The intrinsic organization of the vestibular complex: evidence for internuclear connevtivity

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 (spv) 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.     

Afferent projection from reticular nuclei, inferior olive and cerebellum to lateral vestibular nucleus of the cat as demonstrated by horseradish peroxidase

Afferent connection to lateral vestibular nucleus (LVN) was examined using retrograde transport of horseradish peroxidase (HRP). When HRP was microiontophoretically applied to the immediate vicinity of the LVN neuron, which monosynaptically fired spike upon VIIIth cranial nerve stimulation, HRP-labelled cells were observed in the ipsilateral lateral reticular nucleus, bilateral gigantocellular nucleus, and contralateral dorsal cap and beta-nucleus of inferior olive in addition to various parts of cerebellum.     

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.     

Neuronal activity in the vestibular nuclei after trigeminal stimulation

The activity of 131 vestibular neurons was investigated in 40 guinea pigs during trigeminal stimulation. The influence of trigeminal sensory information was tested by means of electrical stimulation of the trunk of the trigeminal nerve and with nonnociceptive cutaneous stimulation of facial areas. The spontaneous activity of vestibular neurons was modified by trigeminal electrical stimulation with an increase or decrease of the discharge rate. Some units underwent rhythmic modulation. Forty-one percent of recorded units responded also to cutaneous trigeminal stimulation. An analysis of vestibular action potentials evoked by trigeminal stimulation revealed latency values from 1.2 to 6.2 ms. The anatomic-functional relationship between the trigeminal and the vestibular systems is discussed in light of the reported results.     

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

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

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

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

Ascending and descending internuclear projections within the trigeminal sensory nuclear complex

The cells of origin of ascending and descending internuclear pathways in the trigeminal sensory nuclear complex were studied by the method of retrograde transport of horseradish peroxidase in the cat. The cells of origin of the ascending internuclear pathways are distributed in all laminae of the caudal part of the spinal trigeminal nucleus (Vc) except for lamina II and the caudal regions of the pars interpolaris of the spinal trigeminal nucleus (Vi). The cells arising from the Vc project to all rostral trigeminal nuclei except the caudal Vi and dorsal part of the principal trigeminal nucleus (Vpd), and neurons of the caudal Vi project to the dorsomedial (Vo.dm) and rostrodorsomedial (Vo.r) divisions of the spinal trigeminal nucleus and the ventral part of the principal trigeminal nucleus (Vpv), although the main ascending fibers from the Vc arise from laminae III-V and project to the rostral Vi and pars oralis. By contrast, the cells of origin of the descending internuclear pathways are distributed in all trigeminal nuclei, with chain-like connections between the neighboring nuclei, while the caudal regions of the Vi and laminae I-II do not receive any descending projections. The main ascending fibers from the paratrigeminal nucleus (or interstitial nucleus) at the caudal level of the Vi project to the parabrachial nucleus. These findings indicate that the internuclear pathways are differentially organized between the ascending and descending projections, and suggest that the internuclear trigeminal connections have a smaller influence on the trigeminothalamic tract cells in the Vpd, caudal Vi, and lamina I.     

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.     

A reciprocal axonal connection between the subthalamic nucleus and the neostriatum in the cat

Injections of wheatgerm agglutinin conjugated to horseradish peroxidase (WGA-HRP) into several small regions of the head and body of the caudate nucleus and the putamen of the cat result in retrograde cell-labeling of neurons in the ipsilateral subthalamic nucleus. A mediolateral but no rostrocaudal or dorsoventral topography is apparent in the subthalamostriatal projection. Anterograde transport of WGA-HRP and autoradiography after [³H]amino acid injection of the caudate suggest also a reciprocal striatosubthalamic projection.     

Monosynaptic vestibular nerve input to vestibular and adjacent reticular neurons projecting into the ascending medial longitudinal fasciculus.

This electrophysiological study provides evidence that cat neurons both within and ventral to the cytoarchitectural boundary of the vestibular nuclei project into the region of the contralateral ascending medial longitudinal fasciculus. Many of these neurons, including the more ventral ones, receive monosynaptic input from the vestibular nerve. The vestibular complex thus appears to include part of what traditionally has been called reticular formation.     

Location of commissural neurons in the vestibular nuclei of the cat

Commissural neurons were studied in 14 cats by examining the contralateral location of neurons labeled 24 h after the injection of horseradish peroxidase into the vestibular nuclei. After establishing the distribution of labeled cells in a group of seven animals, the changes in this pattern were examined when the retrograde flow of tracer was impeded by midline transection in a second group of seven cats. These results indicated that commissural units were located mainly in the superior and medial vestibular nuclei. The Group Y nucleus also represents a connecting link to the contralateral brain stem, and a moderate number of commissural neurons were found in the descending vestibular nucleus.     

Direct retinal projections to the lateroposterior and pulvinar nuclear complex (LP-Pul) in the cat, as revealed by the anterograde HRP method.

Retinal projections to the lateroposterior and pulvinar nuclear complex (LP-Pul) in the cat were studied using anterograde horseradish peroxidase (HRP) tracing. After injecting HRP into the vitreous cavity of one eye, HRP-labeled presumed axon terminals were found in the LP-Pul bilaterally, with a contralateral predominance. The areas of distribution of these terminals were seen as a thin sheet at the lateral extreme of the LP-Pul, and as a few small spots within the LP-Pul, especially in the regions along the dorsomedial border of the caudal part of the LP-Pul.     

Different distributions of large and small retinal ganglion cells in the cat after HRP injections of single layers of the lateral geniculate body and the superior colliculus

Retinal ganglion cells were labeled with HRP after injecting layers of GL or single strata within the stratum griseum superficiale (SGS). Only small cells were labeled after injecting small cell C layers and upper SGS. Only large cells were labeled after injecting lower SGS. Small and large cells were labeled after injecting medial interlaminar nucleus (MIN) and layers A and A₁.     

Cerebellar projections to the lateral posterior-pulvinar thalamic complex in the cat

Quantitative autoradiographic analysis of opiate receptor binding using [3H]naloxone shows higher levels in the sexually dimorphic region of the medial preoptic area in female rats than in males. Opiate receptor density varies across the estrous cycle being densest in diestrous females. The sexually dimorphic nucleus of the preoptic area lies within the opiate receptor-rich region. Endogenous opiates in the medial preoptic region acting at opiate receptors which are of differential density in males and females could influence sex-specific behavior mediated by the region.     

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.     

The location of the preganglionic neurons that innervate the submandibular gland of the cat. A horseradish peroxidase study

Horseradish peroxidase was injected under pressure in the main excretory duct of the submandibular gland of cats, to locate the perikarya of the preganglionic parasympathetic salivatory neurons in the brainstem. Labeled multipolar neurons were found ipsilaterally in the lateral reticular formation, where they extended from the rostral plane that contains the genu of the facial nerve to the caudal plane that contains the rostral pole of the dorsal motor nucleus of the vagus nerve.     

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.     

A study of the origin of brain stem projections to monkey spinal cord using the retrograde transport method.

We identified brain stem neurons projecting to cervical and lumbar levels of the spinal cord in young rhesus monkeys using the retrograde transport method. The somatotopic organizations of the red nucleus and lateral vestibular nucleus were clarified. In addition, the presence of bulbospinal neurons in the medial vestibular nucleus; the nucleus of the tractus solitarius; the medial and lateral reticular formations; the raphe nuclei magnus, obscurus, and pallidus; the hypothalamus; and the nuclei of the locus ceruleus and subceruleus was confirmed.     

The Eta ganglion cell type of cat retina.

We define a morphologic type of ganglion cell in cat retina by using intracellular staining in vitro. The eta cell has a small soma, slender axon, and delicate, highly branched dendritic arbor. Dendritic fields are intermediate in size among cat ganglion cells, with diameters typically two to three times those of beta cells. Fields increase in size as a function of distance from the area centralis, ranging in diameter from 90 microm to 200 microm centrally to a maximum of 600 microm in the periphery. This increase is unusually radially symmetric. By contrast with other cat ganglion cell types, eta cells do not have markedly smaller dendritic fields within the visual streak than above or below it nor much smaller fields nasally than temporally. Dendrites ramify broadly throughout sublamina a (OFF sublayer) of the inner plexiform layer. They arborize most densely in S2, where they costratify with dendrites of OFF alpha cells. There is apparently no matching ON variety of eta cell. Experiments combining retrograde labeling with intracellular staining indicate that eta cells project to the superior colliculus and to two components of the dorsal lateral geniculate nucleus (the C laminae and medial interlaminar nucleus). Eta cells apparently project contralaterally from the nasal retina and ipsilaterally from the temporal retina. The morphology and projection patterns of the eta cell suggest that its physiologic counterpart is a type of sluggish or W-cell with an OFF center, an ON surround, and possibly a transient light response.