The pattern of innervation of the extrinsic ocular muscles and the intra‐orbital ganglia of the albino mouse

Mahran, Z. Y.; Sakla, Francois B.

doi:10.1002/ar.1091520208

Cited by 21 publications

(6 citation statements)

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“…While primates and cats have long served as models of choice for visuomotor research, the mouse is an increasingly important model for the field. In early studies, the pattern of nerves supplying the extraocular muscles (EOMs) was characterized in mice (Mahran and Sakla, ; Biscoe et al, ; Paterson and Kaiserman‐Abramof, ). More recently, mouse models have been used to investigate eye muscle disorders (Porter et al, ,b; Spencer and Porter, ; Kallestad et al, ).…”

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“…Abbreviations: 4V = fourth ventricle; aVI = accessory abducens nucleus; BC = brachium conjunctivum; CA = cerebral aqueduct; CG = central gray; DR = dorsal raphe; EWcp = centrally projecting Edinger-Westphal nucleus; III = oculomotor nucleus; IO = inferior oblique muscle; IV = trochlear nucleus; LP = levator palpebrae superioris muscle; LR = lateral rectus muscle; MLF = medial longitudinal fasciculus; MR = medial rectus muscle; MRF = mesencephalic reticular formation; ON = optic nerve; PAG = periaqueductal gray; PPRF = paramedian pontine reticular formation; RB = retractor bulbi muscle; SC = superior colliculus; SO = superior oblique muscle; SOA = supraoculomotor area; SOt = superior oblique tendon; SR = superior rectus muscle; Tr = trochlea; VI = abducens nucleus; VIIg = genu of the facial nerve; VIIn = facial nerve; Vs = spinal trigeminal nucleus; WGA-HRP = wheat germ agglutinin conjugated horseradish peroxidase While primates and cats have long served as models of choice for visuomotor research, the mouse is an increasingly important model for the field. In early studies, the pattern of nerves supplying the extraocular muscles (EOMs) was characterized in mice (Mahran and Sakla, 1965;Biscoe et al, 1975;Paterson and Kaiserman-Abramof, 1981). More recently, mouse models have been used to investigate eye muscle disorders (Porter et al, 2003a,b;Spencer and Porter, 2006;Kallestad et al, 2011).…”

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Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Bohlen

Bui

Stahl

et al. 2019

The Anatomical Record

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The organization of extraocular muscles (EOMs) and their motor nuclei was investigated in the mouse due to the increased importance of this model for oculomotor research. Mice showed a standard EOM organization pattern, although their eyes are set at the side of the head. They do have more prominent oblique muscles, whose insertion points differ from those of frontal‐eyed species. Retrograde tracers revealed that the motoneuron layout aligns with the general vertebrate plan with respect to nuclei and laterality. The mouse departed in some significant respects from previously studied species. First, more overlap between the distributions of muscle‐specific motoneuronal pools was present in the oculomotor nucleus (III). Furthermore, motoneuron dendrites for each pool filled the entire III and extended beyond the edge of the abducens nucleus (VI). This suggests mouse extraocular motoneuron afferents must target specific pools based on features other than dendritic distribution and nuclear borders. Second, abducens internuclear neurons are located outside the VI. We concluded this because no unlabeled abducens internuclear neurons were observed following lateral rectus muscle injections and because retrograde tracer injections into the III labeled cells immediately ventral and ventrolateral to the VI, not within it. This may provide an anatomical substrate for differential input to motoneurons and internuclear neurons that allows rodents to move their eyes more independently. Finally, while soma size measurements suggested motoneuron subpopulations supplying multiply and singly innervated muscle fibers are present, markers for neurofilaments and perineuronal nets indicated overlap in the size distributions of the two populations. Anat Rec, 302:1865–1885, 2019. © 2019 American Association for Anatomy

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Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Bohlen

Bui

Stahl

et al. 2019

The Anatomical Record

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“…Extraocular muscles (EOMs) take an exceptional position as classical proprioceptors show a broad interspecies variation in their occurrence [21]. Specifically, muscle spindles can only be found in EOMs of mice [20], even-toed ungulates (goat, sheep, pig, camel, cow) [21], monkeys [12], and humans [4, 18, 23]. While muscle spindles in EOMs of ungulates are comparable with those in other skeletal muscles, muscle spindles in monkey and human EOMs exhibit structural particularities.…”

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Palisade endings are present in canine extraocular muscles and have a cholinergic phenotype

Rungaldier

Pomikal

Streicher

et al. 2009

Neuroscience Letters

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Classical proprioceptors, like Golgi tendon organs and muscle spindles are absent in the extraocular muscles (EOMs) of most mammals. Instead, a nerve end organ was detected in the EOMs of each species including sheep, cats, rabbits, rats, monkeys, and man examined so far: the palisade ending. Until now no evidence appeared that palisade endings are present in canine EOMs. We analyzed dog EOMs by confocal laser scanning microscopy, 3D reconstruction, and transmission electron microscopy. In EOM wholemount preparations stained with antibodies against neurofilament and synaptophysin we found typical palisade endings. Nerve fibers coming from the muscle extended into the tendon. There, the nerve fibers turned 180° and returned to branch into preterminal axons which established nerve terminals around a single muscle fiber tip. Fine structural analyses revealed that each palisade ending in dog EOMs established nerve terminals on the tendon. In some palisade endings we found nerve terminals contacting the muscle fiber as well. Such neuromuscular contacts had a basal lamina in the synaptic cleft thereby resembling motor terminals. By using antibodies against choline acetyltransferase (ChAT) we proved that canine palisade endings are ChAT-immunoreactive. This study shows that palisade endings are present in canine EOMs. In line with prior findings in cat and monkey, palisade endings in dog have a cholinergic phenotype. Keywordsproprioception; dog; extraocular muscle; palisade endings; choline acetyltransferaseThe sense of body position (proprioception) is recognized by specialized receptors in skeletal muscles. These proprioceptors, like Golgi tendon organs (GTOs) or muscle spindles, measure either muscle contraction or muscle stretch and contribute with this information to the cognition of posture. Extraocular muscles (EOMs) take an exceptional position as classical proprioceptors show a broad interspecies variation in their occurrence [21]. Specifically, muscle spindles can only be found in EOMs of mice [20], even-toed ungulates (goat, sheep, pig, camel, cow) [3,16,24], and man [7,19,22] nerve terminals establish contacts on the tendon. Additionally, in some palisade endings of these species nerve terminals contact muscle fibers as well. Rabbits [6] and rats [11] are an exception because in palisade endings of these species exclusively neuromuscular contacts were observed [6,11].At the moment the function of palisade endings is a matter of debate whether these structures are sensory [1,2,8,11,24,29,30], motor [3,15,16,26] The clinic for ophthalmology of the Veterinary University Vienna provided us with the orbits of a 7 years old male/castrated Magyar Vizsla dog. The animal was euthanized because it suffered from a severe glaucoma in both eyes. The orbits were dissected and all rectus EOMs from both sides including the distal tendon were removed. The muscles were immersion-fixed in 4 % paraformaldehyde in 0.1 M phosphate buffered saline (PBS) pH 7.4 for 4 hours and then rinsed in 4°C in 0.1 M PBS pH 7.4. EO...

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“…Many mammalian species do not have muscle spindles in their eye muscles: most monkey species including Macacca fascicularis, dogs, cats, rats, guinea pigs and rabbits do not have muscle spindles, whereas they have been found in humans, some types of monkey, mice and all ungulates (artiodactyls) [15][16][17][18]. The later studies show that the spindles are associated with the orbital layer, or the transition zone of the orbital layer with the global layer; but they are not associated with the global layer ( fig.…”

Section: Muscle Spindlesmentioning

confidence: 99%

Anatomy of the Oculomotor System

Büttner‐Ennever¹

2007

Developments in Ophthalmology

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The sensory and motor control of eye muscles are considered in this chapter. Eye muscles differ from skeletal muscles in several ways. One is the absence of muscle spindles and Golgi tendon organs in the eye muscles of some species, and their poor development in others. Second, eye muscles have an inner 'global layer', and the outer 'orbital layer', each containing different types of muscle fiber. Third, eye muscles contain not only twitch muscle fibers with a single endplate zone (SIFs), but also nontwitch muscle fibers with multiple endplate zones (MIFs), which are otherwise absent from mammalian muscles. There are cuffs of nerve terminals, called palisade endings, around the myotendinous junctions of global layer MIFs. Palisade endings are unique to eye muscles, and have been found in all mammalian species investigated up to now. The function of palisade endings is uncertain, but it is possible that they are 'sensory receptors'. Motoneurons innervating the eye muscles lie in the oculomotor, trochlear and abducens motor nuclei, and are contacted by several relatively independent premotor networks, which generate different types of eye movements such as saccades, vestibulo-ocular reflexes, optokinetic responses, smooth pursuit convergence or gaze-holding. In each motor nucleus, the motoneurons can be divided into two distinct sets: the first set innervating SIF muscle fibers and receiving inputs from all oculomotor premotor networks, and the second set innervating the MIFs and receiving premotor afferents from the gaze holding, convergence or smooth pursuit premotor networks, but not from the saccadic and vestibulo-oculomotor networks. We suggest that the SIF motoneurons and muscles are more suited to driving eye movements, and the MIF motoneurons and muscles to setting the tonic tension in eye muscles. Furthermore the 'palisade ending-MIF unit' may be part of a sensory feedback system in eye muscles, which should be considered in association with the causes and treatment of strabismus.

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The pattern of innervation of the extrinsic ocular muscles and the intra‐orbital ganglia of the albino mouse

Cited by 21 publications

References 15 publications

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Palisade endings are present in canine extraocular muscles and have a cholinergic phenotype

Anatomy of the Oculomotor System

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