor, trochlear, and abducens nuclei were found. These motor neuron pools consisted of two contralateral (superior rectus and superior oblique) and four ipsilateral populations (inferior oblique, inferior rectus, medial rectus, and lateral rectus). The labeled cells formed distinct motor neuron populations, which overlapped little. As expected, the numbers of labeled motoneurons differed in horizontal and vertical eye movers. The numerical difference was especially prominent in comparing the abducens nucleus with one of the vertical recti subdivisions. Nevertheless, there was bilateral symmetry between the motoneurons projecting to the left and right eyes.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of electrode penetrations into the abducens nucleus of the monkey: eye movement recordings and histopathological evaluation of the nuclei and lateral rectus muscles

Two adult rhesus monkeys that had undergone 2 years of electrode penetrations into their abducens and vestibular nuclei, for chronic eye movement studies, were examined histologically. An analysis of their VIth nucleus neurons and lateral rectus muscles revealed the following. Twenty-two percent of the large neurons (30 µm in diameter), on average, were missing and extensive neuropil disruption and gliosis was evident in the experimental side abducens nuclei as compared with the control side in each animal. While the lateral rectus muscles showed small, but inconsistent, changes in total fiber number, the muscle fiber diameters were altered, leading to a more homogenous muscle and making the typical orbital and global subdivisions of the muscle less distinct. Eye movement records from before and after the electrophysiological studies were comparable. We discuss how the complex architecture of the extraocular muscles as well as the possibility of polyneuronal innervation of single muscle fibers could explain our results.     

Specific force of the rat extraocular muscles, levator and superior rectus, measured in situ

Extraocular muscles are characterized by their faster rates of contraction and their higher resistance to fatigue relative to limb skeletal muscles. Another often reported characteristic of extraocular muscles is that they generate lower specific forces (sP(o), force per muscle cross-sectional area, kN/m(2)) than limb skeletal muscles. To investigate this perplexing issue, the isometric contractile properties of the levator palpebrae superioris (levator) and superior rectus muscles of the rat were examined in situ with nerve and blood supply intact. The extraocular muscles were attached to a force transducer, and the cranial nerves exposed for direct stimulation. After determination of optimal muscle length (L(o)) and stimulation voltage, a full frequency-force relationship was established for each muscle. Maximum isometric tetanic force (P(o)) for the levator and superior rectus muscles was 177 +/- 13 and 280 +/- 10 mN (mean +/- SE), respectively. For the calculation of specific force, a number of rat levator and superior rectus muscles were stored in a 20% nitric acid-based solution to isolate individual muscle fibers. Muscle fiber lengths (L(f)) were expressed as a percentage of overall muscle length, allowing a mean L(f) to L(o) ratio to be used in the estimation of muscle cross-sectional area. Mean L(f):L(o) was determined to be 0.38 for the levator muscle and 0.45 for the superior rectus muscle. The sP(o) for the rat levator and superior rectus muscles measured in situ was 275 and 280 kN/m(2), respectively. These values are within the range of sP(o) values commonly reported for rat skeletal muscles. Furthermore P(o) and sP(o) for the rat levator and superior rectus muscles measured in situ were significantly higher (P < 0.001) than P(o) and sP(o) for these muscles measured in vitro. The results indicate that the force output of intact extraocular muscles differs greatly depending on the mode of testing. Although in vitro evaluation of extraocular muscle contractility will continue to reveal important information about this group of understudied muscles, the lower sP(o) values of these preparations should be recognized as being significantly less than their true potential. We conclude that extraocular muscles are not intrinsically weaker than skeletal muscles.     

Eye and neck proprioceptive messages contribute to the spatial coding of retinal input in visually oriented activities

Summary The egocentric localization of objects in extrapersonal space requires that the retinal and extraretinal signals specifying the gaze direction be simultaneously processed. The question as to whether the extraretinal signal is of central or peripheral origin is still a matter of controversy, however. Three experiments were carried out to investigate the following hypotheses: 1) that the proprioceptive feedback originating in eye and neck muscles might provide the CNS with some indication about the gaze direction; and 2) that the retinal and proprioceptive extraretinal inputs might be jointly processed depending on whether they are of monocular or binocular origin. Application of low amplitude mechanical vibrations to either the extraocular or neck muscles (or both) of a subject looking monocularly at a small luminous target in darkness resulted in an illusory movement of the target, the direction of which depended on which muscle was stimulated. A slow upward target displacement occurred on vibrating the eye inferior rectus or the neck sterno-cleido-mastoidus muscles, whereas a downward shift was induced when the dorsal neck muscles (trapezius and splenius) were vibrated. The extent of the perceptual effects reported by subjects was measured in an open-loop pointing task in which they were asked to point at the perceived position of the target. These results extend to visually-oriented behavior the role of extraocular and neck proprioceptive inputs previously described in the case of postural regulation, since they clearly show that these messages contribute to specifying the gaze direction. This suggests that the extraretinal signal might include a proprioceptive component. The proposition that a directional body reference frame may be based on the common processing of various proprioceptive feedbacks is discussed.     

Contractile properties of single skinned fibres from the extraocular muscles, the levator and superior rectus, of the rabbit.

1. The superior rectus and levator palpebrae superioris (levator), two of the extraocular muscles, were dissected from the rabbit and stored in a glycerol-based solution at -20 degrees C in order to prepare single, skinned fibres. 2. The Ca(2+)- and Sr(2+)-activated isometric contractile properties were determined for individual extraocular muscle fibres. Fibres were separated into discrete groups or fibre types on the basis of their physiological characteristics. The superior rectus and levator muscles were both found to consist of fibres which exhibited similar contractile characteristics to fast- and slow-twitch fibres from other mammalian muscle, including type I, type IIA and type IIB fibres. 3. As well as the existence of the normal, classical fibre types in extraocular muscle there were also a large number of fibres from both muscles which exhibited mixed fast- and slow-twitch contractile characteristics within the single contracting unit. Of the fibres sampled, the mixed fibres comprised the second largest population (7/19, 37%) in the levator and the largest fibre population in the superior rectus (11/31, 35.5%). These results are consistent with histochemical and immunohistochemical reports in the literature which suggest the co-existence of fast and slow myosin along the length of the extraocular muscle fibres. 4. Extraocular muscle fibres exhibited lower absolute maximum forces compared with other mammalian limb muscle fibres. However, when corrected for fibre cross-sectional area, the maximum tension development was within the normal range for mammalian limb muscle fibres, except for one group (type IIA) of fast-twitch fibres which exhibited significantly lower maximal tension. 5. The existence of a large proportion of fibres with composite fast- and slow-twitch characteristics highlights the functional and morphological complexity of these muscles. It is postulated that the functional significance of these mixed fibres may be to provide or enhance the resolution for subtle, precise movements of the eye and eyelid.     

Peripheral Muscle Targets and Central Projections of the Mesencephalic Trigeminal Nucleus in Macaque Monkeys

The mesencephalic trigeminal nucleus (MesV) contains the somata of primary afferent neurons that innervate muscle spindles in masticatory muscles and mechanoreceptors in the periodontal ligaments. There are conflicting reports about additional peripheral targets of MesV, such as the extraocular muscles, as well as about its central targets. In addition, only limited primate data are available. Consequently, we examined MesV projections in macaque monkeys. The retrograde tracer wheat germ agglutinin‐conjugated horseradish peroxidase (WGA‐HRP) was injected into masticatory or extraocular muscles to define the peripheral targets of the primate MesV. Numerous labeled neurons were found in ipsilateral MesV after masticatory muscle injections. The scattered distribution of labeled cells, and their presence among clusters of unlabeled cells, suggests the muscle representations overlap. Just a few MesV neurons were labeled after extraocular muscle injections. This correlates with the small number of muscle spindles present in macaque extraocular muscles, suggesting MesV cells supplying extraocular muscle spindles may contribute a minor component to oculomotor proprioception. To examine the central connections of MesV, biotinylated dextran amine (BDA) was injected into the spinal trigeminal nucleus (Vs). The presence of retrogradely labeled MesV cells indicated a projection to Vs from MesV. These injections also anterogradely labeled terminals that lay in close association with MesV cells, suggesting an ascending projection from Vs to MesV. Finally, a small number of MesV neurons were labeled after WGA‐HRP injections into the upper cervical spinal cord. This pattern of central connections indicates MesV and Vs information is combined to guide mastication. Anat Rec, 291:974–987, 2008. © 2008 Wiley‐Liss, Inc.     

Functional variation of neck muscles and their relation to feeding style in Tyrannosauridae and other large theropod dinosaurs

Reconstructed neck muscles of large theropod dinosaurs suggest influences on feeding style that paralleled variation in skull mechanics. In all examined theropods, the head dorsiflexor m. transversospinalis capitis probably filled in the posterior dorsal concavity of the neck, for a more crocodilian‐ than avian‐like profile in this region. The tyrannosaurine tyrannosaurids Daspletosaurus and Tyrannosaurus had relatively larger moment arms for lateroflexion by m. longissimus capitis superficialis and m. complexus than albertosaurine tyrannosaurids, and longer dorsiflexive moment arms for m. complexus. Areas of dorsiflexor origination are significantly larger relative to neck length in adult Tyrannosaurus rex than in other tyrannosaurids, suggesting relatively large muscle cross‐sections and forces. Tyrannosaurids were not particularly specialized for neck ventroflexion. In contrast, the hypothesis that Allosaurus co‐opted m. longissimus capitis superficialis for ventroflexion is strongly corroborated. Ceratosaurus had robust insertions for the ventroflexors m. longissimus capitis profundus and m. rectus capitis ventralis. Neck muscle morphology is consistent with puncture‐and‐pull and powerful shake feeding in tyrannosaurids, relatively rapid strikes in Allosaurus and Ceratosaurus, and ventroflexive augmentation of weaker jaw muscle forces in the nontyrannosaurids. Anat Rec, 290:934–957, 2007. © 2007 Wiley‐Liss, Inc.     

Expression of Utrophin at Dystrophin‐Deficient Neuromuscular Synapses of mdx Mice: A Study of Protected and Affected Muscles

In mdx mice, intrinsic laryngeal muscles are spared and sternomastoid muscles are affected, showing cycles of muscle regeneration. We observed that utrophin and acetylcholine receptors are fragmented only in affected muscles, providing further evidence that changes in the overall distribution of molecules at dystrophic neuromuscular junctions may be correlated with muscle regeneration. Anat Rec, 2011. © 2010 Wiley‐Liss, Inc.     

DiceCT Analysis of the Extreme Gouging Adaptations Within the Masticatory Apparatus of the Aye-Aye (Daubentonia madagascariensis)

Relative to all other primates, the aye-aye (Daubentonia madagascariensis) exists at the extremes of both morphology and behavior. Its specialized anatomy—which includes hypselodont incisors and highly derived manual digits—reflects a dietary niche, unique among primates, which combines tap-foraging with gouging to locate and extract wood-boring larvae. Here, we explore the impact of this extreme dietary ecology upon the masticatory musculature of this taxon with reference to a second, similarly sized but highly generalist lemuriform—the mongoose lemur (Eulemur mongoz). Using non-destructive, high-resolution diffusible iodine-based contrast-enhanced computed tomography techniques, we reconstruct the three-dimensional volumes of eight masticatory muscles, and, for the first time in strepsirrhines, isolate and visualize their constituent muscle fascicles in situ and in three dimensions. Using these data, we report muscle volumes, forces, and fascicle lengths from each muscle portion, as well as their orientation relative to two standardized anatomical planes. Our findings demonstrate the overbuilt nature of the aye-aye's masticatory apparatus, in which each muscle possesses an absolutely and relatively larger muscle volume and PCSA than its counterpart in the mongoose lemur. Likewise, for several adductor muscles, aye-ayes also possess relatively greater fascicle lengths. Finally, we note several unusual features within the lateral pterygoid of the aye-aye—the muscle most responsible for jaw protrusion—that relate to force maximization and reorientation. As this jaw motion is critical to gouging, we interpret these differences to reflect highly specific specializations that facilitate the aye-aye's extreme subsistence strategy. Anat Rec, 2019. © 2019 American Association for Anatomy Anat Rec, 303:282–294, 2020. © 2019 American Association for Anatomy     

A Comparison of Common Hippopotamus (Artiodactyla) and Mysticete (Cetacea) Nostrils: An Open and Shut Case

Hippos are considered the closest living relatives to cetaceans and they have some similar adaptations for aquatic living, such as a modified respiratory tract. Behavioral observations of male and female common hippos (Hippopotamus amphibius) at Disney's Animal Kingdom® and the Adventure Aquarium were conducted to describe and examine movements of the nostrils during respiration (inspiration, expiration, and inter-breath interval). The hippo nostril is a crescent shaped opening with lateral and medial aspects that are mobile and can be adducted and abducted to regulate the nostril opening. Notably, the default (resting) position of the nostrils is closed during the inter-breath interval, even when hippos are resting in water and their heads are not submerged. Similar to cetaceans, this aquatic adaptation protects the respiratory tract from an accidental incursion of water that can occur even when the nostrils are above water. Dissection of a deceased captive common hippo suggests there are separate muscles that pull the medial and lateral aspects for abduction. The internal nasal passage has a nasal plug that is similar in shape but less pronounced than the nasal plugs of two baleen whale species studied (minke whale Balaenoptera acutorostrata, fin whale Balaenoptera physalus). Examination of the musculature suggests fibers attach from the premaxillae and extend caudally to retract the plug to open the nasal passage. We discuss similarities and differences of the nostrils/blowholes of fully aquatic, semi-aquatic, and terrestrial species to assess adaptations related to environmental conditions that may be convergent or derived from a common ancestor. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:693–702, 2019. © 2018 Wiley Periodicals, Inc.     

Lessons from Amphioxus Bauplan About Origin of Cranial Nerves of Vertebrates That Innervates Extrinsic Eye Muscles

Amphioxus is the living chordate closest to the ancestral form of vertebrates, and in a key position to reveal essential aspects of the evolution of the brain Bauplan of vertebrates. The dorsal neural cord of this species at the larval stage is characterized by a small cerebral vesicle at its anterior end and a large posterior region. The latter is comparable in some aspects to the hindbrain and spinal cord regions of vertebrates. The rostral end of the cerebral vesicle contains a median pigment spot and associated rows of photoreceptor and other nerve cells; this complex is known as “the frontal eye.” However, this is not a complete eye in the sense that it has neither eye muscles nor lens (only a primitive retina-like tissue). Cranial nerves III, IV, and VI take part in the motor control of eye muscles in all vertebrates. Using a recent model that postulates distinct molecularly characterized hypothalamo-prethalamic and mesodiencephalic domains in the early cerebral vesicle of amphioxus, we analyze here possible scenarios for the origin from the common ancestor of cephalochordates and vertebrates of the cranial nerves related with extrinsic eye muscle innervations. Anat Rec, 302:452–462, 2019. © 2018 Wiley Periodicals, Inc.