Deiters' Nucleus. Its Role in Cerebellar Ideogenesis : The Ferdinando Rossi Memorial Lecture.

Otto Deiters (1834-1863) was a promising neuroscientist who, like Ferdinando Rossi, died too young. His notes and drawings were posthumously published by Max Schultze in the book "Untersuchungen über Gehirn und Rückenmark." The book is well-known for his dissections of nerve cells, showing the presence of multiple dendrites and a single axon. Deiters also made beautiful drawings of microscopical sections through the spinal cord and the brain stem, the latter showing the lateral vestibular nucleus which received his name. This nucleus, however, should be considered as a cerebellar nucleus because it receives Purkinje cell axons from the vermal B zone in its dorsal portion. Afferents from the labyrinth occur in its ventral part. The nucleus gives rise to the lateral vestibulospinal tract. The cerebellar B module of which Deiters' nucleus is the target nucleus was used in many innovative studies of the cerebellum on the zonal organization of the olivocerebellar projection, its somatotopical organization, its microzones, and its role in posture and movement that are the subject of this review.

Mapping of neural pathways that influence diaphragm activity and project to the lumbar spinal cord in cats.

During breathing, the diaphragm and abdominal muscles contract out of phase. However, during other behaviors (including vomiting, postural adjustments, and locomotion) simultaneous contractions are required of the diaphragm and other muscle groups including abdominal muscles. Recent studies in cats using transneuronal tracing techniques showed that in addition to neurons in the respiratory groups, cells in the inferior and lateral vestibular nuclei (VN) and medial pontomedullary reticular formation (MRF) influence diaphragm activity. The goal of the present study was to determine whether neurons in these regions have collateralized projections to both diaphragm motoneurons and the lumbar spinal cord. For this purpose, the transneuronal tracer rabies virus was injected into the diaphragm, and the monosynaptic retrograde tracer Fluoro-Gold (FG) was injected into the Th13-L1 spinal segments. A large fraction of MRF and VN neurons (median of 72 and 91%, respectively) that were infected by rabies virus were dual-labeled by FG. These data show that many MRF and VN neurons that influence diaphragm activity also have a projection to the lumbar spinal cord and thus likely are involved in coordinating behaviors that require synchronized contractions of the diaphragm and other muscle groups.

Input/output properties of the lateral vestibular nucleus.

This article is a review of work in three species, squirrel monkey, cat, and rat studying the inputs and outputs from the lateral vestibular nucleus (LVN). Different electrophysiological shock paradigms were used to determine the synaptic inputs derived from thick to thin diameter vestibular nerve afferents. Angular and linear mechanical stimulations were used to activate and study the combined and individual contribution of inner ear organs and neck afferents. The spatio-temporal properties of LVN neurons in the decerebrated rat were studied in response to dynamic acceleration inputs using sinusoidal linear translation in the horizontal head plane. Outputs were evaluated using antidromic identification techniques and identified LVN neurons were intracellularly injected with biocytin and their morphology studied.

Ascending and descending projections of the lateral vestibular nucleus in the rat.

The tracer neurobiotin was injected into the lateral vestibular nucleus in rat and the efferent fiber connections of the nucleus were studied. The labeled fibers reached the diencephalon rostrally and the sacral segments of the spinal cord caudally. In the diencephalon, the ventral posteromedial and the gustatory nuclei received the most numerous labeled fibers. In the mesencephalon, the inferior colliculus, the interstitial nucleus of Cajal, the nucleus of Darkschewitch, the periaqueductal gray matter and the red nucleus received large numbers of labeled fibers. In the rhombencephalon, commissural and internuclear connections originated from the lateral vestibular nucleus to all other vestibular nuclei. The medioventral (motor) part of the reticular formation was richly supplied, whereas fewer fibers were seen in the lateral (vegetative) part. In the spinal cord, the descending fibers were densely packed in the anterior funiculus and in the ventral part of the lateral funiculus. Collaterals invaded the entire gray matter from lamina IX up to lamina III; the fibers and terminals were most numerous in laminae VII and VIII. Collateral projections were rich in the cervical and lumbosacral segments, whereas they were relatively poor in the thoracic segments of the spinal cord. It was concluded that the fiber projection in the rostral direction was primarily aimed at sensory-motor centers; in the rhombencephalon and spinal cord, fibers projected onto structures subserving various motor functions.

Ascending and descending projections of the lateral vestibular nucleus in the frog Rana esculenta.

The lectin Phaseolus vulgaris leucoagglutinin was injected into the frog lateral vestibular nucleus (LVN) to study its antero- and retrograde projections. The following new observations were made. 1) In the diencephalon, vestibular efferents innervate the thalamus in a manner similar to that of mammalian species. The projections show a preference for the anterior, central, and ventromedial thalamic nuclei. 2) In the mesencephalon, vestibular fibers terminate in the tegmental nuclei and the nucleus of medial longitudinal fascicle. 3) In the rhombencephalon, commissural and internuclear projections interconnect the vestibular nuclei. Some of the termination areas in the reticular formation can be homologized with the mammalian inferior olive and the nucleus prepositus hypoglossi. Another part of the vestibuloreticular projection may transmit vestibular impulses toward the vegetative centers of the brainstem. A relatively weak projection is detected in the spinal nucleus of the trigeminal nerve, dorsal column nuclei, and nucleus of the solitary tract. 4) In the spinal cord, vestibular terminals are most numerous in the ipsilateral ventral horn and in the triangular area of the dorsal horn. 5) The coincidence of retrogradely labeled cells with vestibular receptive areas suggests reciprocal interconnections between these structures and the LVN. 6) In seven places, the LVN projections overlap the receptive areas of proprioceptive fibers, suggesting a convergence of sensory modalities involved in the sense of balance.

Abducens internuclear and ascending tract of Deiters inputs to medial rectus motoneurons in the cat oculomotor nucleus: neurotransmitters.

The abducens internuclear and ascending tract of Deiters (ATD) pathways are the principal excitatory inputs to medial rectus motoneurons in the oculomotor nucleus and are related to the control of conjugate horizontal eye movements. Differences in the morphology and soma-dendritic distribution of abducens internuclear and ATD synaptic endings are correlated with known differences in the physiological properties of these independent inputs. The present study extends these observations to the ultrastructural localization of the excitatory amino acid neurotransmitters, glutamate and aspartate, using a postembedding immunogold procedure combined with the pre-embedding immunoperoxidase localization of anterogradely transported biocytin from the abducens nucleus and the ventral lateral vestibular nucleus. Consistent with their spheroidal synaptic vesicle content and the asymmetric pre/postsynaptic membrane profile, both the abducens internuclear and ATD synaptic endings are labeled with glutamate and aspartate. However, quantitative analysis of the density of colloidal gold particles associated with mitochondria versus synaptic vesicles/axoplasmic matrix reveals significant differences in the metabolic versus neurotransmitter pools of the amino acids in the two populations of synaptic endings. The findings indicate that both aspartate and glutamate, possibly co-localized, are the excitatory neurotransmitters utilized by abducens internuclear synaptic endings whose burst-tonic physiological activity conveys information related to eye position to medial rectus motoneurons. By contrast, glutamate is the excitatory neurotransmitter associated with ATD synaptic endings whose high frequency burst activity is related to head velocity.

Organization of afferent projections to the ventral and dorsal regions of the cat lateral vestibular nucleus: an HRP study.

Topical organization of afferent projections to Deiters' nucleus originating from cortical, subcortical, brainstem, and spinal cord structures has been revealed in the cat by microiontophoretic injection of horseradish peroxidase (HRP) into the ventral (NVLV) and dorsal (NVLD) regions of the nucleus and subsequent study of retrograde axonal transport of the enzyme. Differences between afferent inputs to the ventral and dorsal parts of the nucleus, considered as representative of the forelimb and hindlimb regions of the structure, have been observed. The trajectories of labeled fiber systems of the nucleus mentioned have been described. Computer reconstruction of the cat lateral vestibular nucleus (NVL) according the contours drawn from frontal sections of the brain has been carried out.

Cerebello-vestibular connections of the anterior vermis. A retrograde tracer study in different mammals including primates.

Purkinje cells were retrogradely labelled from large injections of wheatgerm-coupled horseradish peroxidase in the vestibular nuclei, including Deiters' nucleus. The labelled Purkinje cells were located in two parallel strips in the anterior vermis; the medial strip is located within the A-zone, the lateral strip corresponds to the B-zone. In the ventral part of the anterior lobe the two strips fuse into a single band, in the dorsal part of the anterior lobe they are separated by a wedge-shaped area, corresponding to the X-zone. The B-zone proceeds in the simple lobule, where it deviates laterally and where it terminates at the centre of the ansoparamedian lobule. Identical zonal patterns were observed in cat, rabbit, rat and monkey. The demarcation of the anterior vermis by the lateral border of the B-zone, and the differences in the projection of the A and B-zone are briefly discussed.

Brainstem projection of the vestibular nerve in the guinea pig: an HRP (horseradish peroxidase) and WGA-HRP (wheat germ agglutinin-HRP) study.

We explored the course and termination of primary vestibular afferent fibers within the brainstem of the guinea pig by means of anterograde axonal transport of horseradish peroxidase (HRP) and wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP). Primary vestibular afferent fibers distribute within the entire vestibular nuclear complex, with the exception of the dorsal part of the lateral vestibular nucleus. The superior vestibular nucleus is characterized by the concentration of terminals within its central part. Although terminal labeling is weaker within the periphery, no area completely lacks primary input. The lateral vestibular nucleus can be divided into a ventral and a dorsal part; within the ventral part small and giant cells receive primary afferent fibers, whereas no significant terminal labeling occurs in the dorsal part. The medial vestibular nucleus shows the most uniform labeling, although the lateral part of its rostral third has a few more terminals than the medial half. Primary projection to the descending vestibular nucleus is widespread, although in its rostrodorsal part it is less impressive. Of the small cell groups commonly associated with the vestibular nuclear complex, only group y receives abundant primary input. Whereas group z completely lacks labeled fibers as well as terminals, single primary axons can be observed passing groups x and f. However, no terminals can be found within the borders of these two cell groups. Scanty projections can be detected within the prepositus hypoglossi nucleus, as well as within the external cuneate nucleus, the cochlear nucleus, the abducent nucleus, and parts of the reticular formation.

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.

Synaptic connections of horizontal canal mediated ascending Deiters tract axons on medial rectus motoneurons in cat.

This study demonstrates the termination of ascending tract of Deiters' (ATD) axons on ipsilateral medial rectus (MR) motoneurons. Horseradish peroxidase (HRP) was iontophoretically injected into ATD axons which were recorded in the MR motoneuron pool of the oculomotor nucleus. MR motoneuron cell bodies were identified by retrograde transport of HRP injected into MR muscles in the orbit. ATD axons were identified by Type I responses to horizontal rotation, monosynaptic responses on stimulation of the ipsilateral labyrinth, and no response on contralateral labyrinth or contralateral abducens nucleus or on ipsilateral MR nerve stimulation. Light microscopic examination showed the main stem axons to be lateral to the medial longitudinal fasciculus, and terminal boutons were in contact with ipsilateral identified MR motoneurons (Furuya and Markham: Exp. Brain Res. 43: 289-303, 1981). Light microscopy and semi-thin sections showed boutons of ATD in contact with identified MR motoneuron cell bodies and proximal dendrites. The electron micrographs (EM) showed the HRP-injected ATD axons have synapses on MR motoneurons. ATD boutons made axosomatic and axodendritic synapses on MR motoneurons. The boutons contained numerous spheroidal synaptic vesicles. Several examples showed clear asymmetrical post-synaptic membrane specialization. This confirms the synaptic connection between horizontal canal activated elements in the ATD and MR motoneurons.

The intrinsic organization of the vestibular complex: evidence for internuclear connectivity.

The HRP anterograde and retrograde labeling techniques provide evidence for extensive internuclear connectivity within the vestibular complex. Specifically: (1) the superior vestibular nucleus is topographically and reciprocally related to the spinal (spr) and medial vestibular nuclei (mv); (2) the lateral vestibular nucleus (lv) is reciprocally related to the mv, and (3) the lv receives afferent fibers from the spv but does not reciprocate this input.

The vestibulothalamic pathway: contribution of the ascending tract of Deiters.

Axoplasmic transport techniques were used to determine the contribution of the ascending tract of Deiters (ATD) to the vestibulothalamic projection in cats. Large injections of HRP into the thalamus centered on the border region between the ventrobasal complex and the caudal ventrolateral nucleus resulted in bilateral retrograde labeling of cells in the vestibular nuclear complex and the nucleus prepositus hypoglossi (PH). Similar thalamic injections were also made in animals with extensive bilateral lesions of the medial longitudinal fasciculus (MLF) and the brachium conjunctivum (BC). HRP-positive neurons in these cases were localized principally to the ventral lateral vestibular nucleus and adjacent superior vestibular nucleus ipsilateral to the thalamic injection, evidence that vestibulothalamic neurons in these nuclei may project to the thalamus over the unlesioned ATD. Injections of [35S]methionine into the rostral vestibular nuclear complex in animals with MLF and BC lesions confirmed these findings, demonstrating orthograde transport of radiolabel in the ATD with termination in thalamus. These experiments document a contribution of the ATD to the ipsilateral vestibulothalamic projection; other sources of the vestibulothalamic pathway (PH, Y group) likely travel through projection systems destroyed in the lesions made in the present study.

The vestibular nuclei in the domestic hen (Gallus domesticus): VI. Afferents from the cerebellum.

Following horseradish peroxidase (HRP) injections in the superior, in the Deiters', in the medial, and in the descending vestibular nuclei in the hen, labeled cells are found in lateral longitudinal zones in the ipsilateral cerebellar cortex, most numerously in the anterior lobe, the nodulus, the uvula, and the auricle. Furthermore, labeled cells are found bilaterally in the ventral parts of the medial and intermediate cerebellar nuclei. Lesions in the cerebellar cortex of the anterior lobe and in anterior parts of the posterior lobe result in terminal degeneration, mainly in the nucleus Deiters dorsalis, but also scantily, in peripheral regions of the superior nucleus, the nucleus Deiters ventralis, the ventrolateral part of the medial nucleus and, mainly medially, in the descending nucleus. Lesions in the posterior part of the uvula, in the nodulus, and in the auricle result in much denser degeneration, most heavily affecting the nucleus Deiters dorsalis, but also affecting peripheral regions of the superior nucleus, the nucleus Deiters ventralis, the entire descending and medial nuclei, and the tangential nucleus. Lesions in the medial cerebellar nucleus result in degeneration bilaterally in the vestibular complex, most heavily affecting the nucleus Deiters ventralis and cell group B, but also affecting peripheral regions of the superior nucleus, the medial nucleus- mainly in dorsomedial regions, lateral and caudal parts of the descending nucleus and, very scantily, in the nucleus Deiters dorsalis. The findings are discussed in the light of the data concerning the organization of the cerebellovestibular projections in mammals and the known connections of the vestibular nuclei in birds.

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

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. Axon ascended in ATD to the oculomotor nucleus and terminated in MR motoneuron areas bilaterally and in 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.

Vestibular projections to the monkey thalamus: an autoradiographic study.

Vestibulothalamic projections were studied in the monkey (macaca mulatta) by injecting anerograde trace substances (radioactive leucine and proline) into the vestibular nuclear complex. Terminal labelling was found bilaterally mainly in the nucleus ventroposterior lateralis pars oralis (VPLo) and to a lesser extent in the nucleus ventroposterior inferior (VPI) and nucleus ventralis lateralis pars caudalis (VLc). The labelling was sparse, and scattered over wide areas. The vestibular origin of this projection was confirmed by injecting retrograde tracer substances (horseradish peroxidase and 125I wheat germ agglutinin) into VPLo. In the autoradiographic study no labelling was found in the posterior group.