The vestibuloocular reflex of the adult flatfish. II. Vestibulooculomotor connectivity

The peripheral and central oculomotor organization of the adult flatfish presents no morphological substrates that suffice to explain adaptive changes in its vestibuloocular reflex system. The necessity for an adaptation occurs because of a 90 degrees displacement of the vestibular with respect to the extraocular coordinate axes during metamorphosis. Since a reorganization of vestibuloocular pathways must be hypothesized (12), the location and termination of electrophysiologically identified secondary vestibular neurons with focus on the horizontal canal system was studied with the intracellular horseradish peroxidase method in adult winter flounders. Pseudopleuronectes americanus. The oculomotor target sites of vertical canal related neurons were similar to those described in mammals. Presumed excitatory anterior canal neurons bifurcated after the main axon had crossed the midline. The descending branch headed toward the spinal cord. The ascending branch reached the oculomotor nucleus via the contralateral medial longitudinal fasciculus and terminated in the superior rectus and inferior oblique subdivisions. Presumed inhibitory posterior canal neurons ascended ipsilaterally in the medial longitudinal fasciculus and terminated mainly in the superior rectus and inferior oblique subdivisions. Horizontal canal neurons exhibited characteristics distinctly different from mammalian ones. Two types of second-order neurons were observed. In the first case, cell bodies were located in the anterior portion of the vestibular nuclear complex. After crossing the midline, the axon ascended in the contralateral medial longitudinal fasciculus. Major termination sites were found in the inferior oblique and superior rectus subdivisions of the oculomotor nucleus. Axonal branches then recrossed the midline and terminated in identical locations on the ipsilateral side. In the second case, cell bodies were located in the descending vestibular nucleus. Their axons crossed the midline and also ascended in the contralateral medial longitudinal fasciculus. Major termination sites were in the trochlear nucleus and in the inferior rectus subdivision of the oculomotor nucleus. As in the first case, axonal branches also recrossed the midline and terminated in identical motoneuron pools on the ipsilateral side. The above target sites were exactly those expected to be used in a reciprocal excitatory-inhibitory fashion during compensatory eye movements. Head-down movement would be excitatory for the lower horizontal canal producing contractions of both superior recti and inferior obliques as well as relaxation of the antagonistic inferior recti and superior obliques.(ABSTRACT TRUNCATED AT 400 WORDS)     

Vertical eye movement-related secondary vestibular neurons ascending in medial longitudinal fasciculus in cat. II. Direct connections with extraocular motoneurons

1. The preceding study in the alert cat has shown that many secondary vestibular axons that ascend in the medial longitudinal fasciculus (MLF) increase their firing rate in proportion to downward eye position. In the present study, projection and termination of these downward-position-vestibular (DPV) neurons within extraocular motoneuron pools were studied electrophysiologically by spike-triggered averaging techniques and morphologically be reconstructing their axonal trajectory after intra-axonal injection of horseradish peroxidase (HRP). 2. Extracellular field potentials recorded within the trochlear nucleus and/or the inferior rectus subdivision of the oculomotor nucleus were averaged by the use of spike potentials of single DPV neurons as triggers. All the crossed-DPV axons tested induced negative unitary field potentials in the trochlear nucleus (n = 9) and in the inferior rectus subdivision of the oculomotor nucleus (n = 5), suggesting that they made monosynaptic excitatory connection with motoneurons in these nuclei. The four crossed-DPV axons tested in the two motoneuron pools induced unitary field potentials in both. The majority of crossed-DPV axons terminated in these nuclei were directly activated from the caudal MLF, indicating that they had descending collaterals projecting to the spinal cord as well. The uncrossed-DPV axons did not induce such unitary field potentials either in the trochlear nucleus (n = 4) or in the inferior rectus subdivision (n = 3). 3. All the uncrossed-DPV axons examined (n = 14) induced positive unitary field potentials in the superior rectus subdivision of the oculomotor nucleus, suggesting that they made monosynaptic inhibitory connections with motoneurons innervating the superior rectus muscle. These uncrossed-DPV axons displayed regular firing patterns and were not activated from the caudal MLF. None of the crossed-DPV axons tested (n = 4) induced unitary field potentials in the superior rectus subdivision. 4. Five crossed-DPV axons were injected with HRP. All these axons ascended in the MLF contralateral to their soma, gave off many collaterals to the trochlear nucleus, and projected more rostrally. For three well-stained axons, numerous terminal branches were also found in the rostroventral part of the contralateral oculomotor nucleus, the area corresponding to the inferior rectus subdivision. Some collaterals in the oculomotor nucleus recrossed the midline to terminate in the medial part of the ipsilateral oculomotor nucleus. Other terminations were observed in the interstitial nucleus of Cajal and in the periaqueductal gray adjacent to the oculomotor nucleus. The crossed axons injected included both regular and irregular types, and three of the four examined were activated from the caudal MLF.(ABSTRACT TRUNCATED AT 400 WORDS)     

Morphology of posterior canal related secondary vestibular neurons in rabbit and cat

The morphology of secondary vertical vestibular neurons was investigated by injection of horseradish peroxidase (HRP) into cells connected to the posterior canal system in rabbits (lateral-eyed animals) and cats (frontal-eyed animals). Vestibular neurons were identified by stimulation with bipolar electrodes implanted into the ampullae of the anterior and posterior (PC) semicircular canals of pigmented rabbits; in the cat, these cells were identified by natural and electrical stimulation. Axons monosynaptically activated by PC stimulation were injected with HRP in the medial longitudinal fasciculus (MLF). These were later reconstructed by light microscopy after the brains had been processed with a DAB-CoCl2 method. In the rabbit the majority of the axons bifurcated after crossing the midline with one branch ascending and the other descending in the MLF. The ascending branches gave rise to collaterals that terminated in both the trochlear nucleus and the inferior rectus subdivision of the oculomotor nucleus. In addition some axons also sent collaterals into the paramedian pontine reticular formation, the periaqueductal grey and the interstitial nucleus of Cajal. The descending branches were followed to the caudal part of the medulla in the MLF and gave rise to collaterals terminating in the vestibular nuclei, the medullary reticular formation, the perihypoglossal nuclei, the abducens nucleus, and the facial nucleus. In another cell type axons crossed the midline without giving off any collaterals and proceeded caudally in the caudal MLF. The synaptic effects of the two types of cells were concluded to be excitatory and inhibitory, respectively. Cell bodies of contralaterally projecting neurons were located in either the medial or ventro-lateral vestibular nuclei. In the cat we observed two neuron classes, with contralaterally projecting axons, whose synaptic effects are presumably excitatory. Their cell somata were located in the medial vestibular nucleus. Termination patterns were similar to both the trochlear and oculomotor nuclei, but neither projected to the abducens nucleus. One class of neurons was almost identical to that found in the rabbit with the main axon bifurcating in the MLF. The second type lacked a descending branch in the MLF. Axon collaterals of the latter type crossed the midline within the oculomotor nucleus after terminating in the inferior rectus subdivision to reach a similar portion of the ipsilateral oculomotor nucleus. Collaterals of these axons also terminated bilaterally in the supraoculomotor region between trochlear and oculomotor nucleus, the interstitial nucleus of Cajal and prerubral loci (including the fields of Forel). In similarity to the rabbit, presumed inhibitory vestibular neurons were found with axons directed caudally in the MLF without brain stem collaterals.(ABSTRACT TRUNCATED AT 400 WORDS)     

Second-order vestibular neuron morphology of the extra-MLF anterior canal pathway in the cat

Second-order vestibular neurons form the central links of the vestibulo-oculomotor three-neuron arcs that mediate compensatory eye movements. Most of the axons that provide for vertical vestibulo-ocular reflexes ascend in the medial longitudinal fasciculus (MLF) toward target neurons in the oculomotor and trochlear nuclei. We have now determined the morphology of individual excitatory second-order neurons of the anterior semicircular canal system that course outside the MLF to the oculomotor nucleus. The data were obtained by the intracellular horseradish peroxidase method. Cell somata of the extra-MLF anterior canal neurons were located in the superior vestibular nucleus. The main axon ascended through the deep reticular formation beneath the brachium conjunctivum to the rostral extent of the nucleus reticularis tegmenti pontis, where it crossed the midline. The main axon continued its trajectory to the caudal edge of the red nucleus from where it coursed back toward the oculomotor nucleus. Within the oculomotor nucleus, collaterals reached superior rectus and inferior oblique motoneurons. Some axon branches recrossed the midline within the oculomotor nucleus and reached the superior rectus motoneuron subdivision on that side. Since these neurons did not give off a collateral toward the spinal cord, they were classified as being of the vestibulo-oculomotor type and are thought to be involved exclusively in eye movement control. The signal content and spatial tuning characteristics of this anterior canal vestibulo-oculomotor neuron class remain to be determined.     

Direct excitatory and inhibitory synaptic inputs from the medial mesodiencephalic junction to motoneurons innervating extraocular oblique muscles in the cat

Summary This study investigated the nature of synaptic inputs from the Forel's field H (FFH) in the medial mesodiencephalic junction to inferior oblique (IO) motoneurons in the oculomotor nucleus and superior oblique (SO) motoneurons in the trochlear nucleus in anesthetized cats, using intracellular recording techniques. Stimulation of the FFH induced monosynaptic EPSPs in IO motoneurons on both sides. Paired stimulation of the ipsilateral FFH and contralateral vestibular nerve substantiated that the FFH-induced EPSPs were caused mainly by direct excitatory fibers from the FFH to IO motoneurons and partly by axon collaterals of excitatory neurons in the vestibular nuclei. Among parts of the FFH, the medial part was most effective for producing the EPSPs. Systematic tracking with the stimulating electrode in and around the FFH revealed that effective sites of stimulation inducing negative field potentials in the IO subdivision of the oculomotor nucleus, identified as extracellular counterparts of the EPSPs in IO motoneurons, were also located in the interstitial nucleus of Cajal, nearby reticular formation and posterior commissure, besides within and near the medial part of the FFH. Areas far rostral, dorsal and ventral to the FFH were ineffective. EPSP-IPSPs or EPSPs were mainly induced in SO motoneurons on both sides by FFH stimulation. Latencies of these EPSPs and IPSPs were close to those of the EPSPs in IO motoneurons, indicating their monosynaptic nature. Effective stimulation sites for inducing these synaptic potentials overlapped those for the EPSPs in IO motoneurons. Based on these results, it was suggested that excitatory and inhibitory premotor neurons directly controlling IO and SO motoneurons were located within and near the medial part of the FFH.     

A note on the development of the vestibulo-ocular pathway in the chicken

Summary The vestibulo-ocular pathways have been examined in embryonic chicks using horseradish peroxidase or dil as retrograde and anterograde tracers. The vestibular neurons project to the rostral, external eye motor nuclei over one or the other of three separate pathways; the ipsilateral and controlateral medial longitudinal fascicle and the contralateral brachium conjunctivum. The brachium conjunctivum component originates dorsally in the superior vestibular region and projects to the contralateral inferior oblique and superior rectus motor nuclei. An ipsilateral component of the medial longitudinal fascicle is labeled from more ventral sites in the vestibulo-cerebellar process and terminates in the ipsilateral superior oblique and inferior rectus nuclei. The contralateral medial longitudinal fascicle component originates still more ventrally and terminates in the contralateral superior oblique and inferior rectus motor nuclei. Accordingly, the vestibulo-ocular pathways in chickens operate predominantly on synergistic pairs of external eye muscles. These selective terminal fields are established within a day or two after the first terminals invade the eye motor nuclei during embryo-genesis.Abbreviations Br.C. brachium conjunctivum - EW Edinger Westfahl nucleus - MLF medial longitudinal fascicle - IO inferior oblique muscle - RI inferior rectus muscle - RM medial rectus muscle - RS superior rectus muscle - SO superior oblique muscle - V-O vestibular-ocular - i ipsilateral - x contralateral This paper is dedicated to Professor Fred Walberg on the occasion of his 70th birthday     

The time course of retrograde transsynaptic transport of tetanus toxin fragment C in the oculomotor system of the rabbit after injection into extraocular eye muscles

Summary The aim of this study was to determine the optimal survival time for labelling those neurons that monosynaptically terminate on extraocular motoneurons, i.e. the premotor neurons, after an injection of tetanus toxin fragment C, a retrograde transsynaptic tracer substance, into the eye muscle of the rabbit. Concentrated fragment C was injected into the inferior rectus or inferior oblique muscle and detected immunocytochemically in the brain after survival times of 8 h, 17 h, 2 d, 3 d, 4 d, 5 d, 6 d, 8 d and 12 d. Immunoreactivity was confined to granules within motoneuronal and premotor neuronal cell bodies, but became associated with punctate profiles outlining the somata with longer survival times. The strongest and most consistent labelling of premotor cell bodies was seen after 4 days survival time. The transsynaptic labelling pattern was shown to vary for individual premotor pathways.Abbreviations III oculomotor nucleus - IV trochlear nucleus - Vmes mesencephalic trigeminal nucleus - Vmt motor trigeminal nucleus - VI abducens nucleus - VIacc accessory abducens nucleus - VII facial nucleus - BC brachium conjunctivum, co cochlear nucleus - CR restiform body - d dentate nucleus - DAB diamino-benzidine-tetrahydrochloride - HRP horseradish peroxidase - iC interstitital nucleus of Cajal, iv inferior vestibular nucleus - lgn_d lateral geniculate nucleus dorsalis - lgn_v lateral geniculate nucleus ventralis - lv lateral vestibular nucleus - mgn medial geniculate nucleus - MLF medial longitudinal fasciculus - mv_p medial vestibular nucleus pars parvocellularis - mv_m medial vestibular nucleus pars magnocellularis (= ventral part of the lv) - NIII oculomotor nerve - NV trigeminal nerve - NVII facial nerve - NVIII vestibular nerve - PC posterior commissure - pg periaquaeductal grey - ppH nucleus praepositus hypoglossi - riMLF rostral interstitial nucleus of the medial longitudinal fasciculus - rn red nucleus - sc superior colliculus - sn substantia nigra - so superior olive - sv superior vestibular nucleus - sv_c superior vestibular nucleus contralateral - sv_i superior vestibular nucleus ipsilateral - TR tractus retroflexus - Y Y-group zi zona incerta     

Operational unit responsible for plane-specific control of eye movement by cerebellar flocculus in cat

1. Main findings in our previous studies are as follows: 1) there are three Purkinje cell zones running perpendicular to the long axis of the folia in the cat flocculus, 2) the caudal zone controls activity of the superior rectus (SR) and inferior oblique (IO) extraocular muscles via the y-group and oculomotor nucleus (OMN) neurons, and 3) the middle zone controls activity of the lateral (LR) and medial rectus (MR) muscles via the medial vestibular (MV) and abducens nucleus (ABN) neurons. In the present study, the neuronal pathways from the remaining rostral zone were investigated in the anesthetized cat. 2. Target neurons of rostral zone inhibition in the superior vestibular nucleus (SV) were identified by observing cessation of spontaneous discharges after rostral zone stimulation. Efferent projections were studied by the use of systematic microstimulation techniques. Unitary responses to stimulation of the eighth nerves were also investigated. 3. There are two types of the target neurons: 1) those, being located in the central and dorsal parts of the SV, project to the trochlear and oculomotor nuclei innervating superior oblique and inferior rectus muscles via the ipsilateral medial longitudinal fasciculus (MLF); and 2) those, being located along the dorsal border of the SV, project to the contralateral oculomotor nucleus innervating superior rectus and inferior oblique muscles via the extra-MLF route. 4. Both types receive monosynaptic anterior canal nerve input but not posterior canal nerve input. Some neurons receive polysynaptic excitatory input from the contralateral eighth nerve, although commissural inhibition was never observed. 5. From neuronal connections of the rostral and caudal zones and action of the extraocular muscles, it was expected that 1) activity changes of Purkinje cells in the rostral and/or caudal zones on one side resulted in conjugate eye movement in the plane of the anterior canal on the side of the activity changes, 2) cooperative increased activity on both sides resulted in conjugate downward eye movement, and 3) increased activity on one side and decreased activity on the other side resulted in conjugate rotatory eye movement. The rostral and caudal zones may be responsible for eye-movement control in the sagittal plane by cooperative activity changes on both sides and in the transverse plane by reciprocal activity changes on both sides. For eye-movement control in the anterior canal plane, Purkinje cell activity on one side would be sufficient to produce the required movement. In a functional sense, we call the rostral and caudal zones, the vertical-plane zones.(ABSTRACT TRUNCATED AT 400 WORDS)     

Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits

Summary In anesthetized albino rabbits, ampullary branches of the vestibular nerve were stimulated electrically. Prominent and stable reflex contraction was induced in extra-ocular muscles by applying single current pulses of relatively long duration, 3–5 msec. Survey with a glass microelectrode revealed that, during application of relatively wide pulses to a canal, primary vestibular fibers discharged impulses repetitively at a rate as high as 300–1400/sec and that after being transmitted across second-order vestibular neurons these impulses built up summated EPSPs in oculomotor neurons, large enough to trigger off motoneuronal discharges. From each semicircular canal, prominent reflex contraction was evoked selectively in two muscles; from the anterior canal in the ipsilateral superior rectus and contralateral inferior oblique; from the horizontal canal in the ipsilateral medial rectus and contralateral lateral rectus; and from the posterior canal in the ipsilateral superior oblique and contralateral inferior rectus. Acute lesion experiments indicated that signals for this excitation reached IIIrd and IVth nuclei via three different pathways; from the anterior canal through the ipsilateral brachium conjunctivum, from the horizontal canal through the ipsilateral fasciculus longitudinalis medialis and from the posterior canal through the contralateral fasciculus longitudinalis medialis.This work was supported by a grant from Educational Ministry of Japan (844021).     

Structure of the primate oculomotor burst generator. I. Medium-lead burst neurons with upward on-directions

1. To investigate the structure of the primate burst generator for vertical saccades, we obtained intra-axonal records from vertical medium-lead burst neurons with upward on-directions (UMLBs) in alert, behaving squirrel monkeys, while monitoring their spontaneous eye movements. After physiological characterization, these UMLBs were injected with horseradish peroxidase. 2. UMLBs (n = 14) had no spontaneous activity and emitted bursts of action potentials that preceded rapid eye movements by approximately 6 ms. Parameters of the burst (duration and number of spikes) were highly correlated with parameters of the rapid eye movement (duration and amplitude of the upward displacement of the eyes). 3. The axons of six UMLBs projected to the oculomotor complex. Their somata (4 were recovered) were all in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). Their axons traveled caudally in the medial longitudinal fasciculus (MLF) and ramified in the interstitial nucleus of Cajal (NIC) before entering the oculomotor nucleus. Five axons terminated bilaterally in the subdivisions innervating the superior rectus and inferior oblique muscles and therefore were presumed to be excitatory. One axon terminated in the ipsilateral inferior rectus and superior oblique subdivisions of the oculomotor complex and was presumed to be inhibitory. 4. Additionally, our data demonstrate that the nucleus of the posterior commissure (nPC) may also contain UMLBs. The axon of one such neuron crossed the midline within the posterior commissure and provided terminal fields to the contralateral nPC, riMLF, NIC, and the mesencephalic reticular formation but not to the oculomotor complex. 5. In conclusion, our data demonstrate that the rostral mesencephalon of the monkey contains neurons that have both the activity and the connections that are necessary either to provide motoneurons innervating extraocular muscles of both eyes with the pulse of activity they display during upward saccades or to inhibit their antagonists. Furthermore, our data demonstrate that some UMLBs are better suited for closing the feedback path of the local feedback loop rather than for providing direct input to extraocular motoneurons.     

Localization of proprioceptive neurons innervating the muscle spindles of pig extraocular muscles studied by horseradish peroxidase labelling

Each muscle of the extraocular muscles, containing abundant muscle spindles, was exposed to horseradish peroxidase (HRP) on 8 young pigs (2-month-old, 20-30 kg in body weight, both sexes). The results obtained are follows: The HRP-labelled neurons innervating the superior rectus muscle were always found in a crescent ventro-medio-dorsal fashion in the most medial position of the contralateral oculomotor nucleus. The HRP-labelled cells for the medial rectus muscle appeared close to the superior rectus group in the ipsilateral nucleus. The labelled cells for the inferior rectus muscle appeared in the ventrolateral position of the ipsilateral nucleus and those for the inferior oblique muscle in the area between the medial rectus and inferior rectus muscle groups. The labelled cells for the superior oblique muscle were found in the contralateral trochlear nucleus and those for the lateral rectus muscle bilaterally in the abducens nuclei, predominantly on the ipsilateral side and poorly on the contralateral side. The HRP-labelled cells were composed of large (alpha) and small (gamma) multipolar cells and of bipolar, oval or round (proprioceptive) cells, all intermingled together within the nucleus. The bipolar cells have been also identified in the 3 nuclei by means of Nissl staining technique. On this basis, they should be considered as the proprioceptive neurons. In the shrew-moles, the cell bodies of the proprioceptive neurons innervating the snout muscle spindles have been found close to the ipsilateral glossopharyngeal ganglion and those of the somatic sensory neurons in the ipsilateral trigeminal ganglion. In the pigs, no HRP-labelled cells were found in the trigeminal mesencephalic tract nucleus, but the HRP-labelled cells were found in the ipsilateral trigeminal and the superior cervical sympathetic ganglia. From the results, it could be emphasized that the proprioceptive neurons innervating the pig extraocular muscle spindles are located within the nuclei of the IIIrd, IVth and VIth cranial nerves.     

Spatial properties of second-order vestibulo-ocular relay neurons in the alert cat

Second-order vestibular nucleus neurons which were antidromically activated from the region of the oculomotor nucleus (second-order vestibuloocular relay neurons) were studied in alert cats during whole-body rotations in many horizontal and vertical planes. Sinusoidal rotation elicited sinusoidal modulation of firing rates except during rotation in a clearly defined null plane. Response gain (spike/s/deg/s) varied as a cosine function of the orientation of the cat with respect to a horizontal rotation axis, and phases were near that of head velocity, suggesting linear summation of canal inputs. A maximum activation direction (MAD) was calculated for each cell to represent the axis of rotation in three-dimensional space for which the cell responded maximally. Second-order vestibuloocular neurons divided into 3 non-overlapping populations of MADs, indicating primary canal input from either anterior, posterior or horizontal semicircular canal (AC, PC, HC cells). 80/84 neurons received primary canal input from ipsilateral vertical canals. Of these, at least 6 received input from more than one vertical canal, suggested by MAD azimuths which were sufficiently misaligned with their primary canal. In addition, 21/80 received convergent input from a horizontal canal, with about equal number of type I and type II yaw responses. 4/84 neurons were HC cells; all of them received convergent input from at least one vertical canal. Activity of many vertical second-order vestibuloocular neurons was also related to vertical and/or horizontal eye position. All AC and PC cells that had vertical eye position sensitivity had upward and downward on-directions, respectively. A number of PC cells had MADs centered around the MAD of the superior oblique muscle, and 2/3 AC cells recorded in the superior vestibular nucleus had MADs near that of the inferior oblique. Thus, signals with spatial properties appropriate to activate oblique eye muscles are present at the second-order vestibular neuron level. In contrast, none of the second-order vestibuloocular neurons had MADs near those of the superior or inferior rectus muscles. Signals appropriate to activate these eye muscles might be produced by combining signals from ipsilateral and contralateral AC neurons (for superior rectus) or PC neurons (for inferior rectus). Alternatively, less direct pathways such as those involving third or higher order vestibular or interstitial nucleus of Cajal neurons might play a crucial role in the spatial transformations between semicircular canals and vertical rectus eye muscles.     

Localization of motoneurons innervating the extraocular muscles in the chameleon (Chamaeleo chameleon)

The topography and localization of motoneurons innervating the six extraocular muscles in the chameleon (Chamaeleo chameleon) was studied following HRP injection in each of these individual muscles. Four muscles were innervated ipsilaterally: medial rectus, inferior rectus, inferior oblique and lateral rectus. The medial rectus muscle was innervated by the dorsomedial part of the oculomotor nucleus. The innervation to the inferior rectus muscle arose from the lateral part of the intermediate oculomotor subnucleus, which extended to the lateral part of the dorsal subdivision. The lateral rectus muscle was innervated by the abducens nucleus, which was composed by two subgroups of labeled cells, respectively observed in the principal and accessory abducens subnuclei, whereas efferents to the inferior oblique muscle originated from both the ventral and intermediate oculomotor subnuclei. The contralateral pattern consisted of motoneurons innervating the superior rectus and the superior oblique that were located respectively in the caudal portion of the ventral oculomotor nucleus and in the trochlear nucleus. These results confirmed data reported in most vertebrate species, and were discussed from a comparative and functional point of view.     

Vestibular projections to the nuclei of the extraocular muscles Degeneration resulting from discrete partial lesions of the vestibular nuclei in the monkey

In 35 monkeys attempts were made to produce localized unilateral lesions in individual vestibular nuclei in order to study vestibular projections to nuclei of the extraocular muscles. Portions of the medial, superior and inferior vestibular nuclei were destroyed selectively; lesions in Deiters' nucleus involved small portions of either the superior or inferior vestibular nuclei. Fiber degeneration was studied by the Nauta-Gygax technic. Exclusively ascending fibers from the superior vestibular nucleus project to ipsilateral extraocular nuclei. Ascending fibers from the inferior vestibular arise only from rostral portions of the nucleus, are not numerous and pass to all extraocular nuclei. The medial vestibular nucleus projects ascending fibers via the MLF bilaterally, asymmetrically and differentially to all extraocular nuclei. Prominent projections pass to: (a) the contralateral trochlear nucleus, and (b) the contralateral intermediate cell column and the ipsilateral ventral nucleus of the oculomotor complex. Ascending fibers from Deiters' nucleus, arising only from ventral portions of the nucleus, project primarily to: (a) the contralateral abducens and trochlear nuclei, and (b) specific asymmetrical portions of the oculomotor complex. Ascending vestibular fibers from the medial and lateral vestibular nuclei appear capable of mediating all patterned eye movements resulting from stimulation of ampullary nerves from individual semicircular canals. Vestibular projections to nuclei of the extraocular muscles are most abundant to those nuclei innervating muscles whose primary functions concern horizontal and rotatory eye movements.     

Branching pattern and properties of vertical- and horizontal-related excitatory vestibuloocular neurons in the cat

1. The axonal trajectories of excitatory vestibuloocular neurons and their synaptic contacts with extraocular motoneurons were studied by means of spike-triggered signal averaging and microstimulation techniques. A majority of the excitatory neurons related to the vertical semicircular canals were located in the border of the descending and medial nuclei and the rostral half of the descending nucleus. 2. Individual vestibuloocular neurons activated by stimulation of the ampullary nerve of the anterior semicircular canal excited motoneurons within both the contralateral inferior oblique and contralateral superior rectus motoneuron pools. 3. Individual vestibuloocular neurons receiving input from the ampullary nerve of the posterior semicircular canal excited motoneurons in both the contralateral trochlear nucleus and contralateral inferior rectus motoneuron pools. The branching pattern of single vestibuloocular neurons activated by the anterior and posterior canals probably underlies conjugate eye movement during vertical head rotation. 4. Time to peak and shape indices of unitary excitatory postsynaptic potentials (EPSPs) suggested that the location of the synaptic contact of vestibuloocular neurons was on the soma or proximal dendrites of the target extraocular motoneurons. 5. In contrast, we did not find conclusive evidence that single vestibuloocular neurons receiving input from the horizontal semicircular canal give off axon collaterals to motoneurons innervating both the contralateral lateral rectus and the ipsilateral medial rectus muscles. Projection of horizontal vestibuloocular neurons to motoneurons supplying individual muscles might be useful for convergence during horizontal head movement.     

Localization of motoneurons innervating the extraocular muscles in the chameleon (Chamaeleo chameleon)

The topography and localization of motoneurons innervating the six extraocular muscles in the chameleon (Chamaeleo chameleon) was studied following HRP injection in each of these individual muscles. Four muscles were innervated ipsilaterally: medial rectus, inferior rectus, inferior oblique and lateral rectus. The medial rectus muscle was innervated by the dorsomedial part of the oculomotor nucleus. The innervation to the inferior rectus muscle arose from the lateral part of the intermediate oculomotor subnucleus, which extended to the lateral part of the dorsal subdivision. The lateral rectus muscle was innervated by the abducens nucleus, which was composed by two subgroups of labeled cells, respectively observed in the principal and accessory abducens subnuclei, whereas efferents to the inferior oblique muscle originated from both the ventral and intermediate oculomotor subnuclei. The contralateral pattern consisted of motoneurons innervating the superior rectus and the superior oblique that were located respectively in the caudal portion of the ventral oculomotor nucleus and in the trochlear nucleus. These results confirmed data reported in most vertebrate species, and were discussed from a comparative and functional point of view. Accepted: 18 June 1999     

Vertical semicircular canal inputs to cat extraocular motoneurons

Summary Synaptic potentials were recorded in identified extraocular motoneurons in anesthetized cats, following stimulation of ampullary nerves of the anterior and posterior semicircular canals.Superior rectus motoneurons received disynaptic EPSPs and IPSPs following stimulation of the two ampullary nerves of the anterior and posterior semicircular canals, respectively. In the inferior rectus motoneurons, the effects of anterior and posterior semicircular canal stimulation were a mirror image of those on superior rectus motoneurons.Inferior oblique motoneurons developed disynaptic EPSPs and IPSPs following stimulation of the ampullary nerves of the contralateral anterior and ipsilateral posterior semicircular canals, respectively. In addition, some inferior oblique motoneurons displayed disynaptic IPSPs following stimulation of the contralateral ampullary nerve of the posterior semicircular canal. In the superior oblique (trochlear) motoneurons, disynaptic EPSPs and IPSPs were recorded after stimulation of the contralateral posterior and ipsilateral anterior semicircular canals, respectively.There was no significant connection between the ampullary nerves of the vertical semicircular canals and motoneurons innervating lateral and medial rectus muscles.Abbreviations i- Ipsilateral to the recorded motoneuron - c- Contralateral to the recorded motoneuron - ACN Ampullary nerve of the anterior semicircular canal - HCN Ampullary nerve of the horizontal semicircular canal - PCN Ampullary nerve of the posterior semicircular canal - IO Inferior oblique - IR Inferior rectus - LR Lateral rectus - MR Medial rectus - SO Superior oblique - SR Superior rectus - EPSP Excitatory postsynaptic potential - IPSP Inhibitory postsynaptic potential - PSP Postsynaptic potential - MLF Medial longitudinal fasciculus     

Pathways and terminations of axons arising in the fastigial oculomotor region of macaque monkeys.

The majority of axons from the fastigial oculomotor region (FOR) decussated in the cerebellum at all rostrocaudal levels of the fastigial nucleus (FN) and entered the brainstem via the contralateral uncinate fasciculus (UF). Some decussated axons separated from the UF and ran medial to the contralateral superior cerebellar peduncle and ascended to the midbrain. Uncrossed FOR axons advanced rostrolaterally in the ipsilateral FN and entered the brainstem via the juxtarestiform body. The decussated fibers terminated in the brainstem nuclei that are implicated in the control of saccadic eye movements. In the midbrain, labeled terminals were found in the rostral interstitial nucleus of the medial longitudinal fasciculus, a medial part of Forel's H-field, the periaqueductal gray, the posterior commissure nucleus, and the superior colliculus of the contralateral side. In the pons and medulla, FOR fibers terminated in a caudal part of the pontine raphe, the paramedian pontine reticular formation, the nucleus reticularis tegmenti pontis, the dorsomedial pontine nucleus of the contralateral side, and the dorsomedial medullary reticular formation of both sides. In contrast, FOR projections to the vestibular complex were bilateral and were mainly to the ventral portions of the lateral and inferior vestibular nuclei. No labeled terminals were found in the following brainstem nuclei which are considered to be involved in oculomotor function: oculomotor and trochlear nuclei, interstitial nucleus of Cajal, medial and superior vestibular nuclei, periphypoglossal nuclei, and dorsolateral pontine nucleus. Labeling appeared in the red nucleus only when HRP encroached upon the posterior interposed nucleus.     

Axon collaterals to the extraocular motoneuron pools of inhibitory vestibuloocular neurons activated from the anterior, posterior and horizontal semicircular canals in the cat

The branching pattern of inhibitory vestibuloocular neurons and their synaptic contacts with extraocular motoneurons were studied by means of spike-triggered averaging and local stimulation techniques. Individual vestibuloocular neurons activated by stimulation of the ampullary nerve of the anterior semicircular canal (ACN) inhibited motoneurons in both the ipsilateral (i-) trochlear nucleus and i-inferior rectus motoneuron pools. Individual vestibuloocular neurons receiving input from the ampullary nerve of the posterior semicircular canal (PCN) inhibited motoneurons in both the i-inferior oblique and i-superior rectus motoneuron pools. Probably, these axonal trajectories underlie conjugate eye movement during vertical head rotation. No conclusive evidence was found to indicate that single inhibitory vestibular neurons receiving input from the horizontal semicircular canal (HCN) give off axon collaterals to the i-abducens and the contralateral medial rectus motoneurons. A separate projection of HCN-related neurons to motoneurons supplying the lateral and medial rectus muscles might be useful for convergence during horizontal head movement.     

Arborization of axons in oculomotor nucleus identified by vestibular stimulation and intra-axonal injection of horseradish peroxidase

Summary Axons in the medial rectus (MR) subdivisions of the oculomotor nucleus were identified by horizontal rotation and by electrical stimulation of the vestibular nerves and abducens nuclei. Three types of axons (vestibular type I and II and abducens interneurons) were then injected intra-axonally with horseradish peroxidase (HRP). Each injected axon was reconstructed under the microscope in the frontal and horizontal planes and terminal arborization and boutons contacting with MR motoneurons were studied. The MR motoneurons were identified by retrograde uptake of HRP, HRP being injected in the MR muscle prior to the intra-axonal experiment.The main types of horizontal canal-related axons were as follows: (1) ATD-unilateral termination axons: Most type I axons were of this type. Axons ascended in ascending tract of Deiters (ATD) to the oculomotor nucleus and terminated in ipsilateral MR area. (2) ATD-bilateral termination axons: Very few secondary canal responsive axons were in this group. Axons ascended in ATD to the oculomotor nucleus and terminated in MR motoneuron areas bilaterally and in the Edinger-Westphal nucleus. (3) MLF-bilateral termination axons: Most type II neurons were in this group. Axons went up in the contralateral MLF and into both oculomotor nuclei. Their branches distributed to several motoneuron areas but only infrequently to the MR area; and to the Edinger-Westphal nucleus. (4) AB interneuron axons: Axons ascended in the MLF contralateral to cells of origin and terminated in the contralateral MR motoneuron area.Supported by USPHS Grant No. 06658