Morphology of physiologically identified second-order vestibular neurons in cat, with intracellularly injected HRP

The morphology of horizontal canal second-order type I neurons was investigated by intracellular staining with horseradish peroxidase (HRP) and three-dimensional reconstruction of the cell bodies and axons. Axons penetrated in and around the abducens nucleus were identified as originating from type I neurons by their characteristic firing pattern to horizontal rotation and by their monosynaptic response to stimulation of the ipsilateral vestibular nerve. A total of 47 type I neurons were stained. The cell bodies were located in the rostral portion of the medial vestibular nucleus (MVN) and were large or medium sized and had rather elongated shapes and rich dendritic arborizations. The neurons were divided into two groups: those which projected to the contralateral side of the brain stem (type Ic neurons) and those which projected to the ipsilateral side of the brainstem (type Ii neurons). All stem axons of type Ic neurons crossed the midline and bifurcated into rostral and caudal branches in the contralateral medial longitudinal fasciculus (MLF). Two or three collaterals arising close to this bifurcation distributed terminals in a relatively wide area in the contralateral abducens nucleus. Some of these collaterals projected further to the contralateral MVN and thus are vestibular commissural axons. Some of the rostral and caudal stem axons had collaterals which projected to the contralateral nucleus prepositus hypoglossi (PH), nucleus raphe pontis, or medullary reticular formation. There were at least six classes of type Ii neurons, most of which distributed to a relatively limited region in the ipsilateral abducens nucleus and they were categorized according to their future projections into the following categories: A) no further collaterals beyond the abducens nucleus; B) collaterals in the abducens nucleus and a branch descending and terminating in ipsilateral PH; C) projected to the abducens nucleus, PH, and an area rostral to the abducens nucleus; D) projected to the abducens nucleus and to ipsilateral reticular formation rostral and caudal to the abducens nucleus; E) collaterals in the abducens nucleus and a thick caudal stem axon entering and descending in ipsilateral MLF; F) a thick caudal stem axon entering and descending in ipsilateral MLF and no collaterals to the abducens nucleus. Some type Ii neurons also had recurrent collaterals which projected back to the ipsilateral MVN; these may inhibit type II neurons during ipsilateral rotation.     

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.     

Peripheral and central oculomotor organization in the goldfish, Carassius auratus

Peripheral and central oculomotor organization was studied in the goldfish. The sizes of the extraocular muscles were quantified by counting the fibers contained in a given muscle and by area measurements of the cross-sectional surfaces. All the muscles were of approximately similar size. Kinematics were determined by electrical stimulation of a given muscle. The macroscopic appearance and kinematics of the muscles had the characteristics of other lateral-eyed animals (e.g., rabbit). Locations of extraocular motor neurons were found by retrograde transport of horseradish peroxidase (HRP) following injections into individual extraocular muscles. The eye muscles were innervated by four ipsilateral (lateral rectus, medial rectus, inferior oblique, inferior rectus) and two contralateral (superior rectus, superior oblique) motor neuron pools. The oculomotor nucleus was found in the midbrain, at the level of the caudal zone of the inferior lobe of the hypothalamus. Inferior rectus motor neurons were located rostrally in the oculomotor nucleus, whereas medial rectus, superior rectus, and inferior oblique motor neurons were intermingled in its more caudal portions. All labelled cells were located dorsally and medially to the medial longitudinal fasciculus (MLF) in close proximity to either the floor of the ventricle or the midline region. Occasionally, motor neurons were interspersed within the fiber bundles of the MLF or the exiting fibers of the oculomotor nerve. The trochlear nucleus, containing superior oblique motor neurons, was found in the immediate lateral and caudal neighborhood of the oculomotor nucleus, where its rostral border overlapped with the caudal border of the latter. The abducens nucleus, containing lateral rectus motor neurons, was located in the posterior brainstem in the neighborhood of the vestibular nuclear complex. This nucleus was divided into a rostral and a caudal portion. The axons of ipsilaterally projecting motor neurons headed toward their respective nerve roots via the shortest possible route, as did the axons of superior rectus motor neurons, which crossed the midline without detour to enter the contralateral oculomotor nerve. In contrast, trochlear motor neuron axons arched around the dorsal aspect of the ventricle through the cerebellar commissure to reach the contralateral trochlear nerve. The morphology of individual motor neurons was visualized by intrasomatic injection of HRP. Cell somata had oblong shapes, and their large dendrites were oriented laterally and ventrally. The axons did not collateralize within the midbrain region or the oculomotor nerve as far as they could be traced.(ABSTRACT TRUNCATED AT 400 WORDS)     

Anatomy of physiologically identified eye-movement-related pause neurons in the cat: pontomedullary region

Pause neurons (PNs) are inhibitory neurons close to the midline at the pontomedullary junction that fire tonically and then cease firing just prior to quick eye movements of visual or vestibular origin. Previous physiological evidence has shown that these neurons have a role of central importance in the generation of rapid eye movements in any direction and all major models of ocular motor control incorporate PNs as major elements. In this study in cats, we injected horseradish peroxidase intracellularly into somata or axons of physiologically identified PNs. After appropriate tissue preparation, cell body and axonal reconstructions were performed, with the aid of a camera lucida-equipped microscope. Fifty-three PNs were stained and reconstructed. These consisted of 17 cell bodies and dendrites and 36 axons. Seven of these included both cell bodies and axons. PN somas lay close to the midline in the nucleus raphe pontis and centralis superior, had extensive dendritic arborizations tending to arise from either pole of the elongated soma, and had axons which typically crossed the midline and bifurcated into long branches which extended rostrally and caudally, inferior to the medial longitudinal fasciculus. There were major terminal arborizations and boutons in areas just rostral and caudal to the abducens nucleus in areas where two types of premotor neurons, excitatory and inhibitory burst neurons, are concentrated. Many axosomatic contacts were noted. Other terminal arborizations and boutons were found close to the midline in a region rostral to abducens nucleus containing other neurons known to burst prior to quick eye movements, and in the nucleus reticularis gigantocellularis. Rostral stem axons could be traced to the level of the trochlear nucleus and inferior to the medial longitudinal fasciculus. The caudal stem axons could be traced parallel to the midline and inferior to the medial longitudinal fasciculus and as far caudally as the hypoglossal nucleus.     

Organization of the cerebellum in the pigeon (Columba livia): III. Corticovestibular connections with eye and neck premotor areas.

The connections of the cerebellar cortex with vestibular premotor neurons of the oculomotor and collimotor systems in the pigeon were delineated in experiments using WGA-HRP as an anterograde and retrograde tracer. Putative premotor neuron pools were identified by injections into the oculomotor (mIII) and trochlear nuclei (mIV) and into the most rostral portion of the cervical neck motor nucleus, nucleus supraspinalis (SSp). The retrograde data indicate that ipsilateral projections upon oculomotor neurons arise from the medial portions of the superior (VeS) and tangential (Ta) nuclei. Contralateral projections originate from the infracerebellar nucleus, the interstitial vestibular region including the main (lateral) portion of the tangential nucleus, and from the descending and medial vestibular nuclei (VeD, VeM). These projections were confirmed in anterograde studies that also defined the connections of these vestibular premotor regions with specific subnuclear divisions of the pigeon's "oculomotor" nuclei (mIII, mIV, mVI). The organization of projections from the vestibular nuclei to the pigeon's extraocular motoneurons is similar to that reported in mammals. Projections upon neck premotor neurons arise primarily from neurons in the interstitial region of the vestibular nuclear complex. After injections in SSp, retrogradely labeled neurons were found, contralaterally, in the lateral part of the tangential and superior vestibular nuclei and in the dorsolateral vestibular nucleus (VDL). Ipsilateral labeling was seen in the medial interstitial region (VeM, VeD, and medial Ta). These projections were confirmed in anterograde experiments. With the exception of VDL, vestibular nuclei projecting to neck motoneurons also project to extraocular motoneurons. Thus the infracerebellar nucleus projects exclusively, and the superior vestibular nucleus predominantly, upon oculomotor (mIII, mIV) nuclei; VDL projects predominantly upon the neck motor nucleus, whereas the interstitial vestibular regions (medial Ta, rostral VeD, intermediate VeM) project upon both collimotor and oculomotor neurons. The pattern of retrograde labeling seen in the cerebellar cortex after injections into vestibular premotor nuclei was used to define the projections of specific cerebellar cortical zones upon vestibular eye and neck premotor neurons. Corticovestibular projections upon these regions arise from the auricle and lateral unfoliated cortex, the posterior lobe components of cortical zones B and E, and from the vestibulocerebellum. Each of these cortical zones projects upon components of the vestibular nuclear complex, which are premotor to either oculomotor nuclei or collimotor nuclei. The hodological findings are related to the functional organization of the oculomotor and collimotor systems in the pigeon and compared with the mammalian data.     

Transneuronal transport in the vestibular and auditory systems of the squirrel monkey and the arctic ground squirrel. I. Vestibular system

Transneuronal transport of [3H]proline, [3H]fucose, and [3H]leucine in various combinations from pledgets implanted in the ampulla of a single semicircular duct was studied in the squirrel monkey and arctic ground squirrel after long survival periods. Tritiated amino acids implanted in any single ampulla resulted in labeling of nearly all vestibular and auditory receptors, nearly all cells of the vestibular and spiral ganglia and central transport via nearly all root fibers of both nerves. Primary vestibular fibers were distributed to the vestibular nuclei (VN) and specific parts of the cerebellum in the pattern previously described. Transneuronal transport of [3H]proline by vestibular neurons was present in all known secondary pathways, except those projecting to thalamic nuclei. Observations were similar in both species, except for small differences in commissural vestibular projections. Major commissural transport was to all parts of the opposite medial vestibular nucleus (MVN) and to peripheral parts of the superior vestibular nucleus (SVN), but some transport was present in all contralateral VN, including ventral cell group y. Descending transneuronal transport was evident in vestibulospinal tract (VST) ipsilaterally and in the medial longitudinal fasciculus (MLF) bilaterally. Both [3H]proline and [3]fucose were transported transneuronally to the ipsilateral abducens nucleus (AN); with long survivals [3H]proline was transported peripherally via the ipsilateral abducens nerve root. Ascending transport in the MLF was bilateral, asymmetric and greatest contralaterally. Fibers entered the contralateral MLF near the AN and the lateral wing of the ipsilateral MLF rostral to most of the VN. Terminals in the trochlear nuclei (TN) were bilateral and greatest contralaterally. In the monkey terminals in ipsilateral oculomotor complex (OMC) were distributed uniformly in all subdivisions, except for the medial rectus subdivision (MRS), where terminals were more numerous. The greatest density of terminals was present contralaterally in the superior rectus subdivision (SRS) of the OMC; only sparse terminals were present in the MRS on that side. Transport in the ipsilateral abducens nerve roots in the monkey and the virtual absence of transport to the MRS of the contralateral OMC suggested transneuronal transport to abducens motor neurons, but not to internuclear neurons (AIN). The AIN project only to the MRS of the contralateral OMC and do not appear to receive vestibular input. Comparable observations were made in the AN, TN and OMC of the ground squirrel, although the representation of the extraocular muscles in the OMC is unknown.(ABSTRACT TRUNCATED AT 400 WORDS)     

Monosynaptic activation of long descending propriospinal neurons from the lateral vestibular nucleus and the medial longitudinal fasciculus

In decerebrate cats long descending propriospinal (LDP) neurons were recorded extracellularly in the cervical enlargement. They were identified antidromically by spinal cord stimulation at the L1–L2 level. Inputs to these cells were tested by stimulating the medial longitudinal fasciculus (MLF) 5 to 6 mm rostral to the obex, the lateral vestibular nucleus (LVN), the upper MLF 1 mm caudal to the trochlear nucleus, and the medial vestibular nucleus (MVN), all on the ipsilateral side. Action potentials were elicited in 44% ( ) of LDP neurons in the ventral horn (laminae VII, VIII) at a segmental latency of 1 ms or less following brain stem stimulation. This was considered to be a monosynaptic latency. The most effective stimulation sites were the MLF and the LVN. MLF stimulation accounted for about two-thirds of the monosynaptically elicited action potentials and LVN for about one-third. Another 22% of LDP neurons responded at longer latencies, but some of those responses may also have been monosynaptic. Stimulation of the upper MLF and the MVN were much less effective, indicating that the MLF input was predominantly from fibers originating in the medullary and/or pontine reticular formation.     

Regional differences of brain glucose metabolic compensation after unilateral labyrinthectomy in rats: a [C]2-deoxyglucose study

A unilateral labyrinthectomy was performed on anesthetized adult albino rats. Brain [¹⁴C]2-deoxyglucose (2DG) uptake was measured autoradiographically 3.5 h to 20 days later and compared to sham-operated controls. In the vestibular nuclei (nn.) of labyrinthectomized subjects, large left-right differences of 2DG uptake occurred, which decreased over time. The equalization of vestibular nuclear 2DG uptake paralleled behavioral compensation of body, neck and head postural abnormalities, and known equalization of vestibular nuclear cell firing rates during compensation. There was a small difference of 2DG uptake in medial and lateral vestibular nn. 20 days after lesions when animals had a residual head tilt and tonic eye deviation. In the oculomotor nn., trochlear nn. and interstitial n. of Cajal, large left-right differences of 2DG uptake occurred, which did not change over time. The higher 2DG uptake in these nn. occurred ipsilateral to the labyrinthine lesion and did not correlate with the onset and cessation of nystagmus. The persistent asymmetry did appear to correlate with ipsilateral downward and contralateral upward eye deviation which continued for long periods after the lesion. We hypothesize that the non-compensating metabolic asymmetry in the oculomotor and trochlear nn. could be due to lesioned otolithic input to the vestibular nn. which relays to trochlear and oculomotor nn.     

Morphology and distribution of serotoninergic and oculomotor internuclear neurons in the cat midbrain

Serotoninergic fibers have been reported in both the abducens and facial nuclei of the cat. Furthermore, serotoninergic dorsal raphe and oculomotor internuclear neurons occupy similar locations in the periaqueductal gray overlying the oculomotor and trochlear motor nuclei. To resolve the issue of whether these two populations of neurons overlap, serotoninergic fibers were assayed in the abducens and facial nucleus; then the morphologies and distributions of identified serotoninergic neurons and oculomotor internuclear neurons were determined. Both the abducens and facial nuclei contained varicosities labelled with antibody to serotonin, but a much higher density of immunoreactive fibers was present in the latter, especially in its medial aspect. Distinct synaptic profiles labelled with antibodies to serotonin were observed in both nuclei. In both cases, terminal profiles contained numerous small, predominantly spheroidal, synaptic vesicles as well as a few, large, dense-core vesicles. These profiles made synaptic contacts onto dendritic and, in the facial nucleus, somatic profiles that occasionally displayed asymmetric, postsynaptic, membrane densifications. Following injection of horseradish peroxidase into either the abducens or facial nuclei, double-label immunohistochemical techniques demonstrated that the serotoninergic and oculomotor internuclear neurons form two distinct cell populations. The immunoreactive serotoninergic cells were distributed within the dorsal raphe nucleus, predominantly caudal to the retrogradely labelled oculomotor internuclear neurons. The latter were located in the oculomotor nucleus along its dorsal border and in the adjacent supraoculomotor area. Intracellular injection of horseradish peroxidase revealed that oculomotor internuclear neurons have multipolar somata with up to ten long, tapering dendrites that bifurcate approximately five times. Their dendritic fields were generally contained within the nucleus and adjacent supraoculomotor area. In contrast, putative serotoninergic neurons were often spindle-shaped and exhibited far fewer primary dendrites. Many of these long, narrow, sparsely branched dendrites crossed the midline and extended to the surface of the cerebral aqueduct. In the vicinity of the aqueduct they branched repeatedly to form a dendritic thicket. The axons of the intracellularly stained serotoninergic neurons emerged either from the somata or the end of a process with dendritic morphology, and in some cases they produced axon collaterals within the periaqueductal gray. Thus the oculomotor internuclear and serotoninergic populations differ in both distribution and morphology.(ABSTRACT TRUNCATED AT 400 WORDS)     

Afferents to oculomotor nuclei from area "Y" in Macaca mulatta: an anterograde degeneration study

Electrolytic lesions were placed in the dentate and interpositus nuclei of the monkey M. mulatta and the resulting anterograde degeneration was stained with the Wiitanen or Nauta-Laidlaw techniques. Two of 19 lesions produced preterminal degeneration in the oculomotor nuclei. In both cases the lesions also damaged vestibular area “y” subjacent to the rostral pole of the dentate nucleus. The course and terminal distribution of anterograde degeneration to the oculomotor nuclei was the same in both cases. Degenerating fibers were found in lateral parts of the ipsilateral MLF, and preterminal degeneration was found in the ipsilateral abducens and trochlear nuclei and the dorsal subdivision of the oculomotor nucleus. Degenerating fibers were also traced from the crossed brachium conjunctivum to the contralateral paramedian subdivision of the oculomotor nucleus. These fibers appeared to course in dorsomedial parts of the brachium. Lesions of the dentate and interpositus nuclei which did not damage area “y” produced no anterograde axonal degeneration in the MLF or the oculomotor nerve nuclei. The results are discussed with regard to previous reports of cerebello-oculomotor fibers originating in the dentate and interpositus nuclei. The results suggest that area “y”, rather than the cerebellar nuclei, projects principally to oculomotor neurons that control vertical eye movements.     

Connections and oculomotor projections of the superior vestibular nucleus and cell group ‘y’

Attempts were made to determine brainstem and cerebellar afferent and efferent projections of the superior vestibular nucleus (SVN) and cell group 'y' ('y') in the cat using axoplasmic tracers. Injections of HRP, WGA-HRP and [3H]amino acids were made into SVN and 'y' using two different infratentorial stereotaxic approaches. Controls were provided by unilateral HRP injections involving the oculomotor nuclear complex (OMC), the interstitial nucleus of Cajal (INC) and the deep cerebellar nuclei (DCN). Large injections of SVN almost invariably involved 'y' and dorsal parts of the lateral vestibular nucleus (LVN). Smaller injections involved central and ventral peripheral parts of SVN. Discrete injections of 'y' involved small dorsal parts of LVN. Afferents to SVN are derived mainly from the vestibular nuclei (VN) and parts of the vestibulocerebellum. SVN receives afferents: bilaterally from caudal portions of the medial (MVN) and inferior (IVN) vestibular nuclei and 'y'; contralaterally from ventral and lateral parts of SVN and rostral MVN; and ipsilaterally from the nodulus, uvula and medial parts of the flocculus. Purkinje cells (PC) in medial parts of the flocculus project to central regions of SVN, while PC in the nodulus and uvula appear to project mainly to dorsal peripheral regions of SVN. SVN receives sparse projections from the ipsilateral INC, the contralateral central cervical nucleus (CCN) and virtually no projections from the reticular formation. SVN projects via the medial longitudinal fasciculus (MLF) to the ipsilateral trochlear nucleus (TN), the inferior rectus subdivision of the OMC, the INC, the nucleus of Darkschewitsch (ND) and the rostral interstitial nucleus of the MLF (RiMLF). Contralateral projections of SVN cross in the ventral tegmentum caudal to most of the decussating fibers of the superior cerebellar peduncle and terminate in the dorsal rim of the TN and the superior rectus and inferior oblique subdivisions of the OMC; sparse crossed projections enter the INC and the ND. Cerebellar projections of SVN end as mossy fibers in the ipsilateral nodulus, uvula and in medial parts of the flocculus bilaterally. Retrograde transport from unilateral injections of the OMC indicate that afferents from SVN arise ipsilaterally from central and dorsal regions and contralaterally from dorsal peripheral regions. Ventral cell group 'y' receives small numbers of afferent fibers from caudal central parts of the ipsilateral flocculus. No fibers from ventral 'y' could be traced to other vestibular nuclei, the OMC or the cerebellum.(ABSTRACT TRUNCATED AT 400 WORDS)     

Midsagittal pontomedullary brain stem section: Effects on ocular adduction and nystagmus

Oculomotor function was studied after midsagittal section of the brain stem in rhesus monkeys. After lesions that involved both the medulla and pons, there was permanent paralysis of adduction during conjugate eye movements and divergent strabismus. Analysis of the lesions indicated that activity responsible for ocular adduction had crossed the brain stem in a localized region at the level of the abducens nuclei. The adductive paralysis was probably due to interruption of axons of abducens internuclear neurons that ascend in the medial longitudinal fasciculus (MLF). In view of the functional relationship of this region to ocular adduction and its close anatomic relationship to the MLF, we propose that it be called the MLF decussation. Because the eyes beat synchronously after deep interruption of vestibular commissural fibers, the latter are not essential for the production of quick phases of nystagmus. After medullary lesions, animals had spontaneous downward nystagmus and perverted caloric nystagmus. Optokinetic after-nystagmus was lost. The perverted nystagmus appears due to unmasking of anterior canal responses, secondary to a loss of inhibitory activity that normally crosses the brain stem in the vestibular commissural system.     

Morphology and physiology of abducens motoneurons and internuclear neurons intracellularly injected with horseradish peroxidase in alert squirrel monkeys

Axons of abducens motoneurons and internuclear neurons were penetrated with HRP-filled glass microelectrodes in alert squirrel monkeys. The firing rate of these axons and spontaneous eye movements were recorded and the axons were then injected with HRP for subsequent visualization of the recorded cells. Soma-dendritic and axon and axonal terminal morphology were studied for possible correlation with firing frequency. The physiology of squirrel monkey abducens neurons is qualitatively similar to their counterparts in the rhesus monkey and the cat, being primarily correlated with the position and velocity of the eyes. The locations of moto- and internuclear neurons are similar in the squirrel monkey and cat as are the axonal projections and terminals. However, squirrel monkey abducens cells are smaller than their feline counterparts and have dendrites that are confined to the cellular borders of the abducens nucleus. The size of the soma and proximal dendrites of moto- and internuclear neurons are poorly correlated with either their threshold for recruitment or their tonic eye position sensitivity. However, cells with smaller dendritic trees tended to have higher saccadic eye velocity sensitivity than those with larger trees. Three types of internuclear neurons were distinguishable upon the basis of their axon collaterals. All cells terminated within the medial rectus subdivision of the oculomotor nucleus. One class of cells did not give rise to collaterals before projecting to the oculomotor nucleus and the other classes gave rise to collaterals that terminated in the intermediate and/or caudal interstitial nuclei of the median longitudinal fasciculus. Within the IIIrd nucleus internuclear terminations were usually confined to a single subgroup of medial rectus motoneurons.     

Distribution of the vestibular neurons projecting to the oculomotor and trochlear nuclei in rabbits

Horseradish peroxidase and Fast Blue were injected into the oculomotor and trochlear nuclei of rabbits so as to study the distribution of vestibular neurons that project to these nuclei. After the oculomotor nucleus was injected, labelled neurons were found in the superior, medial, and descending vestibular nuclei as well as in cell group Y. In the superior nucleus, most of the neurons (510 +/- 46) were ipsilateral to the injection, although contralaterally labelled neurons were also observed (104 +/- 19) more peripherally. In cell group Y, 186 +/- 24 contralaterally labelled neurons were observed, whereas hardly any (8 +/- 3) were found on the ipsilateral side. The largest group of labelled neurons (811 +/- 65) constituted a neuronal band located contralaterally in the medial nucleus and rostral part of the descending nucleus. This band rostromedially continued with the caudal part of the group of internuclear neurons of the abducens nucleus. Only 190 +/- 31 neurons were labelled in the medial and descending nucleus ipsilateral to the injected oculomotor nucleus. After injection of the trochlear nucleus, labelled neurons were found in the ipsilateral superior nucleus and contralateral medial and descending nuclei: a few labelled cells were also observed in the ipsilateral medial and descending nuclei as well as in the contralateral cell group Y.     

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.     

Discharge characteristics of axotomized abducens internuclear neurons in the adult cat

The aim of the present work was to characterize the axotomy-induced changes in the discharge properties of central nervous system neurons recorded in the alert behaving animal. The abducens internuclear neurons of the adult cat were the chosen model. The axons of these neurons course through the contralateral medial longitudinal fascicle and contact the medial rectus motoneurons of the oculomotor nucleus. Axotomy was carried out by the unilateral transection of this fascicle (right side) and produced immediate oculomotor deficits, mainly the incapacity of the right eye to adduct across the midline. Extracellular single-unit recording of abducens neurons was carried out simultaneously with eye movements. The main alteration observed in the firing of these axotomized neurons was the overall decrease in firing rate. During eye fixations, the tonic signal was reduced, and, on occasion, a progressive decay in firing rate was observed. On-directed saccades were not accompanied by the high-frequency spike burst typical of controls; instead, there was a moderate increase in firing. Similarly, during the vestibular nystagmus, neurons hardly modulated during both the slow and the fast phases. Linear regression analysis between firing rate and eye movement parameters showed a significant reduction in eye position and velocity sensitivities with respect to controls, during both spontaneous and vestibularly induced eye movements. These firing alterations were observed during the 3 month period of study after lesion, with no sign of recovery. Conversely, abducens motoneurons showed no significant alteration in their firing pattern. Therefore, axotomy produced long-lasting changes in the discharge characteristics of abducens internuclear neurons that presumably reflected the loss of afferent oculomotor signals. These alterations might be due to the absence of trophic influences derived from the target.     

Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey.

Afferent and efferent connections of the fastigial oculomotor region (FOR) were studied in macaque monkeys by using axonal transport of wheat germ agglutinin conjugated horseradish peroxidase (WGA-HRP). When injected HRP is confined to the FOR, retrogradely labeled cells appear in lobules VIc and VII of the ipsilateral vermis and in group b of the contralateral medial accessory olive (MAO). In reference to the maps of topographical organization, the extent of the effective site in the fastigial nucleus (FN) could be assessed from the distributions of labeled Purkinje cells (P cells) in the vermis and labeled olivary neurons in the MAO. In contrast to the unilateral nature of the P-cell and climbing-fiber projections, those from the other brainstem regions to the FOR were bilateral. Following the injection of HRP into the FOR, the largest number of retrogradely labeled cells appeared in the pontine nuclei. Although the number of labeled cells was greater on the contralateral side in both the peduncular and dorsomedial pontine nuclei (DMPN), the number of each side was virtually identical in the dorsolateral pontine nucleus (DLPN). In the nucleus reticularis tegmenti pontis (NRTP), labeled cells were located only in its medial and dorsolateral portions bilaterally. In the vestibular complex, labeled cells appeared in the superior (SVN), medial (MVN), and inferior vestibular nuclei (IVN) bilaterally. The lateral vestibular nucleus (LVN), including y group and the ventrolateral vestibular nucleus, were free of labeled cells. Labeled cells appeared also in the perihypoglossal nucleus (PHN) bilaterally. In the pontine raphe (PR) and paramedian pontine reticular formation (PPRF), labeled cells appeared bilaterally in the caudal third of the area between the oculomotor and abducens nuclei. Labeled cells appeared also in the mesencephalic and medullary reticular formation. Tracing of anterogradely labeled axons demonstrated that most fibers from the FOR decussated within the cerebellum and entered the brainstem via the contralateral uncinate fasciculus. Some crossed fibers ascended with the contralateral brachium conjunctivum and terminated in the midbrain tegmentum. A small contingent of fibers advanced further to the thalamus. In the mesodiencephalic junction, labeled terminals were found contralaterally in the rostral interstitial nucleus of medial longitudinal fasciculus (riMLF) and a medial portion of FOrel's H Field. They appeared also in the central mesencephalic reticular formation (cMRF), the periaqueductal gray (PAG), the posterior commissure nucleus, and the superior colliculus. The oculomotor and trochlear nuclei, the red nucleus, and the interstitial nucleus of Cajal were free of labeled terminals.(ABSTRACT TRUNCATED AT 400 WORDS)     

Cerebellar influences on accessory oculomotor nuclei of the rat: A neuroanatomical,immunohistochemical, and electrophysiological study

With the aim to evaluate a possible neocerebellar control on eye movements, the projections from the cerebellar lateral nucleus (LN) to the accessory oculomotor nuclei (i.e., the nucleus of posterior commissure, the nucleus of Darkschewitsch, and the interstitial nucleus of Cajal), the putative neurotransmitters subserving this pathway, and the nature of the synaptic influences exerted by these projections were studied in adult rats. We used the orthograde transport of horseradish peroxidase conjugated with wheat germ agglutinin (WGA-HRP) to identify the mesencephalic areas where cerebellofugal fibers terminate, and retrograde labeling with the fluorescent dye fluoro-gold to estimate the incidence of cerebellar neurons projecting to the accessory oculomotor nuclei. Orthograde labeling showed that only a small contingent of cerebellofugal fibers reaches the contralateral accessory oculomotor nuclei. The retrogradely labeled cells were located primarily in the small-celled part of LN. By immunohistochemistry, we observed that all the cells retrogradely labeled from the accessory oculomotor area were also stained by using glutamate or aspartate antisera, but none of them were double-stained with a GABA antiserum. Electrical stimulation of the contralateral LN elicited changes in firing rate of a significant fraction of cells belonging to the accessory oculomotor nuclei (36.4% in the nucleus of posterior commissure, 47.1% in the nucleus of Darkschewitsch, and 44.6% in the interstitial nucleus of Cajal). In 57.8% of the cases, the responses were excitations, most of which had latencies and response characteristics compatible with a monosynaptic linkage. The remaining 42.2% of the cases were inhibitions with latencies ranging between 5 and 22 ms. Extracellular field potential recordings within the contralateral accessory oculomotor nuclei were interpreted as arising from impulses propagating along excitatory axons projecting in a bundle from the cerebellum. Stimulation of LN area in rats following intranuclear injection of kainic acid was not capable of evoking short latency excitations, so these responses can be considered to depend on the activation of LN efferents. The LN projection on accessory oculomotor nuclei could be part of the final precise control exerted by the neocerebellum on those brain structures concerned with movements of the eyes. © 1993 Wiley-Liss, Inc.     

Somatomotor connectivity in the midbrain of Rana pipiens

The mesencephalic oculomotor nuclei of Rana pipiens and their surrounding cell groups were investigated using the anterograde and retrograde transport of horseradish peroxidase and Golgi techniques. The cell groups surrounding the oculomotor and trochlear nuclei were divided into the nucleus interstitialis (nInt) groups A, B, and C, the basal optic nucleus, and the nucleus reticularis tegmenti. Afferents to the ventral mesencephalon originate from the retina and from vestibular, cerebellar, visual, and accessory oculomotor nuclei. These afferents produce a sequence of terminal arborizations in which visual afferents are found in the outer neuropil, and accessory oculomotor, vestibular, and cerebellar afferents are found along the inner neuropil and central gray. The oculomotor neurons in anurans have extensive dendritic fields, extending to the outer margins of the neuropils, as do many large cells along the margin of nInt. Other neurons in nInt have dendritic fields restricted to the proximal portions of the neuropil. Efferents from nInt area A project to the cerebellum and bilaterally to the spinal cord. Area B nInt projects to the ipsilateral spinal cord, contralateral nInt, pretectal nucleus lentiformis mesencephali, and ipsilateral trochlear nucleus. Efferents from area C nInt reach the deep tectal layers and ipsilateral spinal cord. The outer portions of the neuropil contain the nucleus of the basal optic root which comprises ganglionic elongate and stellate neurons and projects to the pretectum. In the center of the neuropil peri-nBOR neurons have dendrites directed towards the visual terminal fields and axons towards the central gray and oculomotor neurons. The nucleus reticularis tegmenti receives afferents from the tectum and lateral forebrain bundle and projects to the deep tectal layers. In anurans, the oculomotor neurons receive a variety of visual, somatic, and vestibular afferents and appear relatively undifferentiated, whereas the nInt appears more developed.     

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.