Distribution of vestibular afferents that innervate the sacculus and posterior canal in the gerbil

The central distribution of afferents that innervate the macula of the saccule and the crista of the posterior canal was assessed in the gerbil following the direct injection of horseradish peroxidase (HRP) separately into the sensory neuroepithelia of each peripheral receptor organ. Ganglion cells innervating the posterior canal were located in the caudal part of the inferior ganglion, while those cells innervating the saccule were located in the rostral part of the inferior ganglion, scattered in the superior ganglion, and concentrated at the junction (isthmus) between the two. The paths of the central axons of these two groups of ganglion cells through the vestibular root and their division into ascending or descending pathways were similar. However, the distributions of their terminals were different. The posterior canal projected to medial parts of the vestibular nuclear complex. Terminals were found in the medial and superior vestibular nuclei. The posterior canal also projected to the uvula of the cerebellum. The saccule projected to more lateral-lying brainstem areas. Terminal fields were located in the lateral and descending vestibular nuclei and cell group y. Saccule projections outside the vestibular complex were observed to the lateral cuneate nucleus, the N. gigantocellularis, and the cerebellar cortex. Of the eight areas receiving primary afferent projections from these two organs, only within the medial and descending vestibular nuclei and the cerebellar cortex were overlapping projections observed.     

Central projections of the vestibular nerve: a review and single fiber study in the Mongolian gerbil

The primary purpose of this article is to review the anatomy of central projections of the vestibular nerve in amniotes. We also report primary data regarding the central projections of individual horseradish peroxidase (HRP)-filled afferents innervating the saccular macula, horizontal semicircular canal ampulla, and anterior semicircular canal ampulla of the gerbil.

In total, 52 characterized primary vestibular afferent axons were intraaxonally injected with HRP and traced centrally to terminations. Lateral and anterior canal afferents projected most heavily to the medial and superior vestibular nuclei. Saccular afferents projected strongly to the spinal vestibular nucleus, weakly to other vestibular nuclei, to the interstitial nucleus of the eighth nerve, the cochlear nuclei, the external cuneate nucleus, and nucleus y.

The current findings reinforce the preponderance of literature. The central distribution of vestibular afferents is not homogeneous. We review the distribution of primary afferent terminations described for a variety of mammalian and avian species. The tremendous overlap of the distributions of terminals from the specific vestibular nerve branches with one another and with other sensory inputs provides a rich environment for sensory integration.     

Location of dye-coupled second order and of efferent vestibular neurons labeled from individual semicircular canal or otolith organs in the frog

Vestibular nerve branches innervating the sensory epithelia of the three semicircular canals or of the three otolith organs of frogs were selectively labeled in-vitro with biocytin. Labeled afferent fibers from the semicircular canals, utricle, and lagena were encountered in each of the four vestibular nuclei and their projections overlapped considerably. Saccular afferent fibers projected to the dorsal (acoustic) nuclei and smaller projections to the vestibular nuclei were regionally restricted. Per semicircular canal or otolith organ about equal numbers (11-14) of medium sized vestibular neurons (between 7.5 and 17 microm in diameter) were dye-coupled to afferent fibers. Most of these dye-coupled vestibular neurons were located in the lateral and descending vestibular nuclei between the VIIIth and IXth nerves. The superior vestibular nucleus was relatively free of dye-coupled vestibular neurons. The location of this subpopulation of central vestibular neurons supports the notion that these neurons are part of a particular vestibulospinal pathway. In addition, from each of the canal and/or otolith organs about 3-4 efferent vestibular neurons were labeled retrogradely. These neurons (between 15 and 26 microm in diameter) were located ventral to the vestibular nuclear complex. The branching of efferent vestibular neurons was shown by the presence of neurons that were double labeled by two different fluorescent dyes applied in the same experiment to the anterior and posterior ramus of the same VIIIth nerve, respectively. The branching of these efferent neuron axons explained the presence of collaterals and terminals in the sensory epithelia of a number of untreated ipsilateral endorgans.     

Central vestibular system: vestibular nuclei and posterior cerebellum

The vestibular nuclei and posterior cerebellum are the destination of vestibular primary afferents and the subject of this review. The vestibular nuclei include four major nuclei (medial, descending, superior and lateral). In addition, smaller vestibular nuclei include: Y-group, parasolitary nucleus, and nucleus intercalatus. Each of the major nuclei can be subdivided further based primarily on cytological and immunohistochemical histological criteria or differences in afferent and/or efferent projections. The primary afferent projections of vestibular end organs are distributed to several ipsilateral vestibular nuclei. Vestibular nuclei communicate bilaterally through a commissural system that is predominantly inhibitory. Secondary vestibular neurons also receive convergent sensory information from optokinetic circuitry, central visual system and neck proprioceptive systems. Secondary vestibular neurons cannot distinguish between sources of afferent activity. However, the discharge of secondary vestibular neurons can distinguish between “active” and “passive” movements.

The posterior cerebellum has extensive afferent and efferent connections with vestibular nuclei. Vestibular primary afferents are distributed to the ipsilateral uvula-nodulus as mossy fibers. Vestibular secondary afferents are distributed bilaterally. Climbing fibers to the cerebellum originate from two subnuclei of the contralateral inferior olive; the dorsomedial cell column and β-nucleus. Vestibular climbing fibers carry information only from the vertical semicircular canals and otoliths. They establish a coordinate map, arrayed in sagittal zones on the surface of the uvula-nodulus. Purkinje cells respond to vestibular stimulation with antiphasic modulation of climbing fiber responses (CFRs) and simple spikes (SSs). The modulation of SSs is out of phase with the modulation of vestibular primary afferents. Modulation of SSs persists, even after vestibular primary afferents are destroyed by a unilateral labyrinthectomy, suggesting that an interneuronal network, triggered by CFRs is responsible for SS modulation. The vestibulo-cerebellum, imposes a vestibular coordinate system on postural responses and permits adaptive guidance of movement.     

Spatial distribution of semicircular canal nerve evoked monosynaptic response components in frog vestibular nuclei

Most second-order vestibular neurons receive a canal-specific monosynaptic excitation, although the central projections of semicircular canal afferents overlap extensively. This remarkable canal specificity prompted us to study the spatial organization of evoked field potentials following selective stimulation of individual canal nerves. Electrically evoked responses in the vestibular nuclei were mapped systematically in vitro. Constructed activation maps were superimposed on a cytoarchitectonically defined anatomical map. The spatial activation maps for pre- and postsynaptic response components evoked by stimulation of a given canal nerve were similar. Activation maps for monosynaptic inputs from different canals tended to show a differential distribution of their peak amplitudes, although the overlap was considerable. Anterior vertical canal signals peaked in the superior vestibular nucleus, posterior vertical canal signals peaked in the descending and in the dorsal part of the lateral vestibular nucleus, whereas horizontal canal signals peaked in the descending and in the ventral part of the lateral vestibular nucleus. A similar, differential but overlapping, spatial organization of the canal inputs was described also for other vertebrates, suggesting a crude but rather conservative topographical organization of semicircular canal nerve projections within the vestibular nuclei. Differences in the precision of topological representations between vestibular and other sensory modalities are discussed.     

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.     

Vestibular efferent fibers to ampulla of anterior, lateral and posterior semicircular canals in cats

Origins of vestibular efferent fibers to ampulla of semicircular canals in cats were examined using retrograde transport of horseradish peroxidase. The anterior canal was innervated from bilateral parvocellular reticular nucleus (PCRN), contralateral gigantocellular reticular nucleus and ipsilateral lateral reticular nucleus (LRN); the lateral canal, from ipsilateral PCRN and LRN as well as ipsilateral lateral vestibular nucleus; and the posterior canal, from bilateral PCRN and ipsilateral medial and lateral vestibular nuclei.     

Afferent innervation of the vestibular nuclei in the chinchilla. I. A method for labeling individual vestibular receptors with horseradish peroxidase

A new method was developed for specific labeling of primary vestibular afferent fibers from selected end-organs with horseradish peroxidase (HRP) applied extracellularly in the inner ear space. In 48 chinchillas, labeling was performed successfully in all animals by scratching the surface of the sensory end-organ of interest with an electrolytically sharpened needle and replacing the fluid in the vestibule with 30% HRP solution. Merely replacing the vestibular fluid (endo- and perilymph) with HRP did not label the ganglion cells or the afferent fibers in the brain stem. The specificity of labeling was verified by histological inspection of the ganglion cells and nerve fibers innervating the damaged and intact receptors. When the posterior semicircular canal and saccular receptors were scratched, labeled fibers and ganglion cells were found in the nerve and ganglion rostrodorsally and caudoventrally, respectively. Labeled ganglion cells from different superior vestibular nerve (SVN) receptors did not show as clear a segregation pattern as did labeled receptors from the inferior vestibular nerve (IVN). Once inside the brain stem, labeled fibers from the SVN receptors were rostral to those from the IVN receptors. The fibers of the vestibular root divided into an ascending and a descending branch which formed the vestibular tract. Labeled fibers from the SVN receptors divided rostrolaterally to those from the IVN receptors. In the vestibular tract, fibers coursed in different locations according to the receptor of origin. Fibers from the utriculus were lateral to those from the horizontal semicircular canal, which were lateral to those from the anterior semicircular canal. Fibers from the sacculus were lateral to those from the posterior semicircular canal.     

Organization of eighth nerve afferent projections from individual endorgans of the inner ear in the teleost, Astronotus ocellatus

Eighth nerve fibers from the saccule, utricle, lagena, and the anterior, horizontal, and posterior semicircular canals of a cichlid fish were traced to the octavolateralis region of the brainstem using HRP and degeneration methods. The anterior, magnocellular, descending, and posterior nuclei of the octavus column receive inputs from all endorgans, whereas the tangential nucleus receives projections only from the utricle and semicircular canals. The most rostral projections only from the utricle and semicircular canals. The most rostral projection from each endorgan is found in the eminentia granularis of the vestibulolateral lobe of the cerebellum. Sparse terminals are found in the medial reticular formation from the utricle adn semicircular canals, and utricular and saccular remain terminate in the vicinity of the lateral dendrite of the Mauthner cell. Utricular and semicircular canal projections consistently overlap centrally as do saccular and lagenar inputs. Afferent fibers from all endorgans end within relatively distinct regions throughout the octavus column of nuclei. Saccular and lagenar inputs lie dorsal to the semicircular canal terminations. Utricular endings are complex, however, in that they overlap dorsally with saccular and lagenar terminals and ventrally with the semicircular canal inputs. Cerebellar inputs are found only in the eminentia granularis of the vestibulolateral lobe, and the densest terminals are from the utricle and the semicircular canals; the sparsest are from the saccule. Previous studies in fish have indicated that generally the utricle and semicircular canals are concerned with he maintenance of static and dynamic equilibrium whereas the saccule and lagena are concerned with auditory reception. There is recent evidence, however, for multiple functions within individual endorgans. Our anatomical findings suggest that in Astronotus each otolithic endorgan carries more than one modality; that the semicircular canals are concerned solely with an equilibrium function; and that acoustic information is processed dorsally and vestibular information ventrally along the octavus column of nuclei. No single nucleus appears to be solely auditory in function and only the tangential nucleus, situated ventrally in the octavus column, appears to be solely vestibular.     

Cerebellar, medullary and spinal afferent connections of the paramedian reticular nucleus in the cat

The topographic organization of afferent projections from the deep cerebellar nuclei, medulla oblongata and spinal cord to the paramedian reticular nucleus (PRN) of the cat was studied using the horseradish peroxidase (HRP) method of retrograde labelling. Discrete placements of HRP within each of the dorsal (dPRN) and ventral (vPRN) regions of the PRN showed some segregation of input. The deep cerebellar nuclei project in a predominantly contralateral fashion upon the PRN. A small but significant ipsilateral fastigial afferent component is also present. The fastigial and dentate nuclei contribute the majority of fibers to the dPRN whereas the interposed nucleus provides very little. The vPRN receives a relatively uniform input from all 3 cerebellar nuclei. Both lateral vestibular nuclei contribute the majority of fibers from the vestibular nuclear complex largely from their dorsal division. Additional input arises from bilateral medial and inferior vestibular nuclei. The vPRN receives relatively more fibers from the inferior vestibular nuclei than does the dPRN while inputs from the medial vestibular nuclei are comparably sparse. The PRN receives bilateral projections from the nucleus intercalatus (of Staderini). A significant projection to the contralateral PRN occurs from the ventrolateral subnucleus of the solitary complex and its immediate vicinity. Additional sources of medullary afferent input include the lateral, gigantocellular and magnocellular tegmental fields, the contralateral PRN and the raphe nuclei. Sites of origin of spinal afferents to the dPRN are bilaterally distributed mainly within Rexed's laminae VII and VIII of the cervical cord whereas those to the vPRN are confined largely to the medial portion of the contralateral lamina VI in the C1 segment. A few labelled cells are found in the thoracolumbar cord with those to the vPRN being more caudal. These data provide the neuroanatomical substrate for a better understanding of the functional role of the PRN in mediating cardiovascular responses appropriate to postural changes.     

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)     

Central projections of the utricular nerve in the gerbil

The central projections of primary afferent fibers in the utricular nerve, which convey linear head acceleration signals to neurons in the brainstem and cerebellum, are not completely defined. The purpose of this investigation was twofold: 1) to define the central projections of the gerbil utricular afferents by injecting horseradish peroxidase (HRP) and biotinylated dextran amine (BDA) into the utricular macula; and 2) to investigate the projections of individual utricular afferents by injecting HRP intracellularly into functionally identified utricular neurons. We found that utricular afferents in the gerbil projected to all divisions of the vestibular nuclear complex, except the dorsal lateral vestibular nucleus. In addition, terminals were observed in the interstitial nucleus of the eighth nerve, nucleus Y, external cuneate nucleus, and lobules I, IV, V, IX, and X of the cerebellar vermis. No projections appeared in the flocculus or paraflocculus. Fibers traversed the medial and intermediate cerebellar nuclei, but terminals appeared only occasionally. Individual utricular afferents collateralize extensively, projecting to much of the brainstem area innervated by the whole of the utricular nerve. This study did not produce complete filling of individual afferent collateral projections into the cerebellar cortex.     

Afferent and efferent connections of the vestibulolateral cerebellum of the little skate, Raja erinacea

Horseradish peroxidase and cobaltous lysine tracers are used to determine the afferent and efferent projections of the vestibulolateral cerebellum (VLL) in the little skate, Raja erinacea. The skate VLL has separate divisions, pars medialis and pars lateralis, associated with vestibular and lateralis modalities, respectively. The pars medialis has a typical cerebellar structure with molecular and Purkinje cell layers and granular areas. In addition to known inputs from eighth nerve vestibular fibers and limited mechanosensory lateralis afferents, pars medialis afferents are from the ventral part of the descending octaval nucleus, the lateral funicular nucleus and nucleus of the medial longitudinal fasciculus. The pars lateralis and rostral anterior octaval nucleus may be additional afferent sources. Pars medialis efferents project to ventral descending and anterior octaval nuclei, as mossy fibers to the cerebellar corpus and as parallel fibers in the ventrolateral extreme of the molecular layer in the medial octavolateralis nucleus. The pars lateralis comprises granule and Golgi cells and is subdivided into a dorsal granular ridge (DGR) and lateral granular area (LG) that are the sources of parallel fibers in the molecular layers of the dorsal (electrosensory) and medial (mechanosensory) octavolateralis nuclei. Local injections of tracer reveal a systematic topography of pars lateralis parallel fiber projections and a mossy fiber projection to the corpus. Both DGR and LG receive direct spinal input but afferent sources to DGR and LG are otherwise distinct. While LG is known to receive mechanosensory lateralis afferents and limited eighth nerve fibers, DGR receives no direct cranial nerve input. Additional afferents to LG are predominantly from contralateral LG and the anterior octaval and lateral funicular nuclei. Additional DGR afferents are from three medullary nuclei beneath the cerebellar peduncle, nuclei F and K and paralemniscal nucleus, which also projects directly to the dorsal nucleus. Distinct inputs to DGR and LG suggest different contributions of VLL to medullary processing in electro- and mechanoreception.     

The vestibular complex of the American opossum didelphis virginiana. II. Afferent and efferent connections.

We have demonstrated the connectivity of the opossum's vestibular nuclei using degeneration, autoradiographic and horseradish peroxidase techniques and have found it to be generally comparable to that reported for the cat. Apart from the primary input described in Part I of our study, the cerebellum provides the major source of afferent connections to the vestibular complex. Axons from the cerebellar cortex distribute mainly to vestibular areas which receive no primary afferent projections, e.g., the dorsal part of the lateral vestibular nucleus, the dorsolateral margin of the inferior vestibular nucleus as well as cell groups comparable to "f" and "x." In contrast, fastigial fibers show considerable overlap with primary vestibular input, particularly in the ventral part of the lateral nucleus, the central part of the inferior nucleus and the medial nucleus. Axons of fastigial origin also distribute to the superior vestibular nucleus, to subnuclei "f" and "x" and to the parasolitary region. Although spinal fibers are diffuse within the main vestibular nuclei, they ramify quite densely within subnucleus "x." Most of the spinovestibular projection appears to arise in the cervical spinal cord of the opossum. Ipsilateral connections from the interstitial nucleus of Cajal and surrounding areas end predominantly, but not exclusively, in the medial vestibular nucleus. A crossed midbrain projection has been verified from the red nucleus to cell group "x" and the lateral part of the inferior nucleus, as well as to an area possibly comparable to cell group "z," as described for the cat. In Part I of our study we have shown that the major targets of primary vestibular fibers are the central part of the superior nucleus, a portion of the parabrachial complex possibly comparable to subnucleus "y"," the ventral part of the lateral nucleus and the medial nucleus. All of these primary zones give rise to fibers supplying extraocular nuclei and surrounding areas (present study). The ascending midbrain fibers from the superior nucleus end mainly ipsilaterally, whereas those from the putative subnucleus "y" and the medial vestibular nucleus distribute contralaterally for the most part. Although the dorsal part of the lateral vestibular nucleus has no primary vestibular input, it does receive a major projection from the cerebellar cortex. This same region of the lateral nucleus projects to the spinal cord, but not to extraocular nuclei. The ventral part of the lateral nucleus, and perhaps the medial nucleus, also relay to the spinal cord. Additional projections from all vestibular nuclei to the reticular formation provide indirect routes through which the vestibular nuclei can potentially effect multiple systems, including those innervating the spinal cord. Finally, commissural vestibular connections of the opossum are shown to arise within all four major nuclei.     

Central projections of octavolateralis nerves in the brain of a soniferous damselfish (Abudefduf abdominalis)

Sounds and hydrodynamic stimuli are important cues detected by the octavolateralis system in fishes. The central organization of auditory, mechanosensory, and vestibular projections is known for only a few phylogenetically diverse fishes, and less is known about projections in derived perciforms that use sounds for acoustic communication. We used neuronal labeling to provide a detailed analysis of octavolateralis endorgan projections in a soniferous perciform that does not have accessory morphological structures to enhance hearing. Octavolateralis nerves terminate ipsilaterally within seven medullary octaval nuclei: caudal (CON) and medial (MON) octavolateralis, anterior (AON), descending (DON), magnocellular (MgON), tangential (TON), and posterior (PON) octaval nuclei, and the eminentia granularis (EG). Anterior and posterior lateral line nerves project to the CON and MON, with dense projections to the EG. Semicircular canal nerves project primarily to ventral regions including the TON, ventral DON, intermediate DON (DONi), and MgON. Otolithic, semicircular canal, and anterior lateral line nerves all project to the MgON, which may serve a sensorimotor integration function. The DONi receives primarily segregated projections from all otolithic and semicircular canal nerves, whereas the ventral DON and TON receive principally utricular and semicircular canal afferents. The AON receives dense lateral and ventral projections from the saccule and utricle, and medial and dorsal projections from the lagena. These projection patterns are similar to those reported for non‐sonic perciforms, and indicate the absence of neuroanatomical modifications in first‐order octavolateralis nuclei in species that use acoustic communication. Thus patterns of central projections may be conserved among vocal and non‐vocal perciforms. J. Comp. Neurol. 512:628–650, 2009. © 2008 Wiley‐Liss, Inc.     

Differential projections from the vestibular nuclei to the flocculus and uvula-nodulus in pigeons (Columba livia)

The pigeon vestibulocerebellum is divided into two regions based on the responses of Purkinje cells to optic flow stimuli: the uvula-nodulus responds best to self-translation, and the flocculus responds best to self-rotation. We used retrograde tracing to determine whether the flocculus and uvula-nodulus receive differential mossy fiber input from the vestibular and cerebellar nuclei. From retrograde injections into the both the flocculus and uvula-nodulus, numerous cells were found in the superior vestibular nucleus (VeS), the cerebellovestibular process (pcv), the descending vestibular nucleus (VeD), and the medial vestibular nucleus (VeM). Less labeling was found in the prepositus hypoglossi, the cerebellar nuclei, the dorsolateral vestibular nucleus, and the lateral vestibular nucleus, pars ventralis. In the VeS, the differential input to the flocculus and uvula-nodulus was distinct: cells were localized to the medial and lateral regions, respectively. The same pattern was observed in the VeD, although there was considerable overlap. In the VeM, the majority of cells labeled from the flocculus were in rostral margins on the ipsilateral side, whereas labeling from uvula-nodulus injections was distributed bilaterally throughout the VeM. Finally, from injections in the flocculus but not the uvula-nodulus, moderate labeling was observed in a paramedian area, adjacent to the medial longitudinal fasciculus. In summary, there were clear differences with respect to the projections from the vestibular nuclei to functionally distinct parts of the vestibulocerebellum. Generally speaking, the mossy fibers to the flocculus and uvula-nodulus arise from regions of the vestibular nuclei that receive input from the semicircular canals and otolith organs, respectively.     

Properties of secondary vestibular neurons fired by stimulation of ampullary nerve of the vertical, anterior or posterior, semicircular canals in the cat

Experiments on cats were performed to study the pathway and location of the secondary vestibulo-ocular neurons in response to stimulation of the ampullary nerves of the vertical, anterior or posterior, semicircular canals. Experiments on the medial longitudinal fasciculus transection disclosed that vertical canal-evoked, disynaptic excitation and inhibition were transmitted to the extraocular motoneurons through the contra- and ipsilateral medial longitudinal fasciculus respectively. Secondary vestibular neurons, which receive input from the ampullary nerve of the vertical semicircular canals and send their axons to contralateral medial longitudinal fasciculus, were intermingled in the rostral half of the descending and lateral part of the medial vestibular nuclei. A direct excitatory connection of some of these neurons to the target extraocular motoneurons was confirmed by means of a spike-triggered signal averaging technique. It was also found that neurons activated by antidromic stimulation of ipsilateral medial longitudinal fasciculus were located in the superior vestibular nucleus, some of which made direct inhibitory connections to the target extraocular motoneurons. Both excitatory and inhibitory vestibuloocular neurons made synaptic contact in about half of the impaled target motoneurons.     

Vestibulo-oculomotor connections in an elasmobranch fish,the atlantic stingray,Dasyatis sabina

In elasmobranch fishes, including the Atlantic stingray, the medial rectus muscle is innervated by the contralateral oculomotor nucleus. This is different from most vertebrates, in which the medial rectus is innervated by the ipsilateral oculomotor nucleus. This observation led to the prediction that the excitatory vestibulo-extraocular motoneuron projections connecting each semicircular canal to the appropriate muscle should use a contralateral projection from the vestibular nuclei to the motoneurons. This hypothesis was examined in the Atlantic stingray by injecting horseradish peroxidase unilaterally into the oculomotor nucleus. It was found that vestibulo-oculomotor projections arise from the ipsilateral anterior octaval nucleus and the contralateral descending octaval nucleus. The same pattern was observed when the trochlear nucleus was involved in the injection. There were no cells labeled in the region of the abducens nucleus, and no candidate for a nucleus prepositus hypoglossus was identified. The presence of compensatory eye movements, the directional sensitivity of the semicircular canals, the location of the motoneurons innervating each eye muscle, and our results indicate that the excitatory input to the extraocular motoneurons is derived from the contralateral descending octaval nucleus, and the inhibitory input is derived from the ipsilateral anterior octaval nucleus. The absence of both abducens internuclear interneurons and a nucleus prepositus hypoglossus suggests that eye movements, particularly those in the horizontal plane, are controlled differently in elasmobranchs than in other vertebrates examined to date. © 1994 Wiley-Liss, Inc.     

Otolith fibers and terminals in chick vestibular nuclei

The distribution of gravity-sensing, otolith afferent fibers and terminals was studied in the vestibular nuclei of 4-5-day hatchling chicks by using single and double labeling of fibers and terminals with biocytin conjugated to Alexa Fluor and confocal imaging. The vestibular nuclei are represented in a series of five transverse sections of the brainstem immunolabeled with MAP2. Saccular fibers entered the medulla posterior to and at the level of the posterior tangential vestibular nucleus and coursed through ventral parts, producing ascending and descending branches. Small saccular terminals contacted a few dendrites in the tangential nucleus. In contrast, small saccular terminals contacted many dendrites and a few neuron cell bodies in the ventrolateral vestibular nucleus, vestibulocerebellar nucleus, and descending vestibular nuclei. Utricular fibers coursed through ventral parts of the central tangential nucleus before bifurcating into ascending and descending branches. In the tangential nucleus, utricular fibers formed a few large axosomatic terminals (spoon terminals) and a few small terminals on dendrites. In addition, small utricular terminals contacted numerous dendrites and a few neuron cell bodies in the ventrolateral, vestibulocerebellar, and descending vestibular nuclei. Thus, there was negligible overlap in the distribution of the otolith nerves, although each otolith afferent shared common regions with the canal afferents, previously shown, suggesting that some second-order vestibular neurons process convergent inputs from otolith and canal afferents. Taken together with previous results, the present findings identify discrete regions of the chick vestibular nuclei where second-order vestibular neurons likely process directly convergent otolith and canal inputs.     

Octavolateral projections and organization in the medulla of a teleost fish, the sleeper goby (Dormitator latifrons)

This study is the first to employ simultaneous labeling with different colored fluorescent dyes and confocal microscopy to investigate the central projections of the octavolateral nerves in any fish. Three-dimensional reconstructions of the hindbrain octavolateral nuclei were made and overlap of octavolateral projections was assessed in a teleost, the sleeper goby (Dormitator latifrons). The octavolateral nerves, which innervate the otolithic organs, semicircular canals, and lateral lines, project to seven hindbrain nuclei in diverse, complex patterns. The medulla is generally organized with auditory regions dorsal to vestibular regions. The intermediate subdivision of the descending octaval nucleus (DON) receives interdigitating projections from the otolithic organs, and the dorsomedial DON likely integrates multiple auditory inputs. Afferents from the three otolithic organs (the utricle, saccule, and lagena) project to the intermediate DON in approximately equal proportion, supporting physiological evidence that suggests auditory roles for all three otolithic organs in the sleeper goby. The anterior octaval nucleus receives partially segregated inputs from the octavolateral organs. The dorsal division of the magnocellular octaval nucleus (MgON) receives highly overlapping otolithic organ and semicircular canal input, and we propose that this region is a major octaval integration center. Regions in the ventral medulla (the tangential octaval nucleus, ventral DON, and ventral MgON) receive mainly utricular and semicircular canal inputs, suggesting vestibular roles. Each semicircular canal nerve projects to distinct regions of the hindbrain, with little overlap in most octaval nuclei. Efferent neurons receive bilateral input and project unilaterally to the octavolateral organs.