Somatotopic organization of second order neurons of the eye muscle proprioception

Unit activity was recorded extracellularly from lamb's nucleus principalis and pars oralis of trigeminal nuclear complex following moderate manual stretching of individual extraocular muscles. The oral portion of the spinal trigeminal nucleus and the main sensory nucleus have been investigated by systematic exploration of the second-order neurons of the eye muscle proprioception. Such responses were somatotopically organized. In particular, each single extraocular muscle was represented along the main dorso-ventral axis in this manner: superior oblique and superior rectus in a dorsal layer; inferior rectus and inferior oblique in an intermediate layer, while the medial rectus and the lateral rectus were represented more ventrally. In a few experiments this representation was not observed, due to intermingling of the units. The topographic organization of eye muscle proprioception in the trigeminal nuclear complex described above closely corresponds to that reported by previous authors in the Gasser ganglion.     

Ascending and descending projections to the inferior colliculus in the rat

The ascending and descending projections to the central nucleus of the inferior colliculus (IC) were studied with the aid of retrograde transport of horseradish peroxidase (HRP). HRP-labelled cells were found in contralateral cochlear nuclei, where the majority of different cell types was stained. Few labelled cells were observed in the ipsilateral cochlear nuclei. HRP-positive neurones were found in all nuclei of the superior olivary complex on the ipsilateral side with the exception of the medial nucleus of the trapezoid body, which was never labelled either ipsilaterally or contralaterally. The largest concentration of HRP-labelled cells was usually observed in the ipsilateral superior olivary nucleus. Smaller numbers of labelled cells were present in contralateral nuclei of the superior olivary complex. Massive projections to the inferior colliculus were found from the contralateral and ipsilateral dorsal nucleus of the lateral lemniscus and ipsilateral ventral nucleus of the lateral lemniscus. Many neurones of the central and external nuclei of the contralateral inferior colliculus were labelled with HRP. Topographic organisation of the pathways ascending to the colliculus was expressed in the cochlear nuclei, lateral superior olivary nucleus and in the dorsal nucleus of the lateral lemniscus. HRP--positive cells were found in layer V of the ipsilateral auditory cortex, however, the evidence for topographic organisation was lacking.     

Somatotopic localization of the eye muscle afferents in the semilunar ganglion.

In the medial dorsolateral portion of the semilunar ganglion of curarized and anaesthetized lambs a cellular pool has been identified which contains the perikarya of the first-order neurons of the eye muscle proprioception. Responses to moderate manual stretch of individual eye muscles were recorded by means of tungsten microelectrodes, from single units of the ganglion. They were of the type induced by muscle spindle excitation. Such responses showed a somatotopic localization. The superior rectus and the superior oblique muscles were represented in the most dorsal layers of the ganglion, while the inferior rectus and the inferior oblique muscles projected on the most ventral portion of the pool. The medial and the lateral recti were represented in the medial and lateral parts and occasionally wedged themselves between the cells innervating the superior and the inferior muscles. Thus a somatotopic arrangement of the eye muscle proprioception has been demonstrated for the first time in the semilunar ganglion.     

The eye muscles and their innervation inChaetodon trifasciatus (Pisces,Teleostei, Chaetodontidae)

Synopsis InChaetodon trifasciatus, the large eye has the form of a thick disk rather than that of a globe. A deep cutaneous groove surrounds the eyeball, probably allowing rapid eye movements. The form and innervation of the three pairs of extraocular muscles are described. Each muscle is made of two types of fascicles of fibres, thick and thin. There is neither an anterior nor posterior myodome. The skull attachment of the obliques and of the inferior rectus is made on the thin sagittal ethmoidal membranous septum while that of the other recti occurs on osseous pieces of the skull. The attachment on the eyeball is made on the cartilaginous sclera. The ratio of the lengths of the antagonist muscles, superior vs. inferior oblique, superior vs. inferior rectus and medial vs. lateral rectus, is about 1.43:1. The three oculomotor nerves (III: common oculomotor, IV: trochlear and VI: abducens) as well as the ciliary system are described. For the following reasons, an analogy between the lateral rectus ofChaetodon trifasciatus and the lateral rectus + retractor bulbi of other vertebrates is indicated: (1) the nucleus of nerve III (which innervates four muscles) has four sectors, while that of IV (which innervates only the superior oblique) is made of one sector; (2) nerve VI consists of two roots corresponding to two groups of nerve cells of its motor nucleus and (3) in other vertebrates, nerve VI innervates both the lateral rectus and the retractor bulbi.     

Branching patterns of rabbit oculomotor and trochlear nerves demonstrated by Sihler's stain technique

A modified Sihler's stain technique was used to visualize the branching patterns of oculomotor and trochlear nerves. The levator palpebrae, superior rectus, inferior rectus, medial rectus, inferior oblique, superior oblique and tensor trochlea muscles were isolated from the eyes of normal rabbits and processed using modified Sihler's technique. The distributions and terminal ramifications of the oculomotor and trochlear nerves were observed. Two distinct divisions and terminal branches of the oculomotor nerve were shown in detail together with the trochlear nerve distribution. The application of Sihler's technique enables researchers to trace nerve branching within relatively transparent muscles, whereas the nerve fibers are counterstained and clearly visible. This technique could be useful for detailed studies of the motor control of extraocular muscles.     

The properties of the extraocular muscles of the frog. I. Mechanical properties of the isolated superior oblique and superior rectus muscles.

The mechanical properties of two extraocular muscles (superior oblique and superior rectus muscles) of the frog were studied and compared with those of a frog's skeletal muscle (iliofibularis muscle) which contains the same types of muscle fibres as the oculorotatory muscles. The extraocular muscles are very fast twitching muscles. They exhibit a smaller contraction time, a smaller half-relaxation time, a higher fusion frequency, and a lower twitch-tetanus ratio than the skeletal muscles. The maximum isometric tetanic tension produced per unit cross-sectional area is lower in the extraocular muscles than in skeletal muscles. However, the extraocular muscles show a higher fatigue resistance than the skeletal muscles. With respect to the dynamic properties there are some differences between the various oculorotatory muscles of the frog. The superior rectus muscle exhibits a faster time-course of the contraction, a higher fusion frequency, and a higher fatigability than the superior oblique muscle. An increase of the extracellular K+-concentration evokes sustained contractures not only in the extraocular muscles but also in the iliofibularis muscle; between these muscles there are no striking differences in the mechanical threshold of the whole muscle preparation. The mechanical threshold depends on the Ca++-concentration of the bathing solution and it is found in a range between 12.5 and 17.5 mM K+ in a normal Ringer solution containing 1.8 mM Ca++. The static-mechanical properties of the extraocular muscles of the frog and the dependence of the active developed tension on the muscle extension are very similar to those which are known to exist in the extraocular muscles of other vertebrates. In tetanic activated frog's oculorotatory muscles a linear relationship exists between length and tension. A variation of the stimulation frequency does not change the slope of this curve but causes parallel shifts of the curve. The peculiar properties of the extraocular muscles of the frog are discussed with respect to the muscle fibre types in these muscles and to the diameter of the muscle fibres.     

The properties of the extraocular muscles of the frog. II. Pharmacological properties of the isolated superior oblique and superior rectus muscles.

The pharmacological properties of the superior oblique and the superior rectus muscles of the frog's eye were investigated in comparison with those of a skeletal muscle (iliofibularis muscle) of the same animal. Acetylcholine causes sustained contractures of the extraocular muscles; this effect is increased by physostigmine and decreased or abolished by d-tubocurarine. Also the applications of succinylcholine, choline or caffeine are able to evoke contractures. There are no striking differences in pharmacological properties between extraocular and skeletal muscles of the frog. The time-course of the contractures and the sensitivity of the muscle preparations to the drugs which evoke contractures are identical in extraocular and iliofibularis muscles. In comparison with skeletal muscles there is no higher sensitivity of the extraocular muscles against curare-like drugs. The existence of adrenergic receptors could not be found neither in extraocular nor in skeletal muscles of the frog. It is concluded that in frogs no pharmacological differences exist between the muscle fibre types which compose the extraocular and the skeletal muscles.     

Morphology of the mammalian vestibulo-ocular reflex: the spatial arrangement of the human fetal semicircular canals and extraocular muscles

The vestibulo-ocular reflex is the system of compensatory ocular movements in response to stimulation of the kinetic labyrinth seen in all vertebrates. It allows maintenance of a stable gaze even when the head is moving. Perhaps the simplest influence on the VOR is the spatial orientation of the planes of the semicircular canals relative to the extraocular muscles. It is hypothesized that the extraocular muscles are in parallel alignment with their corresponding semicircular canals in order to reduce the amount of neural processing needed and hence keep reflex times to a minimum. However, despite its obvious importance, little is known of this spatial arrangement. Moreover, nothing is known about any ontogenetic changes in the relative orientations of the extraocular muscles and semicircular canals. The morphologies of fetal and adult specimens of Homo sapiens were examined using magnetic resonance (MR) images. Three-dimensional co-ordinate data were taken from the images and used to calculate vector equations of the extraocular muscles and planes of best fit for the semicircular canals. The relative orientations of the muscles and canals were then calculated from the vectors and planes. It was shown that there are significant correlations between both the anterior and lateral semicircular canals and their corresponding extraocular muscles during ontogeny. In the case of the lateral canal with the medial rectus, the lateral canal with the lateral rectus, and the anterior canal with the inferior oblique, the trend is towards, though never reaching, alignment, whereas the anterior canal and the superior rectus muscle move out of alignment as age increases. Furthermore, it was noted that none of the six muscle-canal pairs is in perfect alignment, either during ontogeny or in adulthood. It was also shown that the three semicircular canals are not precisely orthogonal, but that the anterior and posterior canals form an angle of about 85 degrees , while the anterior and lateral canals diverge by approximately 100 degrees . Overall, it was shown that there is significant reorientation of the extraocular muscles and semicircular canals during ontogeny, but that, in most cases, there is little realignment beyond the fetal period.     

Cranial endothermy and a putative brain heater in the most basal tuna species, Allothunnus fallai

Field studies on the slender tuna Allothunnus fallai revealed cranial temperatures that were 4·8 ± 0·4° C (mean ± s . d .) above the ambient sea surface temperature. Dissections aimed at documenting the cranial heat source revealed a fused extraocular muscle complex positioned beneath the brain of this basal tuna species. The muscle complex is structurally distinct from that documented for any other fish species. In A. fallai , all four extraocular rectus muscle pairs (superior, inferior, medial and lateral rectus) are incorporated into one distinct tissue complex which is positioned between the orbits and in direct contact with the braincase. A combination of morphological, physiological and biochemical techniques were used to characterize the modified muscle tissue, and high-resolution magnetic resonance imaging was used to illustrate its association with the brain and optic nerves. The modified eye muscles lack organized contractile proteins and are perfused by an extensive vascular counter-current system that originates from the internal carotid artery. Vessel diameters, artery–vein configuration, and anatomic position between the systemic circulation and the warm eye muscles all suggest that this system is a heat exchanger. Collectively, these findings suggest that A. fallai has evolved extraocular muscles that may function to warm the brain and eye region. This is the first record of a cranial modification comprised of all four rectus muscles and the only documented occurrence of this mechanism for cranial endothermy among the tunas.     

The neurons of origin of non-cortical afferent connections to the oculomotor nucleus. A retrograde labeling study in the rabbit.

The cellular origin of the brainstem projections to the oculomotor nucleus in the rabbit has been investigated by using free (HRP) and lectin-conjugated horseradish peroxidase (WGA-HRP). Following injections of these tracers into the somatic oculomotor nucleus (OMC), retrogradely labeled cells have been observed in numerous brainstem structures. In particular, bilateral labeling has been found in the four main subdivisions of the vestibular complex, predominantly in the superior and medial vestibular nuclei and the interstitial nucleus of Cajal, while ipsilateral labeling was found in the rostral interstitial nucleus of the medial longitudinal fascicle (Ri-MLF), the Darkschewitsch and the praepositus nuclei. Neurons labeled only contralaterally have been identified in the following structures: mesencephalic reticular formation dorsolateral to the red nucleus, abducens internuclear neurons, group Y, several areas of the lateral and medial regions of the pontine and medullary reticular formation, ventral region of the lateral cerebellar nucleus and caudal anterior interpositus nucleus. This study provides also information regarding differential projections of some centers to rostral and caudal portions of the OMC. Thus, the rostral one-third appears to receive predominant afferents from the superior and medial vestibular nuclei, while the caudal two-thirds receive afferents from all the four vestibular nuclei. Finally, the group Y sends afferents to the middle and caudal, but not to the rostral OMC.     

Afferent signals from pigeon extraocular muscles modify the vestibular responses of units in the abducens nucleus.

Although the extraocular muscles contain stretch receptors it is generally believed that their afferents exert no influence on the control of eye movement. However, we have shown previously that these afferent signals reach various brainstem centres concerned with eye movement, notably the vestibular nuclei, and that the decerebrate pigeon is a favourable preparation in which to study their effects. If the extraocular muscle afferents do influence oculomotor control from moment-to-moment they should exert a demonstrable effect on the oculomotor nuclei. We now present evidence that extraocular muscle afferent signals do, indeed, alter the responses of units in an oculomotor nucleus (the abducens, VI nerve nucleus, which supplies the lateral rectus muscle) to horizontal, vestibular stimulation induced by sinusoidal oscillation of the bird. Such stimuli evoke a vestibulo-ocular reflex in the intact bird. The extraocular stretch receptors were activated by passive eye movement within the pigeon's saccadic range; such movements modified the vestibular responses of all 19 units studied which were all, histologically, in the abducens nucleus. The magnitude of the effects, purely inhibitory in 15 units, depended both on the amplitude and the velocity of the eye movement and most units showed selectivity for particular combinations of plane (e.g. horizontal versus vertical) and direction (e.g. rostral versus caudal) of eye movement. The results show that an afferent signal from the extraocular muscles influences vestibularly driven activity in the abducens nucleus to which it carries information related to amplitude, velocity, plane and direction of eye movement in the saccadic range. They thus strongly support the view that extraocular afferent signals are involved in the control of eye movement.     

Morphological characteristics of lateral rectus motoneurones shown by intracellular injection of HRP.

The morphology of identified lateral rectus motoneurones is described after staining by intracellular iontophoresis of horseradish peroxidase. Soma vary in shape and size according to the number and orientation of primary dendrites. The basic pattern of arborisation shows short primary dendrites which branch close to the soma, forming a distal ramification extending over 600 to 1,200 micrometer from the soma. Distal dendrites extend into the ipsilateral medial vestibular nucleus, the reticular formation and amongst the fibres of the medial longitudinal fasciculus. This extension is greater than that previously seen in procion yellow and Golgi stained lateral rectus motoneurones. The axon originates from the perikarya or from the base of a primary dendrite. No axon collaterals have been observed.     

The dorsomedial nuclear group of cranial nerves in the frog.

The dorsomedial motor nuclei were demonstrated by the cobalt-labeling technique applied to the so-called somatic motor cranial nerves. The motoneurons constituting these nuclei are oval-shaped and smaller than the motoneurons in the ventrolateral motor nuclei. They give rise to ventral and dorsal dendrite groups which have extensive arborization areas. A dorsolateral cell group in the rostral three quarters of the oculomotorius nucleus innervates ipsilateral eye muscles (m.obl.inf., m.rect.inf., m.rect.med.) and a ventromedial cell group innervates the contralateral m. rectus superior. Ipsilateral axons originate from ventral dendrites, contralateral axons emerge from the medial aspect of cell bodies, or from dorsal dendrites, and form a "knee" as they turn around the nucleus on their way to join the ipsilateral axons. A few labeled small cells found dorsal and lateral to the main nucleus in the central gray matter are regarded as representing the nucleus of Edinger-Westphal. The trochlearis nucleus is continuous with the ventromedial cell group of the oculomotorius nucleus. The axons originate in dorsal dendrites, run dorsally along the border of the gray matter and pierce the velum medullare on the contralateral side. A compact dendritic bundle of oculomotorius neurons traverse the nucleus, and side branches appear to be in close apposition to the trochlearis neurons. A dorsomedial and a ventrolateral cell group becomes labeled via the abducens nerve. The former supplies the m. rectus lateralis, while the latter corresponds to the accessorius abducens nucleus which innervates the mm. rectractores. Neurons in this latter nucleus are large and multipolar, resembling the neurons in the ventrolateral motor nuclei. Their axons originate from dorsal dendrites and form a "knee" around the dorsomedial aspect of the abducens nucleus. Cobalt applied to the hypoglossus nerve reaches a dorsomedial cell group (the nucleus proper), spinal motoneurons and sympathetic preganglionic neurons. Of the dorsomedial motor cells, the hypoglossus neurons are the largest, and a branch of their ventral dendrites terminates on the contralateral side. Some functional and developmental biological aspects of the morphological findings, such as the crossing axons and the peculiar morphology of the accessory abducens nucleus, are discussed.     

Localization and morphometric analysis of masticatory muscle afferent neurons in the nucleus of the mesencephalic root of the trigeminal nerve in the cat

Injections of horseradish peroxidase (HRP) were made into the ipsilateral temporal muscle and contralateral masseter muscle of 10 cats in order to identify and characterize neurons in the nucleus of the mesencephalic root of the trigeminal nerve that innervate muscle receptors in the orofacial periphery. Neurons labelled by HRP injections and unlabelled cells from 5 control cats were measured with a computer-based image analyzer, and their position was mapped on a stereotaxic graph. Cells that innervate the masseter and temporal muscles were identified throughout the rostrocaudal extent of the nucleus. There was no indication of a somatotopic pattern nor of a specific segregation within the nucleus for cells innervating muscle receptors. The nucleus contained small, rounded unipolar neurons located primarily in the dorsal border of the periaqueductal gray (PAG) matter in the rostral part of the nucleus and larger oval unipolar neurons which were scattered throughout the nucleus, but were predominant in the pontine portion of the nucleus. HRP injections labelled both large and small cells, as well as occasional multipolar cells. The last-mentioned tended to be located in the lateral margins of the PAG. The mean geometric values obtained for the control group were: area 552.7 microns2 perimeter 110.3 microns; maximum diameter 36.0 microns. and diameter of an equivalent circle 26.1 microns. The mean values of the labelled neurons were: area 606.6 microns2; perimeter 100.1 microns; maximum diameter 36.0 microns, and diameter of an equivalent circle 27.2 microns.     

Regulation pathways of expectancy behavior in the cat: histologic study

In the behaving cat, motion expectancy of an event to occur (for a prey to appear) is accompanied by the development of 14 Hz electrocortical mu rhythms in the hand subarea of cortical somatic area SI. Our first aim here was to identify subcortical sites projecting to this cortical mu focus, using localised retrograde HRP marking. The only site thus labelled was the thalamic zone well known to project to the cortical mu area, and to act as a generator for the mu rhythms (ventral posterior nucleus, VP); no other deep structure could be identified, that could have been considered as a putative zone for control of cortical mu. We then injected minute amounts of HRP into the thalamic mu zone; labelled neurones were located (apart from those expected in the relays of the somatic pathway) in locus coeruleus (bilaterally) and ipsilaterally in the thalamic nuclei anteroventralis and laterodorsalis. In brief then, it seems that the regulation of the VP-SI mu channel (that we could previously demonstrate), by other deep structures is exerted upon the thalamic side.     

Injection of methylprednisolone directly into the extraocular muscles of eyes with disturbed motility secondary to Graves' ophthalmopathy. Preliminary report

Aim of the study was to estimate the efficacy of 6-alpha-methylprednisolone injection into involved extraocular muscles in eyes with motility disturbances caused by endocrine ophthalmopathy. MATERIAL AND METHODS: For further evaluation we qualified 4 patients, 1 female and 3 males, aged: 60, 43, 42 and 64 years, with clinical activity score equal 4, with duration of Graves' ophthalmopathy of mean 2.1 years (0.16 - 5.5). Included were patients with movement restrictions in vertical plane and echographic findings of isolated extraocular muscle involvement (inferior rectus). Each of the patients received 20 mg 6-alpha-methylprednisolone into the muscle belly of inferior rectus, in one case injection was done in both eyes. RESULTS: In all cases we were able to archive lessening of the intraocular pressure in secondary position, with slight improvement in ocular motility and bigger range of duction free of diplopia. CONCLUSIONS: Visual function improvement found by the patients is the best evidence for application of 6-alpha-methylprednisolone into the extraocular muscles of patients with motility disturbances secondary to endocrine ophthalmopathy.     

Number and arrangement of extraocular muscles in primitive gnathostomes: evidence from extinct placoderm fishes

Exceptional braincase preservation in some Devonian placoderm fishes permits interpretation of muscles and cranial nerves controlling eye movement. Placoderms are the only jawed vertebrates with anterior/posterior obliques as in the jawless lamprey, but with the same function as the superior/inferior obliques of other gnathostomes. Evidence of up to seven extraocular muscles suggests that this may be the primitive number for jawed vertebrates. Two muscles innervated by cranial nerve 6 suggest homologies with lampreys and tetrapods. If the extra muscle acquired by gnathostomes was the internal rectus, Devonian fossils show that it had a similar insertion above and behind the eyestalk in both placoderms and basal osteichthyans.     

A horseradish peroxidase study on the mammillothalamic tract in the rat

The mammillary projections to the anterior thalamic nuclei were investigated in the rat, using the horseradish peroxidase (HRP) method. Pars centralis of the medial mammillary nucleus projects to the medial portion of the ateromedial nucleus (AM). Pars medialis (Mm) of the medial mammillary nucleus sends fibers to the ipsilateral AM and sparsely to the medial portion of the contralateral side. The ventral and dorsal portions of Mm project to the anterior and posterior portions of AM, respectively. The pars latralis (Ml) and pars posterior (Mp) of the medial mammillary nucleus send fibers predominantly to the ipsilateral anteroventral nucleus and sparsely to the contralateral side. A slight difference between Ml and Mp projections was observed. The lateral mammillary nucleus projects bilaterally to the anterodorsal nucleus.     

Peripheral pathway of proprioceptive fibres from feline extra-ocular muscles. I. A histological study.

The findings of the previous study (1976) involving orbital operations in 12 cats have been confirmed in this study involving intracranial operations in 20 more cats. The perikarya of origin of afferent fibres from feline extra-ocular msucles have been clearly localised to the trigeminal mesencephalic nucleus. The functional subdivision in the nucleus that was noted earlier has been reaffirmed. Thus the caudal or pontine part was the location of cell bodies from the lateral rectus muscle, the intermediate part contained those from the superior oblique, while the other muscles were represented by cell bodies in the rostral part, there being some degree of overlap in the last two zones. In every instance the representation was shown to be bilateral and the total ratio of cellular representation was in the region of 4:1 (ipsilateral-contralateral). The peripheral pathway of the proprioceptive fibres has been shown to be exclusively along the oculomotor, trochlear and abducent nerves which are therefore sensorimotor.