Ascending and Descending Projections of the Lateral Vestibular Nucleus in the Rat*

Home , Nucleus prepositus, Vestibular cortex

Acta Biologica Hungarica 53 (1–2), pp. 7–21 (2002)

ASCENDING AND DESCENDING PROJECTIONS OF THE LATERAL VESTIBULAR NUCLEUS IN THE RAT*

TIMEA BÁCSKAI, G. SZÉKELY, CLARA MATESZ**

Department of Anatomy, Histology and Embryology, University of Debrecen, Medical and Health Science Center, Nagyerdei krt. 98, H-4012 Debrecen, Hungary

(Received: September 10, 2001; accepted: November 17, 2001)

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.

Keywords: Lateral vestibular nucleus – rat – neurobiotin labeling

INTRODUCTION

Primary afferent fibers originating in the vestibular sense organs terminate on second-order vestibular neurons of the superior (SVN), medial (MVN), lateral or Deiters (LVN) and descending (DVN) vestibular nuclei. Numerous experiments have been performed to study the ascending and descending fiber connections, which con- vey the most versatile functions of these nuclei, but unfortunately the different functions of the individual nuclei, depending on their different fiber connections, are known to only a limited extent. There is general agreement that the most rostral terminals of secondary vestibular fibers are found in different thalamic nuclei. The lateral nuclear group [6, 21, 38, 41],

*Dedicated to Professor József Hámori on the occasion of his 70th birthday. **Corresponding author; e-mail: [email protected]

0236-5383/2002/$ 5.00 © 2002 Akadémiai Kiadó, Budapest 8 TIMEA BÁCSKAI et al. the medial geniculate body [18, 33] and the intralaminar nuclei [11, 18] are the main targets of ascending secondary vestibular fibers. These thalamic nuclei relay vestibular information to wide areas of the prosencephalon, including the motor cortex [16], the limbic system [3, 42], the insula [2], the striatum [18], the auditory cortex [32] and above all the vestibular cortex in the posterior part of the superior temporal gyrus [14]. With these radiations, the vestibular system contributes greatly to the organization of various motor functions. Vestibular inputs to the hippocampus are presumed to generate important cues in orientation in space [39]. In the brainstem region, fiber connections to the mesencephalic tectal and tegmental nuclei are well known in a variety of experimental animals [10, 40], as are the pre- cise interconnections with cranial motor nuclei innervating the external eye muscles [25]. In addition to these, there are extensive connections between vestibular nuclei on either side of the rhombencephalon [9, 13]. The commissural pathways are thought to be of special importance in mediating the neural mechanisms for vestibular compensation, which can be experienced at various times following hemi- labyrinthectomy in different animal species. Despite much work along this line, it is still not clear which of these commissural interactions have specific roles in the com- pensatory mechanisms, and few data are available on intrinsic synaptic connections that can be demonstrated between neurons of the same nucleus in some species [9, 13]. The vestibulo-hippocampal projection is suggested to be an important factor in the mechanism of vestibular compensation [44]. As the vestibular nuclei are virtually embedded into the rhombencephalic reticular formation (RF), many collaterals and direct fiber terminals are found in various parts of this structure [43]. The contributions of the individual nuclei to the RF are not known; nevertheless, vestibular afferents can be shown to terminate in the dorsal vagal nucleus and in the nucleus of the solitary tract [4]. It has been suggested that movements and cardiorespiratory activity are coordinated by a linkage between the control mechanisms of somatomotor and visceromotor activities. The somatic sensory signals required in this regulation are in part conveyed through the vestibular system, indicating the body position in space. Various vestibular inputs to the RF may be the source of dizziness and vomiting reflexes. Unfortunately, the anatomy and physiology of vestibulo-autonomic interactions have not been fully explored. There is a substantial descending projection from the vestibular nuclei onto different parts of the spinal cord [5]. At variance with the classical description that vestibulospinal fibers and the medial longitudinal fascicle travel in the anterior funiculus of the spinal cord, we have located descending fibers in the lateral and dorsal funiculi as well [26, 27]. Another classical thesis that spinal vestibular fibers originate in the LVN was contradicted by the multiple origin of the descending tracts in our experiments. In view of the general situation that very few studies made a point as to the nuclear origin of the different vestibular projections, we have decided to start a series of investigations on the fiber connections of individual vestibular nuclei. In an earlier work we described the projections of the LVN in the frog [19]. In the present paper we give an account of the fiber connections of the LVN in the rat, using the tracer dye neurobiotin.

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MATERIALS AND METHODS

The experiments were performed on 9 adult Wistar rats, in accordance with state reg- ulations and with the approval of the University Animal Care Committee. Under ure- thane anesthesia, the head of the animal was fixed in a stereotactic holder, and the cranial cavity and subsequently the dura mater were opened. A glass micropipette with a tip diameter of 10–15 μm was filled with neurobiotin and introduced into the rostral part of the LVN according to the coordinates of Paxinos and Watson [35]. A positive direct current of 5 μA was used for the injection, with a pulse duration of 7 s, followed by 3–5 s intervals for a period of 15–20 min. After a survival period of 8–14 days, the animals were perfused transcardially with isotonic saline for 2–3 min, followed by a fixative containing 1.25% glutaraldahyde and 2% paraformaldahyde in 0.1M phosphate buffer (pH 7.4). The diencephalon, the brainstem and the spinal cord were removed and fixed by immersion in the same fixative overnight at 4 °C. The blocks of tissue were then washed in 0.1M phosphate buffer, and sections of 60 μm were made with a vibrotome. For the histochemical detection of neurobiotin, the sections were incubated in avidin-biotin-peroxidase complex for 90 min at room temperature and the reaction was visualized with DAB. The sections were mounted on glass slides coated with gelatine, counterstained with 1% toluidine blue, air-dried and coverslipped. Labeled boutons and fibers were drawn through a camera lucida from three con- secutive sections. The photographs were taken with a Nikon microscope.

RESULTS

The neurobiotin injection was restricted to the rostral part of the LVN, 1.2 mm caudally to the interaural line (Fig. 3A). Three animals in which the injection spread into the surrounding structures were excluded from the analysis. Labeled fibers were followed bilaterally in the rostral and the caudal directions from the level of the diencephalon rostrally and as far as the lumbosacral spinal cord caudally.

Rostral projections Diencephalon

Labeled fibers reach the diencephalon by way of the medial longitudinal fascicle (MLF). The fascicle loosens up at the mesencephalic and diencephalic border and the fibers spread predominantly to the caudal one-third of the thalamus (Fig. 2A). The densest termination area is seen in the ventral posteromedial (VPM) (Figs 1A and 2A) and in the gustatory nuclei. Terminals are less numerous in the parafascicular nucleus and in the nucleus of Forel. In the subthalamus, the ventral and dorsal sub-

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Fig. 1. Microphotographs of labeled terminals in the ventral posteromedial nucleus of the thalamus (A) and in the magnocellular part of the red nucleus (B). Bar: 100 μm divisions of the zona incerta are evenly supplied by the fibers of LVN origin. The medial geniculate body and the pretectal nucleus receive vestibular fibers on both sides.

Mesencephalon

The projection of the LVN is equally strong on both sides at this level (Fig. 2B). The inferior colliculus is invaded by appreciable numbers of labeled fibers, probably by more numerous fibers on the side contralateral to than on the side ipsilateral to the injection. A few fibers can also be found in the superior colliculus. The periaqueductal gray matter (PAG) is richly supplied on both sides. A strong projection is detected within the interstitial nucleus of Cajal and the nucleus of Darkschewitch, but the oculomotor and trochlear nuclei receive relatively few fibers. Labeled fibers can be seen all over the mesencephalic RF. The nucleus of MLF, the deep mesencephalic nucleus and the ventral tegmental area can be discerned as receiving substantial numbers of vestibular fibers. It is interesting that both the magnocellular and parvocellular parts of the red nucleus are richly supplied by fibers of LVN origin (Figs 1B and 2B).

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Fig. 2. Camera lucida reconstruction of the fibers and terminals of lateral vestibular nucleus origin at the level of the diencephalon (A) and mesencephalon (B). The asterisk indicates the side of injection. The distance of the section from the interaural line is shown in the lower right corner. 3: motor nucleus of oculomotor nerve; 3rd: third ventricle; APT: anterior pretectal nucleus; Cp: cerebral peduncle; DK: nucleus of Darkschewitsch; DpMe: deep mesencephalic nucleus; F: fields of Forel; Gu: gustatory thalamic nucleus; IC: interstitial nucleus of Cajal; PAG: periaqueductal gray mater, PF: parafascicular thalamic nucleus; RMC: red nucleus, magnocellular part; RPC: red nucleus, parvocellular part; SC: superior colliculus; SN: substantia nigra; VPL: ventral posterolatar thalamic nucleus; VPM: ventral posteromedial thalamic nucleus; VTA: ventral tegmental area; ZID: zona incerta, dorsal part; ZIV: zona incerta, ventral part

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Fig. 3. (A) Cross-section of the brainstem, showing the location of neurobiotin injection into the lateral vestibular nucleus (encircled area) at a distance of –1.80 mm from the interaural line. DC: dorsal cochlear nucleus; MVN: medial vestibular nucleus; SVN: superior vestibular nucleus. (B, C) neurobiotin-labeled terminals in the ipsilateral (B) and contralateral (C) lateral vestibular nucleus. Bar: 100 μm

Pons

Since the vestibular nuclei are situated at this level, the fibers of LVN origin can be followed in different directions from the site of injection. The majority of them remain within the confines of the ipsilateral vestibular nuclear complex and termi-

Acta Biologica Hungarica 53, 2002 Projections of lateral vestibular nucleus in the rat 13 nate in the SVN, the MVN, the DVN and the caudal part of the LVN (Fig. 4A). Similar densities of labeled fibers and terminals can be observed in each nucleus. These fibers represent the intrinsic or internuclear connections of the vestibular nuclear complex (Fig. 3B). Another contingent of labeled fibers proceeds toward the dorsal aspect of the pons, crosses the midline and continues in the direction of the contralateral vestibular nuclear complex (Fig. 3C). This projection represents the

Fig. 4. Camera lucida reconstruction of the fibers and terminals of lateral vestibular nucleus origin at the level of the pons (A) and the medulla oblongata (B). The distance of the section from the interaural line is shown in the lower right corner. The asterisk indicates the side of injection. 6, 7: motor nucleus of the abducens (6) and facial (7) nerve; 7n: root of the facial nerve; DC: dorsal cochlear nucleus; DPGi: dorsal paragigantocellular nucleus; DVN: descending vestibular nucleus; g7: genu of facial nerve; OI: inferior olive; LVN: lateral vestibular nucleus; MVN: medial vestibular nucleus; NA: nucleus ambiguus; nspV: spinal nucleus of trigeminal nerve; tspV: spinal tract of trigeminal nerve; PGi: paragigantocellular nucleus; PHy: nucleus prepositus hypoglossi; Py: pyramidal tract; NTS: nucleus of solitary tract; SVN: superior vestibular nucleus; VC: ventral cochlear nucleus; VGi: ventral gigantocellular nucleus

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Fig. 5. (A) Cross-section of the lower cervical spinal cord, indicating the neurobiotin-labeled terminals in the ventral horn. The broken line indicates the border of white and gray matter. (B, C) Labeled terminals in the ipsilateral (B) and contralateral (C) paragigantocellular nucleus of the reticular formation following neurobiotin injection into the lateral vestibular nucleus. Bar: 100 μm

Acta Biologica Hungarica 53, 2002 Projections of lateral vestibular nucleus in the rat 15 commissural connections of the LVN. A small proportion of the LVN fibers take a ventral course and terminate within the spinal nucleus of the trigeminal nerve. This vestibulo-trigeminal connection is the strongest in the mandibular division of the subnucleus oralis; its maxillary and ophthalmic divisions receive only a few fibers and terminals. A large number of fibers of LVN origin converge on the bilateral MLF, and emit collaterals to different structures. A small proportion of these collaterals terminate in the abducens nucleus on both sides, and a few fibers enter the motor nucleus of the facial nerve. The majority of the collaterals terminate in the dorsal part of the pontine reticular formation (RF). The dorsal paragigantocellular nucleus and the parvocellular reticular nucleus are distinguished by a rich supply of vestibular fibers with an ipsilateral dominance (Figs 4A and 5A, B).

Caudal projections Medulla oblongata

The nuclei of the dorsal and ventral areas of the RF, the dorsal paragigantocellular nucleus and the ventral gigantocellular nucleus contain fibers of LVN origin (Fig. 4B). Preterminal fibers and terminals form a rich network in the ventral part of the medulla oblongata and in the inferior olive, mainly ipsilateral to the side of injection. Other structures of the medulla oblongata that receive vestibular fibers are the nucleus of the prepositus hypoglossi, the nucleus of the solitary tract, and the gracile and cuneate nuclei. The subnucleus interpolaris and caudalis of the spinal nucleus of the trigeminal nerve are only weakly supplied by fibers of LVN origin.

Spinal cord

Descending fibers travel bilaterally in all funiculi of the spinal cord, but the majority of them are found in the ipsilateral anterior funiculus. At the upper (Fig. 6A) and lower (Fig. 5C) cervical levels, most of the terminals are distributed ipsilaterally in Rexed laminae V, VII, VIII and IX; a few of them also occur in laminae III and IV. The central cervical nucleus receives fibers mainly on the ipsilateral side. A few terminals are seen bilaterally in both ventral horns of the thoracic segments. The lumbar part of the spinal cord (Fig. 6B) contains a very rich projection. The ipsilateral ventral horn, and laminae VII and VIII are abundantly supplied by labeled fibers. The distribution of the descending fibers, although they are smaller in number, is similar on the contralateral side. A few fibers and terminals can be detected in laminae V and VI. A similar termination pattern is found in the upper sacral segments of the spinal cord (Fig. 7); terminals are occasionally found in laminae II and IV at this caudal level.

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Fig. 6. Camera lucida reconstruction of the fibers and terminals of lateral vestibular nucleus origin at the level of the cervical (A) and lumbar (B) parts of the spinal cord. The Arabic numerals indicate the level of sections. The dotted lines show the borders of Rexed laminae. The asterisk indicates the side of injection. CCN: central cervical nucleus

Fig. 7. Camera lucida reconstruction of the fibers and terminals of lateral vestibular nucleus origin at the level of the second sacral segment of the spinal cord. The dotted lines label the borders of Rexed laminae. The asterisk indicates the side of injection

Acta Biologica Hungarica 53, 2002 Projections of lateral vestibular nucleus in the rat 17

DISCUSSION

With the neurobiotin labeling technique, we have studied the efferent fiber connections of the LVN. The literature contains a large body of data on the fiber connections of the vestibular system, but the projections of individual nuclei have been investigated with a histological technique only sporadically [34]. Apart from our previous study on the frog [19], this is the first paper which gives an account of efferent connections of the LVN alone in a mammal. Due to its reciprocal connections with the cerebellum, this nucleus occupies a unique place among the vestibular nuclei, and this nucleus was regarded as the output port of the vestibular system toward the spinal cord. The present results demonstrate that the LVN sends fibers as far as the diencephalon rostrally, and the sacral spinal cord caudally. The diencephalic fibers show a preference for the posterior one-third of the thalamus. The densest termination area was found in the VPM. This is in agreement with the previous finding of an investigation of the projection from more than one vestibular nucleus: the posteroventral nuclei are involved in areas receiving vestibular input [38]. The main afferent pathways, the medial lemniscus and the spinothalamic tract, are known to terminate in these thalamic sites. With vestibular fibers in these nuclei, the VPM and VPL may be regarded as an integrating center of somatic and vestibular inputs that are indispensable to adjust and maintain the posture of the body. In this context, it may be interesting to refer to the presence of LVN terminals in the dorsal column nuclei and in the dorsal horn of the spinal cord, the sites of origin of somatic inputs to the posteroventral nuclei of the thalamus. The moderate amount of LVN termination in some parts of the ventrobasal complex may be interpreted in a similar manner. This area receives vestibular fibers from the DVN [38], and physiological experiments indicate proprioceptive inputs to the ventral thalamic nuclei from muscles and joints in monkeys [7]. The presence of LVN fibers in the parafascicular nucleus and in the nucleus of Forel is interesting from the aspect that these areas may be homologized to the cen- tromedian nucleus in primates [16]. This nucleus receives multiple sensory-motor information, and the LVN appears to contribute to these inputs. Furthermore, the cen- tromedian nucleus relays striatal connections [15], and the parafascicular projection of the LVN may represent the origin of a vestibulo-thalamostriatal projection. Dopaminergic receptors in the striatum are assumed to be involved in the vestibular compensation in rats [12]. The presence of LVN fibers in the red nucleus is interesting in this context; this connection may point to the importance of impulses arising in the LVN in the mechanism of vestibular compensation. A large number of LVN fibers were found in the zona incerta. This area receives multiple afferent inputs from the spinal trigeminal nucleus, the dorsal column nuclei and the deep cerebellar nuclei, and is presumed to play a role in the production of ori- enting movements [17]. Vestibular input may certainly contribute to the processing of these complex activities. It is not easy to find a functional interpretation for the rich vestibular termination in the gustatory nucleus, unless this area is regarded as part of the nonspecific nuclei of the thalamus, which relays vestibular inputs to the

Acta Biologica Hungarica 53, 2002 18 TIMEA BÁCSKAI et al. hippocampus. It is postulated that the hippocampus generates important cues in orientation in space, and the vestibulo-hippocampal projection contributes to the mechanism of vestibular compensation. The major role played by vestibular fibers in the mesencephalon is the mediation of the delicate vestibulo-ocular reflexes. According to the present findings, the LVN takes only a minor part in this activity, and physiological experiments support this conclusion [28, 31]. There are extensive LVN connections all over the RF in the brainstem. The periaqueductal gray matter is richly supplied by vestibular fibers. These connections are probably involved in static motor coordination, as suggested by the finding that elec- trical stimulation of the PAG facilitates responses of the deep dorsal muscles evoked by the stimulation of the LVN. The assumption that the PAG is involved in vestibular compensation is supported by the increases in c-fos RNA and protein level in this area following labyrinthectomy. In the rostral part of the rhombencephalon, the projection of the LVN onto the dorsal part of the RF and the paragigantocellular nucleus is especially strong. More caudally, the projection extends to the ventromedial part of the FM. The number of LVN fibers is appreciably high in the medial part of the RF, an area known to control the activity of somatic motoneurons [43] and preganglionic vegetative motoneurons [1, 30]. The projection to the lateral part of the RF is weaker; this area contains a number of vegetative nuclei known as respiratory and cardiovascular areas and cardiovascular system [22, 43] in physiological experiments. Some of the neurons in these areas express the c-fos early gene during eme- sis, suggesting the presence of a “vomiting” nucleus [29]. The LVN also sends a few fibers to the nucleus of the solitary tract and to the dorsal nucleus of the vagus. The relatively few fibers in this lateral part of the RF suggest that the LVN has only a weak influence on vestibulo-vegetative functions; the MVN and DVN have been reported to be the main sources of vestibular input to these vegetative areas [4, 43]. The commissural and ipsilateral projections, which interconnect the vestibular nuclei on the same and contralateral sides, are of special interest from the aspect of finding a possible substrate for the neural mechanism of vestibular compensation. The lack of vestibular input on one side may be compensated by a probable higher activity in the commissural and internuclear connections. The general interest in this question has generated a number of experiments on a variety of animal species [9, 13, 20]. It is difficult to summarize the many, and slightly differing results. It seems that these interconnections are confined to the ipsilateral side with extensive reciprocal relations between the SVN, MVN and DVN. There are only two reports [13, 20] which give an account of contralateral connections between the NVN and DVN. The LVN takes only a minor part in these internuclear relations with its interconnections with the DVN and MVN, this latter being in reciprocal relation [36]. Earlier degeneration studies succeeded in demonstrating contralateral interconnections between the two LVNs in different animal species. In the present experiment, we could reveal both contralateral and ipsilateral projections to all vestibular nuclei. To estimate from the number of labeled fibers in the nuclei, the ipsilateral projections were appreciably stronger than the contralateral ones. It was interesting to observe

Acta Biologica Hungarica 53, 2002 Projections of lateral vestibular nucleus in the rat 19 intranuclear connections within the LVN. When the tracer was injected into the posterior part of the nucleus, its anterior half contained a large number of stained fibers. Since these fibers did not leave the confines of the nucleus, it may be supposed that they established connections in loco with LVN neurons. This notion requires electron microscopic verification. The projection of vestibular fibers onto the spinal cord has been investigated and reinvestigated several times. In classical descriptions, a bilateral medial vestibulospinal tract and an ipsilateral lateral vestibulospinal tract were discerned. Fibers trav- eling in these tracts were presumed to originate in the LVN and to supply the rostral part of the spinal cord. Later, a third tract was added to the descending vestibular projection: the caudal vestibular tract [36]. Axons in this tract travel bilaterally in the ventral, lateral and dorsolateral funiculi, and the cells of LVN origin lie in the caudal pole of the DVN and MVN [36]. In consequence of recent findings [8], this subdivision of the vestibulospinal projection is considered to be an oversimplification. It has been shown that a single vestibular fiber may give collaterals to more than one spinal segment at different levels, and the MVN and DVN also contribute to the medial and lateral vestibular tracts. Although we have investigated only the LVN projection, we believe that the distribution, origin and termination of the vestibulospinal tracts are too complex to allow a rigorous subdivision on the basis of our present knowledge. We have found that fibers of LVN origin travel in all funiculi on both sides in the rat. They are more numerous in the anterior and in the ventral part of the lateral funiculus on the ipsilateral side. Numerous collaterals invade the cervical, brachial and lumbosacral segments; relatively few of them are seen in the thoracic segments. Except for laminae I and II, they present all over the gray matter, and in especially large number in laminae VII and VIII. There have been reports based on philologi- cal experiments about their direct terminations on motoneurons [23, 24]. The number of labeled fibers suggests that the lumbosacral part of the spinal cord receives the richest projection from the LVN.

ACKNOWLEDGMENTS

The authors thank Mrs. B. Szanitter, Mrs. D. Á. Miklós and Mrs. Á. Nagy for technical assistance. The study was supported by the Ministry of Education (FKFP 0425/99), and the Hungarian Scientific Research Fund (OTKA T 034376).

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