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)     

Connections of the superior vestibular nucleus with the oculomotor and red nuclei in the rat: an electron microscopic study

Phaseolus vulgaris leucoagglutinin (PHA-L) was injected into the individual vestibular nuclei of the rat to study their efferent connections. One of the major differences between the connections of these nuclei was found at the level of the mesencephalon: the eye-moving cranial nerve nuclei received the densest projection from the superior vestibular nucleus (SVN). In the present electron microscopic study, we have found that terminals of SVN origin established symmetric synaptic contacts in the oculomotor nucleus. More than two-thirds of PHA-L-labeled boutons terminated on dendrites, the rest of them established axosomatic contacts. Most of the labeled terminals were GABA-positive, supporting the results of previous physiological experiments, which showed inhibitory effects. In the mesencephalon, the other termination area was found in the red nucleus. The PHA-L-labeled boutons of SVN origin were in close contact with the perikarya and proximal dendrites of the magnocellular part of the red nucleus. The types of synaptic contacts and distribution of terminals of SVN origin were similar to those found in the oculomotor nucleus. Our results indicate that the SVN can modify the activity of the cerebellorubral and corticorubral pathways, exerting inhibitory action on the neurons of the red nucleus.     

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)     

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.     

Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey

Attempts were made to determine the afferent and efferent connections of the medial (MVN), inferior (IVN) and lateral (LVN) vestibular nuclei (VN) in the cat and monkey using retrograde and anterograde axoplasmic transport technics. Injections of HRP and [3H]amino acids were made selectively into MVN, IVN and LVN and into: (1) MVN and IVN, (2) LVN and IVN and (3) all 4 VN. Contralateral afferents to MVN arise from (1) the nuclei prepositus (NPP) and intercalatus (NIC), (2) all parts of MVN and cell group 'y' and (3) parts of the superior vestibular nucleus (SVN), IVN and the fastigial nucleus (FN). Ipsilateral projections to MVN arise from: (1) a central band of the flocculus and the nodulus and uvula, (2) the interstitial nucleus of Cajal (INC), and (3) visceral nuclei of the oculomotor nuclear complex (OMC). Efferent projections of MVN are to: (1) the ipsilateral supraspinal nucleus (SSN), and (2) the contralateral central cervical nucleus (CCN), MVN, SVN, cell group 'y', the rostroventral region of LVN, the trochlear nucleus (TN) and the INC. Projections to the abducens nuclei (AN) and the OMC are bilateral. Some ascending fibers in the cat cross within the OMC. In the monkey fibers from MVN end in a central band of the ipsilateral flocculus. Afferents to IVN arise ipsilaterally from SVN, the nodulus, the uvula and the anterior lobe vermis. Contralateral afferents arise from: (1) parts of CCN, MVN, SVN, IVN and cell group 'y' and (2) the central third of the FN. IVN receives bilateral projections from the perihypoglossal nuclei (PH) and the visceral nuclei of the OMC. Efferents from IVN project: (1) ipsilaterally to nucleus beta of the inferior olive, (2) contralaterally to parts of MVN, SVN and cell group 'y' and (3) bilaterally to the paramedian reticular nuclei. No commissural fibers interconnect cell groups 'f' and 'x'. Ascending fibers from IVN terminate contralaterally in the TN and the OMC. In the monkey fibers from IVN terminate in the ipsilateral nodulus, uvula and anterior lobe vermis; no fibers project to FN in either the cat or the monkey. Afferents to the LVN arise primarily from the ipsilateral anterior lobe vermis and bilaterally from rostral parts of the FN. No commissural fibers interconnect the LVN. Projections of the LVN are primarily to spinal cord via the vestibulospinal tract (VST); collaterals of the VST terminate in the lateral reticular nucleus (LRN). Ascending uncrossed projections from LVN in the cat terminate in the medial rectus subdivision of the OMC.(ABSTRACT TRUNCATED AT 400 WORDS)     

Evidence for glycine as an inhibitory neurotransmitter of vestibular, reticular, and prepositus hypoglossi neurons that project to the cat abducens nucleus

The localization and distribution of brain-stem afferent neurons to the cat abducens nucleus has been examined by high-affinity uptake and retrograde transport of 3H-glycine. Injections of 3H-glycine selectively labeled (by autoradiography) only neurons located predominantly in the ipsilateral medial vestibular and contralateral prepositus hypoglossi nuclei, and in the contralateral dorsomedial reticular formation, the latter corresponding to the location of inhibitory burst neurons. The specificity of uptake and retrograde transport of 3H-glycine was indicated by the absence of labeling of the dorsomedial medullary reticular neurons ipsilateral and in close proximity to the injection site, where local uptake by diffusion could have occurred. The selectivity of uptake and transport was demonstrated by the absence of retrograde labeling following injections of 3H-GABA or 3H-leucine into the abducens nucleus. The immunohistochemical localization of glycine and GABA revealed a differential distribution of the 2 inhibitory neurotransmitter candidates in the extraocular motor nuclei. Glycine-immunoreactive staining of synaptic endings in the abducens nucleus was dense with a widespread soma-dendritic distribution but was sparse in the trochlear and oculomotor nuclei. By contrast, GABA-immunoreactive staining within the oculomotor and trochlear nuclei was associated with synaptic endings that were particularly prominent on the somata of motoneurons. GABA-immunoreactive staining in the abducens nucleus, however, was sparse. These differences between glycine- and GABA-immunoreactive staining in the extraocular motor nuclei were correlated with differences in the immunoreactivity of axons in the descending (glycine) and ascending (GABA) limbs of the medial longitudinal fasciculus. Glycine-immunoreactive neurons, furthermore, were observed in the same locations as neurons that were labeled autoradiographically by retrograde transport of 3H-glycine from the abducens nucleus. Electrophysiological recordings from abducens motoneurons and internuclear neurons revealed a marked reduction in the slow positivity of the orthodromic extracellular potential elicited by ipsilateral vestibular nerve stimulation following systemic administration of strychnine, an antagonist of glycine. Intracellular recordings demonstrated that the vestibular-evoked disynaptic inhibitory postsynaptic potentials in abducens neurons were effectively blocked by strychnine but were unaffected by picrotoxin, an antagonist of GABA.(ABSTRACT TRUNCATED AT 400 WORDS)     

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)     

The vestibulothalamic connections in the rat: A morphological analysis using wheat germ agglutinin-horseradish peroxidase

The vestibulothalamic connections were studied in the rat using wheat germ agglutinin-horseradish peroxidase (WGA-HRP). The distributions of anterograde labelling of fibers and terminals in the brainstem and the thalamus were analyzed by injecting WGA-HRP into the superior (SVN) and lateral (LVN) vestibular nuclei, and the medial (MVN) and inferior (IVN) vestibular nuclei. The distributions of retrograde labelling of cells were analyzed in the vestibular nuclear complex by injecting WGA-HRP into the thalamus centered in the central lateral nucleus (CL), ventral posterolateral nucleus (VPL), and rostral part of the dorsal medial geniculate nucleus (rMGd). The vestibular projection to the CL via the medial longitudinal fasciculus (MLF) and the ascending tract of Deiters (ATD) originates mainly in the contralateral MVN and ipsilateral SVN. The vestibular projections to the VPL and the ventral lateral nucleus (VL) via MLF, ATD and superior cerebellar peduncle (SCP) originate mainly in the MVN and SVN, bilaterally. The projection to the rMGd via the lateral lemniscus-inferior collicular brachium, and MLF (and SCP) originates in the contralateral IVN.     

Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflexes of the squirrel monkey

The morphology of 35 vestibular neurons whose firing rate was related to vertical eye movements was studied by injection of horseradish peroxidase intracellularly into physiologically identified vestibular axons in alert squirrel monkeys. The intracellularly injected cells were readily classified into four main groups. One group of cells, down position-vestibular-pause neurons (down PVPs; N = 12), increased their firing rate during downward eye positions, paused during saccades, and were located in the medial vestibular nucleus (MV) and the adjacent ventrolateral vestibular nucleus (VLV). They had axons that crossed the midline and ascended in the medial longitudinal fasciculus (MLF) to terminate in the trochlear nucleus, the lateral aspect of the caudal oculomotor nucleus, and the dorsal aspect of the rostral oculomotor nucleus. A second group of cells (N = 15) were also located in the MV and VLV, but increased their firing rate during upward eye positions, and paused during saccades. These cells had axons that crossed the midline and ascended in the contralateral MLF to terminate in the medial aspect of the oculomotor nucleus. A third group of cells (N = 4) were located in the superior vestibular nucleus, generated bursts of spikes during upward saccades, and increased their tonic firing rate during upward eye positions. These cells had axons that ascended laterally to the ipsilateral MLF to terminate in regions of the trochlear and oculomotor nuclei similar to those in which down PVPs terminated. A fourth group of cells (N = 4), located in the VLV, had axons that projected to the spinal cord, although they had firing rates that were significantly correlated with vertical eye position. Electrical stimulation of the vestibular nerve evoked spikes at monosynaptic latencies in each of the above classes of cells, six of which were injected with horseradish peroxidase. Each group of cells had collateral projections to other areas of the brainstem. Some of the neurons that projected to the contralateral trochlear and oculomotor nuclei had collaterals that crossed the midline to terminate in the oculomotor nucleus ipsilateral to the soma, and some gave rise to small collaterals that terminated in the abducens nucleus. Other areas of the brainstem that received collateral inputs from neurons projecting to oculomotor and trochlear nuclei included the interstitial nucleus of Cajal, the caudal part of the dorsal raphe nucleus, the nucleus raphe obscurus, Roller's nucleus, the intermediate and caudal interstitial nuclei of the MLF, and the nucleus prepositus.     

Commissural and ipsilateral internuclear connection of vestibular nuclear complex of the cat

Commissural and ipsilateral intrinsic connections of the vestibular nuclear complex of cats were investigated using retrograde transport of horseradish peroxidase (HRP). HRP was microiontophoretically injected into limited areas (0.2-0.5 mm in diameter) of the respective vestibular nuclei. In the commissural connections, major fibers were observed between the bilateral superior vestibular nuclei (SVN) and between the bilateral descending vestibular nuclei (DVN); a moderate number of fibers was found from the medial vestibular nucleus (MVN) to the contralateral MVN, SVN and lateral vestibular nucleus (LVN) and from the DVN to the contralateral LVN. Minor commissural connections were detected between the bilateral LVN. The ipsilateral internuclear connections of the vestibular nuclear complex were: (1) from the LVN, MVN and DVN to the SVN, (2) from the MVN and DVN to the LVN and (3) from the MVN to the DVN. Minor ipsilateral intrinsic connections were found from the SVN to the MVN.     

Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey

Attempts were made to determine the central projections of ganglion cells innervating individual semicircular ducts in the monkey by implanting or injecting tritiated amino acids (leucine and/or proline), or horseradish peroxidase (HRP), selectively into a single ampulla. Central transport via the vestibular ganglion in animals receiving isotope implants or injections fell into three categories: (1) transport from ganglion cells innervating all receptive elements of the labyrinth, (2) transport from ganglion cells innervating the three semicircular ducts, and (3) transport from cells of the inferior vestibular ganglion innervating the posterior semicircular duct. Transneuronal transport of isotope was observed in secondary vestibular fibers in animals where proline was used and survival exceeded 12 days. Transneuronal labeling of secondary auditory fibers was independent of the [³H]amino acid used, and occurred with survivals of 10 or more days. HRP implanted into the ampulla of the lateral semicircular duct in several animals produced retrograde transport to efferent vestibular and cochlear neurons, but did not result in transganglionic labeling of primary vestibular or auditory fibers.Primary vestibular fibers terminate throughout the superior (SVN) and medial vestibular nuclei (MVN). Within SVN, terminals are most pronounced in its central large-celled portion, but extend into peripheral parts of the nucleus, except for a small medial area near its junction with the oral pole of MVN. Primary projections to MVN are homogenously distributed throughout the nucleus excepting a small circular area of sparse terminals along its ventral margin. Primary vestibular afferents terminate mainly in rostral and caudal portions of the inferior vestibular nucleus (IVN), but do not reach cell group ‘f’. Projections to the lateral vestibular nucleus (LVN) are restricted to its ventral part. Primary projections to the accessory vestibular nuclei reach the interstitial nucleus of the vestibular nerve (NIVN) and cell group ‘y’. Fibers project beyond the vestibular nuclei (VN) to terminate ipsilaterally in the accessory cuneate nucleus (ACN), the subtrigeminal lateral reticular nucleus (SLRN), and well-defined portions of the reticular formation (RF). Projections to SVN and MVN are derived primarily from ganglion cells innervating the semicircular ducts, while projections to caudal IVN, cell group ‘y’ and ACN are related mainly to macular portions of the vestibular ganglion. NIVN receives both macular and duct afferents. Posterior duct afferents terminate in medial portions of SVN, in rostrolateral portions of MVN, and in rostral IVN.Transneuronal transport of isotope increases the volume of terminal label in the ipsilateral VN, but not in dorsal LVN, or cell groups ‘f’ or ‘x’. The quality of transneuronal transport in secondary vestibular fibers is dependent upon: (1) survival time, (2) proximity to the VN, and (3) the excitatory or inhibitory nature of the projection.Primary vestibulocerebellar fibers terminate heavily in the ipsilateral nodulus and ventral uvula. Lesser projections reach the flocculus, deep folia of vermal lobules V and VI, and the lingula. Primary vestibulocerebellar projections terminate as mossy fiber rosettes in the granular layer of these cortical areas. No primary vestibular fibers terminate in the primate fastigial nuclei.     

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.     

Projections of the vestibular and cerebellar nuclei in Rana pipiens

The efferent projections and cytoarchitecture of the vestibulocerebellar region were examined to determine the nuclear boundaries and potential homologies. The anterior portion of the vestibular complex projects to the ipsilateral oculomotor and trochlear nuclei and is the major source of commissural fibers. Neurons in the rostromedial portions of the complex project to the contralateral trochlear nucleus. Large neurons in the ventrolateral portion of the complex give rise to a bilateral vestibulospinal pathway. Medium-sized neurons in the neuropil and small neurons in the central gray giving rise to bilateral projections to the spinal cord and oculomotor nuclei as well as commissural and ipsilateral cerebellar efferents. Projections from the nucleus of the cerebellum reach the contralateral spinal cord and cerebellar nucleus and there is also a bilateral projection to the ventral rhombencephalic and mesencephalic basal plates. The medial portion of the nucleus gives rise to commissural, ipsilateral mesencephalic and contralateral spinal projections. The lateral portion of the nucleus projects to the contralateral ventral mesencephalon. On the whole, the results of this investigation substantiate the division of the anuran vestibular complex in anurans into nuclei which may be homologous to the superior nucleus and nucleus of Deiters in mammals. The case for distinct descending and medial nuclei is less compelling. Further, it appears possible to divide the nucleus of the cerebellum into medial and lateral components whose connectivity is similar to that of reptiles and to a lesser extent mammals.     

Regional differences of brain glucose metabolic compensation after unilateral labyrinthectomy in rats: a [14C]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.     

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.     

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.     

The vestibular nuclei in the domestic hen (Gallus domesticus) III. Ascending projections to the mesencephalic eye motor nuclei

Following injections of horseradish peroxidase in the oculomotor and the trochlear nuclei in the hen, the occurrence of labeled cells was plotted in the vestibular nuclei. The majority of labeled cells was localized in the superior, the medial, and the tangential nucleus. Within the superior nucleus the cells were found mainly caudally, extending medially and ventrally in central areas. In the medial nucleus labeled cells were localized exclusively in its rostral half, mainly in ventrolateral regions. Most, if not all, cells in the nucleus tangentialis project rostrally. In addition, rostrally projecting vestibular cells were found in the cell group A and the rostrolateral part of the descending nucleus. The projection to the oculomotor nuclear complex is from the superior nucleus and the cell group A bilateral but chiefly ipsilateral, from the medial nucleus bilateral, from the tangential nucleus and the rostral pole of the descending nucleus chiefly contralateral. Massive labeling was found in the abducens nucleus, somewhat less in the reticular formation, mainly in the lateral regions of the medial part at the level of the abducens and facial nuclei. Labeled cells were, in addition, found in the deep layers of the optic tectum, and scattered cells in the nucleus raphe. The findings are discussed in the light of what is known of the organization of the vestibular nuclei in the hen and the rostral projection of the vestibular nuclei in mammals.     

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.     

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.     

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.