rostrocaudal and ventrodorsal change in neuronal cell size in human medial vestibular nucleus

THE ANATOMICAL RECORD 246~403-409 (1996)

Rostrocaudal and Ventrodorsal Change in Neuronal Cell Size in Human Medial Vestibular Nucleus

CELSO DfAZ, CARLOS SUAREZ, ANA NAVARRO, CARMEN GONZALEZ DEL REY, JUAN CARLOS ALVAREZ, ELENA MgNDEZ, AND JORGE TOLNIA

Seccidn de Otorrinolaringologia, Hospital San Agustin, Aviles (CD.); Departamento de Otorrimlaringologla, Hospital Central de Asturias (C.S.), Departamento de Morfologia y

Biologia Celular, Facultad de Biologia y Medicina, Universidad de Oviedo (AN. , C.GD.R., J.C.A., EM. , J.T.), Spain

ABSTRACT Backgroud: The present paper describes the cytoarchitectonic, morphometric, and three-dimensional characteristics of the human medial vestibular nucleus (MVN). We also studied the regional distribution, in size, of the different neurons and its possible relationship with a functional polarization of the different regions of the nucleus.

Methods: Nine adult human brainstems (30-50 years of age) without neurological problems were used. Specimens were obtained from necropsy and fixed in 4% paraformaldehyde and 5% acetic acid in distilled water. After fixation, blocks were washed, dehydrated, and embedded in paraffin and serial sectioned at 20 pm. Sections were stained with formaldehyde- thionin, dehydrated, cleared in eucalyptol, and mounted with Eukitt. MVN neurons were drawn with the aid of a camera lucida at 200-pm intervals at 3 9 0 ~ magnification. Serial W-pm frozen sections were used to determine the volume of the MVN. The three-dimensional reconstruction of MVN was accomplished with a drawing program in a Macinthosh I1 computer and an AVS on a Stardent workstation computer.

Results: In the three-dimensional reconstruction, the human MVN shows a pyramidal form. The base of this pyramid constitutes the rostral limit, and its vertex forms the caudal border of the MVN. The estimated volume is 30.44 f 0.85 mm3, with a neuronal population of 127,737 cells and 4,136 neurons/mm3 in density. The average neuronal cross-section changes from one minimum at caudal level (212.46 f 2.04 pm2) to one maximum at rostral level (491.47 f 5.08 pm?. Four cell types, small (<200 pm'), medium (200-500 pm'), large ~500-1OOO pm2), and giant (>1,000 pm2) cells, were observed. Medium cells constitute 66%, small cells 18%, and large and giant cells 15% and 1% of the neuronal population. Conctwrions: The MVN shows a variation in neuronal size, and it has the

highest neuronal density of all the human vestibular nuclei. Large cells predominate in rostral regions of the MVN, with significant differences in the area and diameter of the cells among rostral, central, and caudal regions. Furthermore, the largest cells are grouped in the ventrolateral part of the nucleus, close to its boundaries with the inferior and the lateral vestibular nuclei. The morphological polarization, with respect to the neuronal size of the MVN, can be related to a functional polarization of rostral and caudal regions of this nucleus. o im Wiey-Liss, Inc.

Key words: Morphometric, Neuroanatomy, Cytoarchitectonic, Structure, 3-D reconstruction. Vestibular nuclei, Human

The medial vestibular nucleus (MVN) is the largest and longest of the vestibular nuclei in all mammals that have been studied to date (Olszewski and Baxter, 1954; Brodal and Pompeiano, 1957; Sadjadpour and Brodal, 1968; Henkel and Martin, 1977; Sugawara,

0 1996 WILEY-LISS. INC.

Received October 25, 1995; accepted June 24, 1996. Address reprint requests to Dr. Jorge Tolivia, Departamento de

Morfologia y Biologia Celular, Facultad de Biologia y Medicina, Uni- versidad de Oviedo, Juliln Claveria s/n, Oviedo 33006, Spain.

404 DfAZ ET AL.

1978; Rubertone and Haines, 1982; Brodal, 1984; Gstoettner and Burian, 1987; Gonzalez del Rey et al., 1991; Suarez et al., 1993), except in the chinchilla (Suarez et al., 1989; Newman et al., 1992). The MVN extends for the most part along the floor of the fourth ventricle, and it is laterally related to the lateral vestibular nucleus (LVN) and caudally to the superior vestibular nucleus (SVN). This part of the vestibular complex is characterized by its high cellular density and a minor presence of myelinated fibers, in contrast with the rest of the vestibular nuclei (Brodal, 1974).

Studies on the fiber connections have shown the ex- istence of a complex system of afferent and efferent projections to and from the MVN. The spinal cord (Pompeiano and Brodal, 1957b; Brodal and Angaut, 1967; Rubertone and Haines, 1982; Prihoda et al., 1991), the cerebellum (Angaut and Brodal, 1967; Haines, 1975, 1976, 1977; Carleton and Carpenter, 1983; Langer et al., 19851, vestibular labyrinth (Stein and Carpenter, 1967; Gacek, 1969; Carleton and Car- penter, 1984; Uchino and Hirai, 1984; Burian et al., 1990; Newman et al., 1992), reticular formation (Ger- rits and Voogd, 19861, and parietal cortex (Faugier- Grimaud and Ventre, 1989) have connections with this vestibular nucleus.

Efferent projections from the MVN principally sup- ply the oculomotor nuclei (Gacek, 1971, 1977, 1979; Steiger and Buttner-Ennever, 1979; Yamamoto et al., 1978; McCrea et al., 1986, 1987a,b), the spinal motoneurons that innervate the cervical muscles (Peter- son and Coulter, 1977; Peterson et al., 1978) and the cerebellum (Kotchabhakdi and Walberg, 1978). There- fore, the MVN plays an important role in the regula- tion of ocular, cephalic, and cervical movements (Isu and Yokata, 1983; Uchino and Hirai, 1984; Shinoda et al., 1992). Moreover, the MVN is an important compo- nent of the commissural system and can play an important role in the central mechanisms of compensa- tion, which appears after peripheral vestibular lesions (Carpenter, 1988). In addition, within a given area of the vestibular complex, there are morphological differences among neurons, depending on the sites to which they project (Mitsacos et al., 1983a,b). However, some studies have shown a close correlation between physiological and morphological properties of the primary vestibular neurons (Honrubia et al., 1989). It is also likely that in the vestibular nuclei differences among the sizes of neurons may reflect different physiological properties. There are only partial data in the literature about objective measurements related to possible functional differences observed in the vestibular nuclei in human (Diaz et al., 1993). Thus, a morphometric study of the MVN neurons will provide basic information to plan and interpret future physiological studies.

MATERIALS AND METHODS In the present study, the brainstems of nine adult

humans (30-50 years of age) without neurological problems were used. Specimens were obtained from necropsies and were fixed for 3 days in 4% paraformaldehyde, 5% acetic acid in distilled water. After fixation, six blocks were washed in distilled water, dehydrated through successive alcohols, cleared in two baths of butyl acetate, embedded in paraffin, and blocked in a suitable mold.

Serial sections of 20 Fm in thickness were obtained and attached to albumin-coated slides, dried at 36°C for 24 hr, deparaffined, hydrated, and stained for Nissl substance with a modification of formaldehyde-thionin method (Tolivia et al., 19941, dehydrated, cleared in eucalyptol, and mounted with Eukitt.

To study the neuronal morphometric parameters, all neurons of the MVN were drawn with the aid of a camera lucida at intervals of 200 Fm under microscope magnification (390 x ). Only neurons in which the nu- cleolus was visible were considered, and special care was taken to discard glial cells. With the staining method used (formaldehyde-thionin modification), neurons and glial cells show appreciable differences in cy- toplasmatic and nuclear coloration, which permits the distinction between the two types of nerve cells. This method applies the metachromatic characteristics of thionin to obtain the differential stain of neurons and myelinic fibres. This technique belongs to the class of progressive colorations that stains the nervous cells in blue tones and the myelinic fibers in red. This method may be used for Nissl-like coloration, thus shortening the time of stain, to achieve a cytoarchitectonic study. When this method is applied, the neurons show a dark blue cytoplasm and a pale blue nucleus, whereas the cytoplasm of the glial cells does not appear colored. However, these cells present an intensely colored nucleus of a slightly purple tone.

The total number of neurons was estimated by mul- tiplying the mean number of neurons counted in some representative sections by the number of sections that spanned the region. These data were corrected with a factor reported by Abercrombie (1946).

Serial 50-pm-thick frozen sections of three brainstems were stained by the formaldehyde-thionin method (Tolivia and Tolivia, 1985) and drawn with camera lucida (40 x 1. The volume of the MVN was de- termined by integrating all area measurements of each section from the most rostral to most caudal levels.

The study of morphometric parameters and the volume of the MVN were accomplished with the microim- age processing (MIP) program developed by MICRON SPAIN for image analysis in an IMCO-10 KONTRON. Data obtained from morphometric study were statisti- cally tested by using analysis of variance (ANOVA) in an SPSS/PC+ program in an IBM computer; P < 0.05 was the level of significance. The methodology used in the present study was previously applied to a study of the morphometric characteristics of the nucleus su- praopticus of the hamster (Navarro et al., 1994). The three-dimensional reconstruction of MVN was accomplished with a drawing program (Canvas 3.0, Deneba Software) in a Macintosh I1 computer and an AVS (Ad- vanced Visualization System) on a Stardent workstation computer.

RESULTS The medial vestibular nucleus is the longest and the

most voluminous of all vestibular nuclei. Transverse sections shows a triangular shape with a dorsolateral extension that approaches the dorsal cochlear nucleus (Fig. 1). The MVN extends rostrocaudally for about 9.9 2 0.8 mm. The rostral part of the MVN appears in a ventrolateral position with respect to the nucleus of the abducens nerve (Fig. 2). Caudally, the MVN ends be-

NEURONAL DISTRIBUTION IN HUMAN MEDIAL VESTIBULAR NUCLEUS 405

Fig. 1. Transverse section of human medulla oblongata; the plane of this section is shown in Figure 2. In this micrograph, the MVN at the medial level can be observed. CR, corpus restiforme; Fs, fasciculus solitarius; IV-v, fourth ventricle; MVN, medial vestibular nucleus;

N-IX, glossopharyngeal nerve; NFs, nucleus fasciculus solitarius; NPH, nucleus praepositus hypoglossi; RP, raphe; Spt, tractus spinalis nervi trigemini. Bar = 1 mm.

tween the cephalic pole of the gracilis nucleus and the group "g" of Brodal (Brodal and Pompeiano, 1957). At the rostral level, the MVN appears dorsolaterally related to neurons of the inferior pole of the SVN, and their boundaries are not clearly distinguishable be- cause their neurons are intermingled at this level (Fig. 2). The lateral limit of MVN is marked by the medial region of the LVN. The nucleus is limited ventrally to the reticular formation and medially to the caudal region of the motor nucleus of the abducens nerve (Fig. 2).

At the medial level, the lateral boundaries of MVN are marked by the LVN and the inferior vestibular nucleus (IVN) in the rostrocaudal direction (Figs. 1 & 2). Its ventral limit appears to be marked by the nucleus of solitary fascicle and the dorsal motor nuclei of vagus (Fig. 2). The nucleus of the solitary fascicle and the dorsal motor nuclei of vagus are dorsomedially dis- placed with respect to the MVN a t a more caudal level.

At the caudal level, the MVN is ventromedially limited by the nucleus of solitary fascicle and its lateral limit is marked by the IVN. In the three-dimensional reconstruction the MVN shows a general pyramidlike shape in its rostrocaudal orientation (Fig. 2). In addition, this nucleus shows a triangular profile in transverse section at most cross-sectional levels (Fig. 1). The base of this pyramid constitutes the rostral limit of the nucleus, and the vertex forms the caudal border of the MVN (Fig. 2).

The estimated volume of the MVN is 30.44 * 0.85

mm3 and contains the most cells of all vestibular nuclei, with a neuronal population of 127,737 cells and a neuronal density of 4,136 neurons/mm3. The average neuronal cross-sectional surface of the MVN is 348.96 4 1.33 pm2, with a maximum value of 1,885 km2 and a minimum value of 80.10 pmZ. The neurons of medium size (200-500 pm2) are the most abundant and constitute 66% of the entire population; small cells (<200 pm2) represent 18% and large (500-1000 pm2) and giant (>1,000 pm2) cells represent only 15% and 1% of the neuronal population (Fig. 4).

If the average neuronal cross-sectional surface is studied in the rostral, medial, and caudal regions of the MVN, a regional variation with a minimum value at the caudal level (212.46 * 2.04 pm2) and a maximum value at the rostral level (491.47 * 5.08 pm2) of the nucleus can be observed (Fig. 3). Moreover, neurons located in the ventrolateral region of the rostral portion of the MVN, near the LVN and IVN, show a greater average cross-sectional surface (695.43 & 26.95 pm2) than neurons located in the proximity of the raphe (340.60 2 4.46 pm2) and the floor of the IV ventricle (318.57 2 4.08 pm2).

The maximum diameter of the MVN neurons is 28.00 * 0.32 pm. The highest percentage of cells (51%) ranges between 20 and 35 pm, with 35% of cells being less than 20 pm and only 14% larger than 36 pm. The maximum diameter also decreases in rostrocaudal direction (Fig. 3).

406 DfAZ ET AL.

Fig. 2. A three-dimensional reconstruction of the MVN. The reconstruction shows a dorsolateral view throughout the floor of the fourth ventricle. The axes established on transversal sections, used as con- stant reference for three-dimensional reconstruction, appear repre- sented in the circle. The dashed line shows the level section of Figure

1. X, floor of the fourth ventricle; Y, raphe; Z axis that extends in the rostrocaudal direction. IVN, inferior vestibular nucleus; LVN, lateral vestibular nucleus; SVN, superior vestibular nucleus; VI, abducens nucleus; XII, hypoglossal nucleus.

DISCUSSION The cytoarchitectonic characteristics of the human

MVN are similar to that reported in previous studies in different mammals (Brodal and Pompeiano, 1957; Hen- kel and Martin, 1977; Sugawara, 1978; Rubertone and Haines, 1982; Brodal, 1984; Gstoettner and Burian, 1987; Suarez et al., 1989; Gonzalez del Rey et al., 1991; Newman et al., 1992; Suhrez et al., 1993). This nucleus

shows a wide variation in the size of its neurons, and it has the highest neuronal density of all the vestibular nuclei. Moreover, the impression of a rostrocaudal de- crease in the sue of MVN cells, which is described for other mammals (Brodal and Pompeiano, 1957; Henkel and Martin, 1977; Rubertone and Haines, 1982; Brodal, 1984; Gstoettner and Burian, 1987; GonzAlez del Rey et al., 1991; Suarez et al., 19931, with the ex-


Square micrometers Micrometers

Rostra1 Medial Caudal

AREA E MAX. DIAMETER

Fig. 3. Graph showing variation in both average cellular area and average neuronal maximum diameter in human MVN neurons at three levels: rostral, medial, and caudal.

80%

60%

40%

2w

0%

66%

1%

e m 200-500 500-1000 >loo0

Square micrometers

Fig. 4. Graph showing neuronal distribution as a function of cellular

ception of the chinchilla (Suarez et al., 1989; Newman et al., 1992), was confirmed in this quantitative study.

When the neuronal area and maximum diameter are studied, a regional distribution of cell size is clearly observed. Large neurons appear predominantly in the rostral region of the MVN, and a clear diminution of neuronal size can be observed in caudal direction. Fur- thermore, the largest cells were grouped in a ventrolateral position inside the nucleus, close to the boundaries of the IVN and LVN. These cytomorphometric data are in accordance with previously reported cytoarchitectonic studies (Sadjadpour and Brodal, 1968; Langer et al., 1985). The morphological polarization with respect to the neuronal size of the MVN may re- late to a functional polarization of rostral vs. caudal regions of this nucleus.

Studies on fiber connections show different afferent and efferent projections in both parts of the MVN. Am- pullar and floccular afferents mainly end in the rostrolateral region (Walberg et al., 1958; Stein and Carpen- ter, 1967; Gacek, 1969; Langer et al., 1985; Burian et al., 19901, and this region projects to the ocular motor nuclei (Gacek, 1977, 1979; Yamamoto et al., 1978; Steiger and Buttner-Ennever, 1979; McCrea et al., 1986, 1987a,b; Carpenter, 1988; Highstein and Mc- Crea, 1988).

area of neurons in the entire MVN.

Electrophysiologically identified secondary vesti- bule-ocular neurons intra-axonally labeled with horseradish peroxidase have been classified as large to giant cells, all of which are located in the rostral part of the MVN (McCrea et al., 1986,1987a; Ohgaki et al., 1988). The rostrolateral portion of the MVN, together with the ventromedial LVN and the rostromedial IVN, constitutes the so-called Zone I (Buttner-Ennever, 1992). This area is characterized by large to giant neurons and receives inputs from all canal and otoliths and projects to the oculomotor nuclei and the spinal cord via the medial vestibulospinal tract. In contrast, afferent and efferent cerebellar (from the nodulus and uvula) and spinal projections have been found in the caudal region of the MVN, where small neurons are more common (Angaut and Brodal, 1967; Pompeiano and Brodal, 1957a; Haines, 1977; Kotchabhakdi and Walberg, 1978; Peterson et al., 1978; Neuhuber and Zenker, 1989; Prihoda et al., 1991). Thus, this morphometric study of the MVN and its neurons provides use- ful data that correlate the anatomical distribution of these cells with their physiological properties.

Human primary vestibular neurons and fibers show great anatomical similarities to the animal ones (Hon- rubia et al., 1987; Gbmez et al., 1990; Lee et al., 1990); these anatomical characteristics are reflected in physiological properties of individual nerve fibers (FernBn- dez et al., 1988; Honrubia et al., 1989). Second-order kinetic vestibular neurons are large and discharge with higher amplitude than do tonic vestibular neurons, the former being almost exclusively innervated by thick axons (Sato and Sasaki, 1993). In contrast, tonic neurons are small or medium size and mainly receive thin axons (Sato and Sasaki, 1993). Thick axons present the most irregular spontaneous firing, whereas neurons with regular spontaneous activity have thin axons, suggesting that the variation in firing regularity may be associated with neuron size (Baird et al., 1988). Electron microscopic studies have shown two different patterns of synaptic contacts in the vestibular nuclei: axodendritic and en passant (regular fibers) and axosomatic (irregular fibers; Sato and Sasaki, 1993). These morphological features correlate with the elec- trophysiological properties of vestibular nuclei neurons. The kinetic neurons show low-threshold and large-amplitude potentials, whereas the tonic neurons have opposite properties.

ACKNOWLEDGMENTS This work was supported by FISS (93/0634) and Uni-

versidad de Oviedo (DF/95-218-5) grants. We thank K. Beykirch (UCLA Division of Head and Neck Surgery, Los Angeles, CAI for technical assistance in computers.

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