Central oculomotor circuits

Recent data and hypotheses concerning the central oculomotor pathways are reviewed. Lateral and vertical eye movements are discussed successively, beginning in each case with the final common pathway and then progressing step by step along the main supranuclear tracts selectively involved in the 3 types of eye movements: vestibular movements, saccades and smooth pursuit. It is now established that the final common pathway of lateral eye movements in frontal-eyed species is the abducens nucleus, which controls not only the ipsilateral lateral rectus, but also, through the internuclear neurons, almost all the conjugate lateral activity of the opposite medial rectus. The ascending tract of Deiters, providing direct excitatory vestibular signals to the medial rectus motoneurons, could either have totally regressed in man or would play only a minor functional role. Likewise, a direct inhibition of the medial rectus motoneurons now seems unlikely or ineffective, the relaxation of this muscle resulting essentially from the disfacilitation mediated by the abducens internuclear neurons. This particular mechanism could be explained by the fact that the medial rectus motoneurons also receive messages of convergence, a slow disjunctive movement independent of lateral eye movements. Convergence is performed by excitatory reticular neurons near the oculomotor nucleus and by inhibitory pathways projecting onto the abducens motoneurons, perhaps passing through the internuclear neurons of the oculomotor nucleus. The premotor relay of horizontal reflex eye movements is the medial vestibular nucleus (M.V.N.) which contains excitatory and inhibitory neurons projecting onto the contralateral and ipsilateral abducens nuclei respectively. Afferences of the M.V.N. arise from: the labyrinth, through the vestibular nerve (vestibulo-ocular reflex); the neck, through the dorsal part of the medullary tegmentum (cervico-ocular reflex); the peripheral retina and the visual pathways (for the vestibular contribution of optokinetic nystagmus), perhaps via the pretectum, the nucleus reticularis tegmenti pontis (N.R.T.P.) and/or the nucleus prepositus hypoglossi (N.P.H.) (visuo-ocular reflex). The premotor relay for all ipsilateral saccades is the paramedian pontine reticular formation (P.R.F.) which excites the ipsilateral abducens nucleus and inhibits the contralateral abducens nucleus, via the burst inhibitory neurons located ventrally to the ipsilateral abducens nucleus.(ABSTRACT TRUNCATED AT 400 WORDS)     

Extra- and intracellular HRP analysis of the organization of extraocular motoneurons and internuclear neurons in the guinea pig and rabbit

The distribution of extraocular motoneurons and abducens and oculomotor internuclear neurons was determined in guinea pigs by injecting horseradish peroxidase (HRP) into individual extraocular muscles, the abducens nucleus, the oculomotor nucleus, and the cerebellum. Motoneurons in the oculomotor nucleus innervated the ipsilateral inferior rectus, inferior oblique, medial rectus, and the contralateral superior rectus and levator palpebrae muscles. Most motoneurons of the trochlear nucleus projected to the contralateral superior oblique muscle although a small number innervated the ipsilateral superior oblique. The abducens and accessory abducens nuclei innervated the ipsilateral rectus and retractor bulbi muscles, respectively. The somata of abducens internuclear neurons formed a cap around the lateral and ventral aspects of the abducens nucleus. The axons of these internuclear neurons terminated in the medial rectus subdivision of the contralateral oculomotor nucleus. At least two classes of guinea pig oculomotor internuclear interneurons exist. One group, located primarily ventral to the oculomotor nucleus, innervated the abducens nucleus and surrounding regions. The second group, lying mainly in the dorsal midline area of the oculomotor nucleus, projected to the cerebellum. Intracellular staining with HRP demonstrated similar soma-dendritic organization for oculomotor and trochlear motoneurons of both guinea pigs and rabbits. Dendrites of oculomotor motoneurons radiated symmetrically from the soma to cover approximately one-third of the entire nucleus, and each motoneuron sent at least one dendrite into the central gray overlying the oculomotor nucleus. In both species, a small percentage of oculomotor motoneurons possessed axon collaterals that terminated both within and outside of the nucleus. The dendrites of trochlear motoneurons extended into the medial longitudinal fasciculus and the reticular formation lateral to the nucleus. Our data on the topography of motoneurons and internuclear neurons in the guinea pig and soma-dendritic organization of motoneurons in the guinea pig and rabbit show that these species share common organizational and morphological features. In addition, comparison of these data with those from other mammals reveals that dendritic complexity (number of dendrites per motoneuron) of extraocular motoneurons exhibits a systematic increase with animal size.     

Organization of the six motor nuclei innervating the ocular muscles in lamprey

The topography of motoneurons supplying each of the six ocular muscles of the lamprey, Lampetra fluviatilis, was studied by selective application of HRP to the cut nerves of identified muscles. In addition, the distributions of motoneuron populations to both eyes were studied simultaneously with fluorescein and rhodamine coupled dextran-amines (FDA and RDA) applied to cut ocular muscle nerves of either side. The motoneuron pool of the caudal oblique muscle is represented bilaterally in the trochlear (N IV) motor nucleus. The dorsal rectus muscle is innervated from a contralateral group of oculomotor (N III) motoneurons and the remaining four muscles exclusively from the ipsilateral side (N III and N VI). The inferior and posterior rectus muscles are both innervated by the abducens nerve. In contrast to all jawed vertebrates, only three eye muscles (the dorsal rectus, rostral rectus, and rostral oblique) are innervated by the oculomotor nerve in lampreys (N III). Lampreys have a motor nucleus similar to the accessory abducens nucleus previously described only in tetrapods. They lack the muscle homologous to the nasal rectus muscle of elasmobranchs and the medial rectus muscle of osteognathostomes. The distribution of the dendrites of different groups of motoneurons was studied and is considered in relation to inputs from tectum and the different cranial nerves.     

Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey

The anatomical characteristics of vestibular neurons, which are involved in controlling the horizontal vestibulo-ocular reflex, were studied by injecting horseradish peroxidase (HRP) into neurons whose response during spontaneous eye movements had been characterized in alert squirrel monkeys. Most of the vestibular neurons injected with HRP that had axons projecting to the abducens nucleus or the medial rectus subdivision of the oculomotor nucleus had discharge rates related to eye position and eye velocity. Three morphological types of cells were injected whose firing rates were related to horizontal eye movements. Two of the cell types were located in the ventral lateral vestibular nucleus and the ventral part of the medial vestibular nucleus (MV). These vestibular neurons could be activated at monosynaptic latencies following electrical stimulation of the vestibular nerve; increased their firing rate when the eye moved in the direction contralateral to the soma; had tonic firing rates that increased when the eye was held in contralateral positions; and had a pause in their firing rate during saccadic eye movements in the ipsilateral or vertical directions. Eleven of the above cells had axons that arborized exclusively on the contralateral side of the brainstem, terminating in the contralateral abducens nucleus, the dorsal paramedian pontine reticular formation, the prepositus nucleus, medial vestibular nucleus, dorsal medullary reticular formation, caudal interstitial nucleus of the medial longitudinal fasciculus, and raphé obscurus. Eight of the cells had axons that projected rostrally in the ascending tract of Deiters and arborized exclusively on the ipsilateral side of the brainstem, terminating in the ipsilateral medial rectus subdivision of the oculomotor nucleus and, in some cases, the dorsal paramedian pontine reticular formation or the caudal interstitial nucleus of the medial longitudinal fasciculus. Two MV neurons were injected that had discharge rates related to ipsilateral eye position, generated bursts of spikes during saccades in the ipsilateral direction, and paused during saccades in the contralateral direction. The axons of those cells arborized ipsilaterally, and terminated in the ipsilateral abducens nucleus, MV, prepositus nucleus, and the dorsal medullary reticular formation. The morphology of vestibular neurons that projected to the abducens nucleus whose discharge rate was not related to eye movements, or was related primarily to vertical eye movements, is also briefly presented.     

The organization of the extraocular motor nuclei in the atlantic stingray,Dasyatis sabina

Retrograde transport of HRP was used to determine the location and organization of the motor nuclei innervating the extrinsic eye muscles of the stingray, an elasmobranch fish. Oculomotor neurons are located both medial to and immediately ventrolateral to the MLF in the rostral midbrain. A ventral oculomotor nucleus was found among the IIIrd nerve rootlets close to the base of the midbrain. The dendrites of cells in the dorsal nucleus appear to be preferentially oriented in the transverse plane penetrating the MLF. Motoneuron pools innervating individual muscles are incompletely segregated in the dorsal group. However, the ventral nucleus innervates only the inferior oblique muscle. Dorsally, motoneurons innervating a single muscle are found on both sides of the MLF. In the caudal midbrain, the majority of trochlear motoneurons are located immediately ventrolateral to the MLF. Abducens motoneurons are scattered in the medulla from a ventrolateral position resembling the location of the nucleus in teleost fish to a dorsomedial position close to the MLF as in most other vertebrates. In contrast to other vertebrates, the medial rectus muscle is innervated by the contralateral oculomotor nucleus. Motoneurons innervating the other muscles have the same laterality as found in other vertebrates.     

Afferents to the abducens nucleus in the monkey and cat

The abducens nucleus is a central coordinating element in the generation of conjugate horizontal eye movements. As such, it should receive and combine information relevant to visual fixation, saccadic eye movements, and smooth eye movements evoked by vestibular and visual stimuli. To reveal possible sources of these signals, we retrogradely labeled the afferents to the abducens nucleus by electrophoretically injecting horseradish peroxidase into an abducens nucleus in four monkeys and two cats. The histologic material was processed by the tetramethyl benzidine (TMB) method of Mesulam. In both species the largest source of afferents to the abducens nucleus was bilateral projections from the ventrolateral vestibular nucleus and the rostral pole of the medial vestibular nucleus. Scattered neurons were also labeled in the middle and caudal levels of the medial vestibular nucleus. Large numbers of neurons were labeled in the ventral margin of the nucleus prepositus hypoglossi in the cat and in the common margin of the nucleus prepositus and the medial vestibular nucleus in the monkey, a region we call the marginal zone. Substantial numbers of retrogradely labeled neurons were found in the dorsomedial pontine reticular formation both caudal and rostral to the abducens nuclei. In the monkey, large numbers of labeled neurons were present in the contralateral medial rectus subdivision of the oculomotor complex, while smaller numbers occurred in the ipsilateral medial rectus subdivision and elsewhere in the oculomotor complex. In the cat, large numbers of retrogradely labeled cells were present in a small periaqueductal gray nucleus immediately dorsal to the caudal pole of the oculomotor complex, and a few labeled neurons were also dispersed through the caudal part of the oculomotor complex. Occasional labeled neurons were present in the contralateral superior colliculus in both species. The size and distribution of the labeled neurons within the intermediate gray differed dramatically in the two species. In the cat, the retrogradely labeled neurons were very large and occurred predominantly in the central region of the colliculus, while in the monkey, they were small to intermediate in size and were distributed more uniformly within the middle gray. Among the afferent populations present in the monkey, but not in the cat, was a group of scattered neurons in the ipsilateral rostral interstitial nucleus of the medial longitudinal fasciculus and a denser, bilateral population in the interstitial nucleus of Cajal.(ABSTRACT TRUNCATED AT 400 WORDS)     

Motoneurons of twitch and nontwitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys

Eye muscle fibers can be divided into two categories: nontwitch, multiply innervated muscle fibers (MIFs), and twitch, singly innervated muscle fibers (SIFs). We investigated the location of motoneurons supplying SIFs and MIFs in the six extraocular muscles of monkeys. Injections of retrograde tracers into eye muscles were placed either centrally, within the central SIF endplate zone; in an intermediate zone, outside the SIF endplate zone, targeting MIF endplates along the length of muscle fiber; or distally, into the myotendinous junction containing palisade endings. Central injections labeled large motoneurons within the abducens, trochlear or oculomotor nucleus, and smaller motoneurons lying mainly around the periphery of the motor nuclei. Intermediate injections labeled some large motoneurons within the motor nuclei but also labeled many peripheral motoneurons. Distal injections labeled small and medium-large peripheral neurons strongly and almost exclusively. The peripheral neurons labeled from the lateral rectus muscle surround the medial half of the abducens nucleus: from superior oblique, they form a cap over the dorsal trochlear nucleus; from inferior oblique and superior rectus, they are scattered bilaterally around the midline, between the oculomotor nucleus; from both medial and inferior rectus, they lie mainly in the C-group, on the dorsomedial border of oculomotor nucleus. In the medial rectus distal injections, a "C-group extension" extended up to the Edinger-Westphal nucleus and labeled dendrites within the supraoculomotor area. We conclude that large motoneurons within the motor nuclei innervate twitch fibers, whereas smaller motoneurons around the periphery innervate nontwitch, MIF fibers. The peripheral subgroups also contain medium-large neurons which may be associated with the palisade endings of global MIFs. The role of MIFs in eye movements is unclear, but the concept of a final common pathway must now be reconsidered.     

Internuclear neurons in the ocular motor system of frogs.

Medial and lateral rectus motoneurons of frogs were localized after retrograde labeling with horseradish peroxidase (HRP) injected in the medial rectus muscle or applied on the cut end of the abducens nerve. Coordinates of these cell columns were used as target areas for the injection of small amounts of HRP (20-60 nl) and [3H]leucine (25-40 nl) and as search areas for retrogradely and anterogradely labeled internuclear neurons (INT) in in vivo and in vitro experiments. HRP injection in the medial rectus subdivision of the oculomotor nucleus (n = 6) resulted in retrograde labeling of cell bodies in the contralateral principal abducens nucleus. On the average about 16 cells per animal were found. Somatic diameters were about 13.5 +/- 2.8 microns (n = 32). The number and the size of these abducens internuclear neurons (AbINT) are smaller than those of lateral rectus motoneurons (n = 75; diameter: 19 +/- 3.2 microns). A crossed projection of AbINT to medial rectus motoneurons in the contralateral oculomotor nucleus is further supported by autoradiographic results. Following injection of [3H]leucine into the abducens nucleus, a high density of silver grains was visible within the contralateral oculomotor nucleus, mainly in the caudal part of the oculomotor nucleus, where medial rectus motoneurons are located. Injection of [3H]leucine in vivo (n = 4) and in vitro (n = 3) resulted in a similar high density of silver grains within the contralateral oculomotor nucleus, but the background level of silver grains was significantly higher after in vitro (264 +/- 38/2,500 microns2) than after in vivo injections (195 +/- 17/2,500 microns2). HRP injection in the principal abducens nucleus (n = 9) resulted in retrograde labeling of cell bodies in the medial rectus subdivisions of the bilateral oculomotor nuclei. Ipsilateral projections predominated, with about 10 (+/- 8) labeled cells over contralateral projections (about 3 +/- 2). Average diameters of these oculomotor internuclear neurons (OcINT) were again smaller (10.8 +/- 2 microns; n = 18) than those of medial rectus motoneurons (14.4 +/- 3 microns; n = 52). In addition, retrogradely labeled cells were consistently encountered in the bilateral vestibular nuclei, the cerebellar nuclei, the dorsal brainstem caudal to the abducens nuclei, and ipsilaterally in the pretectum. Most of the vestibular neurons were located in the rostral part of the vestibular nuclear complex. These neurons might constitute part of the three-neuronal arc of the vestibulo-ocular reflex in the frog. Labeled cells in the pretectum were restricted to the ipsilateral posterior thalamic nucleus (P).(ABSTRACT TRUNCATED AT 400 WORDS)     

Identification of abducens motoneurons, accessory abducens motoneurons, and abducens internuclear neurons in the chick by retrograde transport of horseradish peroxidase

The location of the motoneurons innervating the lateral rectus, pyramidalis, and quadratus muscles of the chick has been determined by application of horseradish peroxidase (HRP) to these muscles and their nerve branches, and internuclear neurons in the abducens nucleus have been identified by injection of HRP into the oculomotor nucleus. Quantitative results were obtained by means of a semiautomatic image analyzer. Lateral rectus motoneurons were observed only in the ipsilateral principal abducens nucleus, where they numbered 500-550, and quadratus and pyramidalis motoneurons only in the ipsilateral accessory abducens nucleus. The 325-375 internuclear neurons that appeared in the principal abducens nucleus contralateral to the oculomotor nucleus injected with HRP were practically confined to the rostral two thirds of the nucleus, where they tended to surround the lateral rectus motoneurons in dorsal or lateral positions, though a minority of interneurons also mingled with the motoneurons in the center or at the medial face of the nucleus. Most interneurons were small and elongated, but a minority of larger interneurons morphologically similar to the lateral rectus motoneurons were also distinguishable. The 100-110 quadratus motoneurons and the 45-55 pyramidalis motoneurons mingled in the accessory abducens nucleus were larger than the lateral rectus motoneurons and sent their axons into the ipsilateral abducens nerve.     

Afferents to the oculomotor nucleus in the goldfish (Carassius auratus) as revealed by retrograde labeling with horseradish peroxidase.

The goal of this work was to compare the distribution and morphology of neurons projecting to the oculomotor nucleus in goldfish with those previously described in other vertebrate groups. Afferent neurons were revealed by retrograde labeling with horseradish peroxidase. The tracer was electrophoretically injected into the oculomotor nucleus. The location of the injection site was determined by the antidromic field potential elicited in the oculomotor nucleus by electrical stimulation of the oculomotor nerve. Labeled axons whose trajectories could be reconstructed were restricted to the medial longitudinal fasciculus. In order of quantitative importance, the afferent areas to the oculomotor nucleus were: (1) the ipsilateral anterior nucleus and the contralateral tangential and descending nuclei of the octaval column. Furthermore, a few labeled cells were found dorsomedially to the caudal pole of the unlabeled anterior octaval nucleus; (2) the contralateral abducens nucleus. The labeled internuclear neurons were arranged in two groups within and 500 microns behind the caudal subdivision of the abducens nucleus; (3) a few labeled cells were observed in the rhombencephalic reticular formation near the abducens nucleus, most of which were contralateral to the injection site. Specifically, stained cells were found in the caudal pole of the superior reticular nucleus, throughout the medial reticular nucleus and in the rostral area of the inferior reticular nucleus; (4) eurydendroid cells of the cerebellum, located close to the contralateral eminentia granularis pars lateralis, were also labeled; and (5) a small and primarily ipsilateral group of labeled cells was located at the mesencephalic nucleus of the medial longitudinal fasciculus. The similarity in the structures projecting to the oculomotor nucleus in goldfish to those in other vertebrates suggests that the neural network involved in the oculomotor system is quite conservative throughout phylogeny. Nevertheless, in goldfish these projections appeared with some specific peculiarities, such as the cerebellar and mesencephalic afferents to the oculomotor nucleus.     

Innervation of the medial rectus muscle in the ratfish,Hydrolagus colliei

Oculomotor organization in elasmobranch fish (sharks, skates, and rays) differs from that in other vertebrates in that the medial rectus muscle is innervated by contralateral rather than ipsilateral motoneurons. Distinguishing whether this innervation pattern is unique to the elasmobranchs, or is the ancestral pattern for cartilaginous fishes, requires examination of a representative of the sister group to the elasmobranchs, the holocephalans (ratfish). In the present study, the innervation pattern of the medial rectus was examined in a ratfish, Hydrolagus colliei, by using biotinylated dextran amines (BDA, 3,000 MW). Labeled cells were revealed in the contralateral oculomotor nucleus. Therefore, an innervation pattern in which the medial rectus muscle is innervated by contralateral motoneurons is the primitive condition for cartilaginous fishes. J. Comp. Neurol. 400:571–579, 1998. © 1998 Wiley-Liss, Inc.     

Oculomotor system of the weakly electric fish Gnathonemus petersii

The peripheral and central aspects of the extraocular system were studied in the weakly electric fish Gnathonemus petersii. All six extraocular muscles show a similar composition of large and small fibers grouped characteristically in the proximal and distal regions respectively. The exit of the three extraocular nerves from the brain is similar to that in other vertebrates. However, the intracephalic and intracranial course of the trochlear nerve is unusual, partly because of the extraordinary hypertrophy of the cerebellum. The three nerves course rostrally on the ventral brain surface; the trochlear nerve penetrates the orbital cavity separately from the two other nerves. The fiber-diameter spectrum of each extraocular nerve is bimodal; unmyelinated fibers were not observed in any of the nerves. The location of the extraocular motor nuclei was established by retrograde axonal transport of HRP or cobaltic-lysine complex. The oculomotor nucleus is situated ventral to the posterior pole of the magnocellular mesencephalic nucleus and the trochlear nucleus is found caudal and dorsal to this. The abducens nucleus is situated at the level of the octavolateral efferent nucleus and consists of a single group of cells on each side of the ventral tegmentum. The oculomotor nucleus of G. petersii shows a somatotopic organization. The superior rectus muscle receives a contralateral innervation whereas the inferior rectus and oblique muscles and the internal rectus muscles receive an ipsilateral innervation. The superior oblique muscle is innervated by contralateral trochlear motoneurons and the external rectus by ipsilateral abducens motoneurons. The majority of extraocular motoneurons have piriform perikarya and long beaded dendrites that extend laterally in the oculomotor and abducens nuclei and rostrally in the trochlear nucleus. The terminal dendritic portions of trochlear motoneurons widely overlap with oculomotor dendrites and perikarya. In all three nuclei the axon originates opposite to the main dendrite. Collaterals of the hairpin-bend abducens axons could be identified in a few cases. The oculomotor system of G. petersii appears basically similar to that of other teleosts; the differences observed concern mainly the structure of the abducens nucleus, the intracranial and intracephalic course of the trochlear nerve, and the relatively small number of axons in each nerve.     

Abducens internuclear and ascending tract of deiters inputs to medial rectus motoneurons in the cat oculomotor nucleus: synaptic organization

Abducens internuclear and ascending tract of Deiters (ATD) inputs to medial rectus motoneurons in the oculomotor nucleus are important for conjugate horizontal movements. In the present study, the organization of these separate populations of neurons and their synaptic connections with medial rectus motoneurons in the cat oculomotor nucleus have been examined by light and electron microscopy by using retrograde and anterograde axonal tracers. Consistent with the patterns of retrograde horseradish peroxidase labeling, the abducens internuclear projection is predominantly, if not exclusively, contralateral, whereas the ATD projection is exclusively ipsilateral, as demonstrated by anterograde autoradiographic and biocytin labeling. Both populations of synaptic endings contain spheroidal synaptic vesicles and establish synaptic contacts with modest postsynaptic densifications. In addition, ATD synaptic endings frequently are associated with subjunctional dense bodies and subsurface cisternae. The two populations of excitatory inputs differ, however, in their soma-dendritic distribution. The majority of abducens internuclear synaptic endings contact distal dendrites, whereas the majority of ATD synaptic endings contact proximal dendrites or somata. Abducens internuclear synaptic endings furthermore have a higher density of mitochondria than ATD synaptic endings. The more proximal location of ATD synaptic endings is consistent with the faster rise time and earlier reversal to polarizing currents of ATD excitatory postsynaptic potentials in comparison to those evoked by the abducens internuclear pathway as determined electrophysiologically. Given the differences in the physiologic signals conveyed by the abducens internuclear (eye velocity and eye position) and ATD (head velocity) pathways, the findings in this study suggest that the soma-dendritic stratification of the two inputs to medial rectus motoneurons may provide a means for the separate control of visuomotor and vestibular functions, respectively.     

Abducens internuclear neurons and their role in conjugate horizontal gaze

Experimental evidence suggests that brain stem lesions producing paralysis of lateral gaze and dissociation of conjugate horizontal eye movements have certain common features. Both of these disturbances involve abducens internuclear neurons (Abd IN) or their projections. Attempts were made to determine the course and terminal distribution of Abd IN in the monkey by autoradiographic techniques. Tritiated amino acids injected in the abducens nucleus (Abd N) labeled: (1) root fibers ipsilaterally, and (2) fibers that ascended in medial parts of the contralateral medial longitudinal fasciculus (MLF). In the opposite oculomotor complex (OMC) silver grains were profuse over the ventral nucleus (VN, medial rectus muscle) and patchy over caudal parts of the dorsal nucleus (DN, inferior rectus muscle). Labeling of cells in the reticular formation nucleus to Abd N resulted in transport ipsilaterally, outside the MLF, to the rostral interstitial nucleus of the MLF (RiMLF), a cell group considered to be concerned with vertical eye movements. Bilateral labeling of Abd N and cells of the nucleus prepositus (NPP) resulted in bilateral: (1) transport of isotope via root fibers and the MLF, and (2) selective distribution of silver grains in the OMC. Bilateral silver grain distribution in the OMC suggested profuse terminations in VN, patchy terminations in DN and vertical, linear terminations in caudal parts of the medial nucleus (MN, superior rectus muscle). Comparisons with more discrete unilateral labeling of cells in Abd N suggested that cells of the NPP project selectively to terminations in MN, and may be related to upward eye movements. Two conclusions were drawn: (1) The paresis of ocular adduction which occurs in both anterior internuclear ophthalmophlegia and in paralysis of lateral gaze results from involvement of Abd IN or their ascending projections, and (2) the NPP appears to project selectively to parts of MN of the OMC, a cell group said to provide crossed innervation for the superior rectus muscle.     

Localization of motoneurons controlling the extraocular muscles of the rat

The localization of extraocular motoneurons in the rat was investigated by injecting horseradish peroxidase and [¹²⁵I]wheat germ agglutinin¹⁷ as retrogade tracer substances into individual eye muscles. The organization of subnuclei was found to be most similar to the rabbit. The subgroups representing the medial rectus and inferior rectus muscles are located in the rostral two thirds of the ipsilateral oculomotor nucleus (nIII) with some medial rectus motoneurons scattered laterally along the edge of the medial longitudinal fasciculus. The motor pool controlling the inferior oblique muscle is located in the middle third of the ipsilateral nIII. The motoneurons of the superior rectus muscles are in the caudal two-thirds of contralateral nIII while the levator palpebrae muscle has a bilateral innervation in the oculomotor nucleus. The motoneurons of the superior oblique are located in the contralateral trochlear nucleus although a few labeled neurons were scattered laterally in amongst the fibers of the medial longitudinal fasciculus. The cell bodies of lateral rectus motoneurons regional separation between the latter and internuclear neurons was found after injecting HRP into the oculomotor nucleus.     

Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. II. Inhibitory burst neurons

Electrophysiological and intracellular labelling studies in the cat have identified a population of saccadic burst neurons in the medullary reticular formation that have an inhibitory, monosynaptic projection to the contralateral abducens nucleus. In the present study, intraaxonal recording and injection of horseradish peroxidase were used to identify and characterize the corresponding population of inhibitory burst neurons (IBNs) in the alert squirrel monkey. Squirrel monkey IBNs are located in the reticular formation ventral and caudal to the abducens nucleus and project contralaterally to the abducens. Additional contralateral projections are present to the vestibular nuclei, the nucleus prepositus, and the pontine and medullary reticular formation rostral and caudal to the abducens. All neurons fire a burst of spikes during saccades and are silent during fixation. In most neurons the burst begins 5-15 msec before saccade onset. The number of spikes in the saccadic burst is linearly related to the amplitude of the component of the saccade in the neuron's on-direction. Linear relationships also exist between burst duration and saccade duration and between firing frequency and instantaneous eye velocity. For all neurons, the on-direction is in the ipsilateral hemifield, with a vertical component that may be either upward or downward. Neurons with projections to the vertically related descending and superior vestibular nuclei tend to have on-directions with larger vertical components than neurons that lack these projections. These results, together with those on excitatory burst neurons reported in the preceding paper, demonstrate a reciprocal organization of burst neuron input to the abducens in the monkey similar to that found in the cat and indicate a major role for these neurons in generating the oculomotor activity in motoneurons as well as in other classes of premotor neurons.     

The motor nuclei and sensory neurons of the IIIrd, IVth, and VIth cranial nerves in the monitor lizard, Varanus exanthematicus

The motor nuclei of the oculomotor, trochlear, and abducens nerves of the reptile Varanus exanthematicus and the neurons that subserve the sensory innervation of the extraocular muscles were identified and localized by retrograde and anterograde transport of horseradish peroxidase (HRP). The highly differentiated oculomotor nuclear complex, located dorsomedially in the tegmentum of the midbrain, consists of the accessory oculomotor nucleus and the dorsomedial, dorsolateral, intermediate, and ventral subnuclei. The accessory oculomotor nucleus projects ipsilaterally to the ciliary ganglion. The dorsomedial, dorsolateral, and intermediate subnuclei distribute their axons to the ipsilateral orbit, whereas the ventral subnucleus, which innervates the superior rectus muscle, has a bilateral, though predominantly contralateral projection. The trochlear nucleus, which rostrally overlaps the oculomotor nuclear complex, is for the greater part a comma-shaped cell group situated lateral, dorsal, and medial to the medial longitudinal fasciculus. Following HRP application to the trochlear nerve, almost all retrogradely labeled cells were found in the contralateral nucleus. The nuclear complex of the abducens nerve consists of the principal and accessory abducens nuclei, both of which project ipsilaterally. The principal abducens nucleus is located just beneath the fourth ventricle laterally adjacent to the medial longitudinal fasciculus and innervates the posterior rectus muscle. The accessory abducens nucleus has a ventrolateral position in the brainstem in close approximation to the ophthalmic fibers of the descending trigeminal tract. It innervates the retractor bulbi and bursalis muscles. The fibers arising in the accessory abducens muscles form a loop in or just beneath the principal abducens nucleus before they join the abducens nerve root. The afferent fibers conveying sensory information from the extraocular muscles course in the oculomotor nerve and have their perikarya in the ipsilateral trigeminal ganglion, almost exclusively in its ophthalmic portion.     

Elasmobranch oculomotor organization: anatomical and theoretical aspects of the phylogenetic development of vestibulo-oculomotor connectivity

The oculomotor organization of two elasmobranch species, smooth dogfish (Mustelus canis) and little skate (Raja erinacea), was studied by investigating the extraocular muscle apparatus and the oculomotor motoneuron distribution. The macroscopic appearance of the eye muscles was similar to any lateral-eyed vertebrate species (e.g., goldfish, rabbit). The size of extraocular muscles was expressed by counting single muscle fibers and comparing cross-sectional areas of the extraocular muscles. There were significant differences in the number of fibers in the six extraocular muscles in dogfish, but not in skate. Fiber sizes varied considerably; thus, the number of fibers did not relate to cross-sectional areas. In the dogfish, no one pair of agonist-antagonist extraocular muscles was larger than the others, suggesting that there was no preference for eye movements in a particular plane of space. However, the lateral rectus was more than twice the size of most of the other muscles. In the skate, cross-sectional areas of the horizontal eye muscles were smaller than those of the vertical eye movers. This may indicate a reduced utilization of horizontal eye muscles, which may reflect the bottom-dwelling habitat and mode of locomotion of the skate. The distribution of the extraocular motoneurons was determined by injecting horseradish peroxidase (HRP) into single eye muscles. Medial rectus, superior rectus, and superior oblique motoneuron populations were located contralateral to their respective muscles. Lateral rectus, inferior rectus, and inferior oblique motoneurons were located ipsilateral to their muscles. This distribution is in contrast to almost all other vertebrates studied thus far, where medial rectus motoneurons are located ipsilateral to the muscle which they innervate. The oculomotor arrangement in elasmobranchs is likely to have consequences for the circuitry responsible for the production of conjugate compensatory eye movements in the horizontal plane. We hypothesize that, in contrast to other vertebrates, the basic elasmobranch vestibulo-ocular reflex pathway consists of three identically structured three-neuron-arcs connecting the three semicircular canals to their respective extraocular muscles. This innervation pattern may constitute a special feature of the elasmobranch brain or a phylogenetically older arrangement of eye movement pathways.     

Comparison of vestibular and abducens internuclear projections to the medial rectus subdivision of the oculomotor nucleus in the monkey

Comparisons were made of projections from the vestibular nuclei (VN) and abducens internuclear neurons (AIN) to cell group A of the medial rectus subdivision (MRS) of the oculomotor nuclear complex. Cell group A, the major component of the MRS, receives projections only from the ipsilateral VN and the contralateral AIN. Neither ipsilateral vestibular projections to cell group A, arising from the medial vestibular nucleus, nor projections from MVN to the opposite abducens nucleus, match the massive projection of AIN to the MRS.