Macro and microstructural organization of the rabbit's celiac-mesenteric ganglion complex ( Oryctolagus cuniculus)

ANNALS OF ANATOMY

Macro- and microstructural organization of the rabbit's celiac-mesenteric ganglion complex

( Oryctolagus cuniculus)

Tais H. de C. Sasahara*, Romeu R. de Souza, Mdrcia R. F. Machado*, Ronaldo A. da Silva, Wanderley L. Guidi, and

Antonio Augusto C. M. Ribeiro

Department of Surgery, College of Veterinary Medicine, University of S~o Paulo (USP), Av. Prof. Dr. Orlando Marques de Paiva, 87 CEP: 05508-000, Silo Paulo, Brazil, and *Department of Morphology and Physiology, University of the State of S~o Paulo

(UNESP-Jaboticabal)

Summary. The macro- and microstructures of the rabbit celiac-mesenteric ganglion complex are described in 20 young animals. We found ten celiac ganglia, twenty-seven cranial mesenteric ganglia and eleven celiac-mesenteric ganglia. The celiac ganglia had a rectangular shape in nine cases (90%) and a circular one in one case (10%). The cranial mesenteric ganglia presented triangular (66.7%), rectangular (11.1%), L-shape (18.5%) and semilunar (3.7%) arrangements. The celiac-mesenteric ganglia were organized in three patterns: a single left celiac-mesenteric ganglion having a caudal portion (72.7%); celiac- mesenteric ganglia without a caudal portion (18.2%) and a single celiac-mesenteric ganglion with two portions: left and right (9.1%).

The microstructure was investigated in nine celiac-mesenteric ganglia. The results showed that the celiac-mesenteric ganglion is actually a ganglion complex constituted of an agglomerate of ganglionic units separated by nerve fibers, capillaries and septa of connective tissue. Using the semi-thin section method we described the cellular organization of the celiac-mesenteric ganglion complex. Inside of each ganglionic unit, there were various cell types: principal ganglion neurons (PGN), glial cells (satellite cells) and SIF cells (small intensely fluorescent cells or small granular cells), which are the cytologic basis for each ganglionic unit of the rabbit's celiac-mesenteric ganglion complex.

Key words: Celiac ganglion - Cranial mesenteric ganglion - Sympathetic ganglia - Rabbits

Correspondence to: A. A. Coppi Maciel Ribeiro E-mail: [email protected]

Introduct ion

The prevertebral ganglia are responsible for the control of visceral functions. These functions are regulated by syn- aptic connections that occur inside the ganglia between the preganglionic and postganglionic fibers. The celiac- mesenteric ganglion innervates the stomach, intestine, li- ver, pancreas and spleen, involving vasoconstriction, peri- stalsis and glandular secretion.

The studies regarding this subject have mainly been performed on laboratory animals. For instance, the guinea-pig celiac ganglion is formed by two lobes of neural tissue. These lobes are connected and surround the origin of the cranial mesenteric artery (Messenger and Furness 1992).

Three main constituents of the rat left celiac mesenteric ganglion are: the left suprarenal ganglion which is continuous with the left celiac nerve and the left splanchnic trunk; the left celiac ganglion and the superior mesenteric ganglion which are connected to one another and the in- termesenteric ganglia. Moreover, the greater splanchnic nerve is continuous with the right suprarenal ganglion (Hamer and Santer 1981).

Apart from small rodents there is little data concerning the macro- and microstrueture of the celiac-mesenteric plexus in large mammals and no comparative studies have been performed to investigate possible allometric adaptations, which should make differences in the ganglionic macro- and microrganization.

Morphologic studies revealed that the caudal mesenteric, celiac-mesenteric and cranial cervical ganglia are formed by several ganglionic units, which are surrounded by connective tissue septa in buffaloes (Ribeiro et al.

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2000 a), in the domestic cat (Ribeiro et al. 2000 b) and in dogs (Ribeiro et al. 2002; Gagliardo et al. 2003). All the ganglia were surrounded by a connective tissue capsule that contained fibroblasts and collagen fibers.

Similar studies were carried o u t by Gabella et al. (1988) in sheep superior cervical ganglion focusing on morphometr ic aspects of principal ganglion neurons and glial cells.

Due to the lack of specific data in rabbits, this paper describes the correlation between the macro- and microstructures of the celiac-mesenteric plexus, focusing on the morphologic relationships among their different cell types. The results will give support for comparative, stereologic and morphometr ic studies in order to support developmental , clinical and neurologic investigations in Veterinary Medicine.

was up to three days. The specimens were washed with a cacodylate buffer solution and postfixed in 2% osmium tetroxide. Next, the samples were en-bloc stained with saturated aqueous uranyl acetate solution for 1 hour in the dark. The material was dehydrated in graded series of alcohol (from 50% to 100%) and embedded in propylene oxide and araldite mixture in different proportions up to pure Araldite (Polyscience®). Then, the material was cut into 0.4-0.5 ~tm thick sections, dried on a hot plate, stained with toluidine blue, mounted under a coverslip with a drop of araldite, and examined and photographed using a DMR Leica microscope.

Results

Macrostructure

Material and methods

Macrostructure

Twenty 34-day-old New Zealand rabbits (nine male and eleven female) weighing 850 g on average were used in this study. The animals came from the Animals House of University of Sao Pau- lo State and were euthanised by endovenous injection of pento- barbitone (150 a 200 mg/kg). After this procedure, a celiotomy was performed to observe the origins of the celiac and cranial mesenteric arteries and their respective ganglia. The dissection was carried out under surgical microscope (LEICAM651) (6-40 x). In order to improve this method, the abdominal cavity was immersed for 2 hours in a 60% acetic acid alcoholic solution and a 20% hydrogen peroxide aqueous solution to facilitate the visualization of the whole extension of the celiac-mesenteric plexus in 11 specimens. In addition, the same region was immersed in a 40% picric acid solution for i hour.

For adequate denomination of the components of the celiac- mesenteric plexus, we used the terminology in accordance with the International Committee on Veterinary Nomenclature (1994).

Microstructurc

Conventional Light Microscopy: Four celiac-mesenteric ganglia were perfused by abdominal aorta with a 10% formaldehyde solution in PBS (pH7.4; 0.1 M; 20°C). Then the ganglia were immersed in the same fixative solution for at least 2 hours. The material was dehydrated in a graded series of alcohol (from 70% to 100%). Then the ganglia were embedded in Paraplast (Sigma) and cut into 5-8 tam thick sections and stained with hematoxylin- eosin (H. E.), toluidine blue, picrosirius (for observation with po- larized and non-polarised light) and Masson's trichromstain. The sections were observed and photographed under the DMR LEI- CA microscope.

Semi-thin section Light Microscopy: Five celiac-mesenteric ganglia were used for semi-thin microscopy. They were perfused via the abdominal aorta and immersed in a Karnovsky's modified fixative solution (3% glutaraldehyde and 1% formaldehyde in 0.125 M Na cacodylate (pH 7.4) at room temperature. After this procedure they were cut in half along the length and also cut into cranial, middle and caudal portions. The period of the fixation

Celiac ganglia

We found 10 celiac ganglia (20.8%). Nine on the left antimere and one on the right antimere. These ganglia were rectangular in shape in nine cases (90%) and circular in one instance (10%). The only celiac ganglion found on the right antimere was rectangular (11.1%) and in the left antimere, we found the same shape in 8 cases (88.9%). The circular shape was found on the left antimere.

All the celiac ganglia were located caudolaterally to the celiac artery (cases 4, 5, 6) (Fig. 3).

Cranial mesenteric ganglia

We were able to identify twenty-seven cranial mesenteric ganglia (56.3%), eight on the left antimere, eighteen on the right antimere and one that had two portions: right and left. The cranial mesenteric ganglia had a triangular profile in eighteen cases (66.7%), a rectangular one in 3cases (11.1%), an L-shaped arrangement in 5cases (18.5%) and a semilunar arrangement in one case (3.7%). All the triangular ganglia were located on the right antimere. In addition, on the left antimere we found L-shaped and rectangular ganglia.

In six animals, the left cranial mesenteric ganglia projected towards the caudal margin of the homonymous artery (case 4) (Figs. 1 A and 3).

The left cranial mesenteric ganglion also presented a periarterial position (10%; case 5) (Fig. 3). The semilunar arrangement was found only in animal 6 (case 6). In this case, the left and the right portions were connected on the caudal margin of the cranial mesenteric artery (Fig. 3).

Celiac-mesenteric ganglia

We have observed eleven celiac-mesenteric ganglia (22.9%), ten on the left antimere and one which had two portions: right and left. These ganglia were distributed according to three possible patterns:

A single left celiac-mesenteric ganglion having a caudal portion. Eight ganglia were classified in this category

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(72.7%), all of them on the left antimere and presenting an L-shaped arrangement (case 3). The ganglia had a periarterial position and they were projected to the caudal margin of the homonymous artery (Fig. 3).

Celiac-mesenteric ganglion without a caudal portion. Two celiac-mesenteric ganglia were located at the left surface of the cranial mesenteric artery in two animals (18.2%) (case 2) (Fig. 3).

A single celiac-mesenteric ganglion with two portions: left and right. The left and right portions were connected at the caudal margin of the cranial mesenteric artery. This arrangement had a semi-lunar conformation (9.1%) (case 1) (Fig. 3).

Three-dimensional arrangement patterns of the celiac-mesenteric plexus

Analysing the macrostructure of the celiac, cranial mesenteric and celiac-mesenteric ganglia under an overall view (involving the two antimeres together), we were able to classify the framework of the celiac-mesenteric plexus in six different cases.

Case 1. A single celiac-mesenteric ganglion with two portions: left and right one. This case represented 5% of the animals studied (Fig. 3).

Case2. Left celiac-mesenteric ganglion associated with the right cranial mesenteric ganglion by means of interganglionic fibers. This was found in 10% of the animals analysed (Figs. 1 B, 3).

Case 3. Left celiac-mesenteric ganglion having a caudal portion joined to the right cranial mesenteric ganglion by means of interganglionic fibers. This case represented 40% of the animals studied (Fig. 3).

Case 4. Left celiac ganglion associated by means of interganglionic fibers with the left cranial mesenteric ganglion. This last had a caudal portion, which was associated by interganglionic fibers with the right cranial mesenteric ganglion. This case represented 30% of the animals studied (Figs. 1 A, 3).

Case 5. Left celiac ganglion joined by means of interganglionic fibers with a left cranial mesenteric ganglion. This did not have a caudal portion. In the right antimere, there was a right cranial mesenteric ganglia only. This case represented 10% of the animals studied (Fig. 3).

Case 6. Left celiac ganglion associated with one cranial mesenteric ganglion by means of interganglionic fibers. The cranial mesenteric ganglion had two portions: left and right. In the right antimere, the right portion of the cranial mesenteric ganglion was associated with the right celiac ganglion by means of interganglionic fibers. This case represented 5% of the animals studied (Fig. 3).

Microstructure

The celiac-mesenteric ganglion was seen as a ganglion complex constituted of an agglomerate of ganglion units (Fig. 2 A) separated by nerve fibers, mast cells, capillaries and of connective tissue septa. These connective tissue septa were mainly formed by type I collagen fibers and fibroblasts. The type III collagen fibers (reticular fibers) however, were more frequently distributed inside the ganglion units. All the ganglionic complex was surrounded by a single and thick capsule composed predominantly of type I collagen fibers. In this capsule, which is a continuation of the sheath of incoming and outgoing nerves, the presence of capillaries was also observed.

Fig. 1. Gross structure of the rabbit celiac-mesenteric ganglion complex (A-B). A: Right antimere. Cranial mesenteric artery (cma), celiac artery (ca). Right cranial mesenteric ganglion (~-), associated by means of interganglionic fibers (arrows) with the caudal portion of the left cranial mesenteric ganglion (m). B: Left antimere. Celiac artery (ca), cranial mesenteric artery (cma). Left celiac-mesenteric ganglion (,) associated to the greater splanchnic nerve (arrow). Right cranial mesenteric ganglia (*).

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Fig. 2. Semi-thin structure of the rabbit celiac-mesenteric ganglion complex (A-D). A: Principal ganglion neurons (n). Eccentric nucleus containing nucleoli (arrow). Ganglionic units (u). Scale bar = 35 gin. Toluidine Blue. B: Principal ganglion neuron (m). Ec- centric nucleus (~ ) . Nucleolus (arrow). Neuropil (*). Scale bar = 15 gm. Toluidine Blue. C: Two binucleate neurons (*). Nucleus of glial cell (arrow). Post ganglionic fiber (p). Scale bar = 15 ~tm. Toluidine Blue. D: Capillary (larger arrow). Tight cluster of SIF cells (arrows) close to the principal ganglion neuron. Scale bar = 15 gin. Toluidine Blue.

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Inside each ganglion unit there were various cell types. The principal ganglion neurons had a circular or spindle profile and their nuclei were predominantly eccentric (Figs. 2 A and 2 B). The capillaries were surrounding each ganglionic unit such as vascular circles and contained endothelial cells (Fig. 2 D).

Using Semi-thin Section Light Microscopy we were able to observe more details regarding the cellular organization of the celiac-mesenteric ganglion complex due to the better resolution of the semi-thin sections.

Inside each ganglion, different cell types were found. The principal ganglion neuron (PGN) was surrounded by a group of cells of the glial type (satellite cells) which together with the fibroblasts and collagen fibers composed the glial capsule, which was well defined (Fig. 2B). This structure along with the axons and vessels characterized the nenropil wrapping the ganglion neurons (Figs. 2 B and 2C). The large capillaries surrounded each ganglionic unit such as vascular circles and contained endothelial cells. These capillaries were termed intraganglionic and interunits. Small capillaries were also observed inside the ganglionic units. These capillaries were termed intraganglionic and intraunits (Fig. 2 D).

Ganglionic units

The ganglion units were composed of principal ganglion neurons (PGN), glial cells, SIF cells and intraunit capillaries and were separated by connective septa, fibroblasts and interunit capillaries (Figs. 2 A, 2 B, 2 C and 2 D).

Ganglionic cell types

Principal ganglion neurons (PGN). The principal ganglion neurons had a circular, near circular or spindle-shaped profile and their postganglionic fibers were clearly obser- vable. Their nuclei were predominantly eccentric, but some of them were central. Each nucleus contained one or two well delineated and stained nucleoli (Figs. 2 A and 2 B). Furthermore, Binucleate Principal ganglion neurons were also observed (Figs. 2 C and 2 D).

Glial cells (satellite cells). Only the glial cell nuclei were observed around the principal ganglion neurons. The pro- cesses of the glial cells formed a complete wrapping around each ganglion neuron constituting its glial capsule, together with the collagen fibers. In the majority of the PGN observed, the glial cell was single. However, two or three glial cells were seen around the same PGN distributed at three different points along the only capsule (Fig. 2 C).

SIF cells (small intensely fluorescent cells) or small granular cells or chromaffin cells. They have been classified into two types. The first type formed clusters located in close proximity to the capillaries and arterioles. The second type of SIF cells were scattered within the ganglion in close contact with the principal ganglion neurons.

Under semi-thin section light microscopy, the two types of SIF cells were identified based on two standard aspects: location and tight clusters of 3-6 cells. These structural characteristics make SIF cells easily differentiable (Fig. 2D).

Case 1

Case 2

Case 3

J ~

Case 4

Case 5

Case 6

12

1 = Celiac-mesenteric ganglion with two portions: left and right.

2 = Right cranial mesenteric ganglion.

3 = Left celiac-mesenteric ganglion. 4 = Right cranial mesenteric gang-

lion. 5 =Left celiac-mesentefic ganglion

with a caudal portion. 6 =Right cranial mesenteric gang-

lion. 7 = Left celiac ganglion 8 = Left cranial mesenteric ganglion

with a caudal portion. 9 = Right cranial mesenteric gang-

lion. Left celiac ganglion. Left cranial mesenteric ganglion. Right celiac ganglion. Left celiac ganglion. Cranial mesenteric ganglion with two portions: left and fight.

10= 11=

t14 12 = 13=

j ~ 14 =

Fig. 3. Arrangement types of the celiac-mesenteric plexus in rabbits (Oryctolagus cuniculus). Celiac artery (CA), cranial mesenteric artery (CMA).

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Discussion

The studies of the autonomic ganglia, especially of the celiac, the cranial mesenteric and the celiac-mesenteric, were performed by several authors who described their morphology in different species such as cats (Furuzawa et al. 1996); goats (Bhamburkar and Prakash 1993); rats (Hamer and Santer 1981), guinea pigs (Messenger and Furness 1992), rabbits (Langenfeld 1988), coypu (Langen- feld 1991 a, b); buffaloes and cats, respectively (Ribeiro et al. 2000 a, b). However, few authors have studied the as- sociation of the macro and microscopic aspects especially in large and medium-sized mammals (Ribeiro et al. 2000 a, b), or the correlation between the structure and ultrastructure (Ribeiro et al. 2002), predominating works that focused only on the macroscopic or the microscopic points of view.

In this way, Paz and Rosen (1989), by means of macroscopic study observed that the human celiac ganglion had a triangular shape as the most common one. This shape seems to be the result of the ganglion connections. Hamer and Santer (1981) however, noted the rat's right celiac ganglion had a pear shape and was smaller than its coun- terpart on the left. The left celiac ganglion was more elongated than the right one.

In our study the left celiac ganglion had a rectangular conformation as the most common, but a circular arrangement was found as well. Further, the only right celiac ganglion had a rectangular shape.

In contrast to Paz and Rosen (1989), we did not find a triangular shape in the celiac ganglia and yet, in rabbits we can affirm that the most common celiac ganglion shape is the rectangular (90% of the cases).

The different forms of the ganglia are associated with each animal species. Hence, morphologic variation can be found. In buffaloes the most frequent disposition was one celiac-mesenteric ganglion with two portions: right and left (Ribeiro et al. 2000a). In addition, the fusion between the celiac ganglion and the cranial mesenteric ganglia was the most frequent arrangement observed in cats (Ribeiro et al. 2000 b).

In rats, the right celiac and the right superior mesenteric ganglia were fused, but on the left antimere these ganglia were interligated only by means of nerve fibers. The position of the ganglia was almost parallel to the abdominal aorta, with slight superomedial inclination. The right celiac ganglion lies caudolateral to the celiac artery and the left celiac ganglion also lies caudolateral to this artery in a similar position (Hamer and Santer 1981). In our study, we have found the left celiac-mesenteric ganglion projecting to the caudal margin of the cranial mesenteric artery (40%) and connected to the right cranial mesenteric ganglion (case3). In 90% of cases no celiac ganglia were found on the right antimere.

Therefore, the predominant rabbit's celiac-mesenteric plexus three-dimensitional pattern is that represented in case 3 (40% of animals).

However, the ganglia can assume different forms, dis- positions and relations with the other nerve components of this plexus. All of these aspects are important to under- stand the ganglion activity. The different macroscopic conformation can also reveal the complex organization of the ganglionic cells showing the importance of the comparative studies involving the interrelationship between macro- and microstructural aspects.

For instance, the microarrangement of the ganglion cells in clusters may indicate the formation of functional pockets for the innervation to a vast number of effector organs with divergent functions (Bhamburkar and Pra- kash 1993).

Yet when the celiac-mesenteric ganglia were observed under both macro- and microscopic views, it was possible to establish a correspondence between the connective ganglionic capsule and the different ganglionic cells and ganglion units surrounded by it, and consequently the in- ternal cellular organization.

Concerning this subject, Gabella et al. (1988) in sheep and Gabella (1995) in rats, found that the superior cervical ganglion is constituted by different types of cells: principal ganglion neurons, nerve fibers, fibroblasts, glial cells, mast cells, SIF cells and capillaries. Sudhakar and Rao (1979) also noted the presence of a few of these elements in the buffalo autonomic ganglia, but being just a generic description, did not mention their complex organization in ganglionic units.

The cellular organization of the rabbit celiac-mesenteric ganglion is similar to that reported by Gabella et al. (1988) and Gabella (1995) for the superior cervical ganglion.

In terms of cytologic PGN features, there were binucleate neurons, in contrast to Appenzeller (1990) and Mio- lan and Niel (1996) who reported that in mammals these cells were only mononucleate, though Ermilov et al. (2000) have found binucleate neurons in guinea pigs. Further, we have also observed the predominance of eccentric PGN nucleus as cited by Cormack (1987) and Wheater et al. (1994).

The PGN were all individually ensheathed by the pro- cesses of a single satellite cell (glial cell), in accordance with the studies of Brodal (1984), Gabella (1995) in rats, and Appenzeller (1990) in humans.

The glial cells originate the glial capsule which limits the diffusion of extracellular fluids in contrast to the sensory ganglia where the satellite cells are arranged loosely around the principal neuron allowing the free diffusion of neurotracers, such as horseradish peroxidase (HRP) (Ga- bella 1995). Moreover, in some cases two or three glial cells were seen involving the PGN in the rabbit's celiac- mesenteric ganglion complex.

The third major cell type found in the rabbit's celiac- mesenteric ganglion was SIF cells (small intensely fluorescent cells), also called chromaffin cells or small granular cells.

These cells, which originate from the neural crest, are heterogeneous in distribution, morphology and chemical

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composition and are part of a large group of chromaffin and chromaffin-like cells, which include cells of paragan- glia and the adrenal medulla, and cells scattered in many tissues outside the nervous system.

Under light microscopy, SIF cells arc identified by their small size and their distribution in tight clusters (Szurs- zewski and Miller 1994; Gabella 1992, 1995, 1998). Furthermore, Miolan and Niel (1996) classified these SIF cells into two types in accordance with their location.

The first type forms clusters located close to fene- strated capillaries, reflecting their neuroendocrinal role. The second type of SIF cells were scattered within the ganglion and were in close contact with the principal ganglion neurons, suggesting that they may function as in- terneurons.

In the rabbit's celiac-mesenteric ganglion we have reported cells in clusters of 3-6 associated with capillaries and arterioles and also in contact with PGNs. For the rat pelvic ganglion Gabella et al. (1992) have described clusters of 5-20 cells, also close to capillaries. Moreover, in the canine celiac-mesenteric ganglion complex SIF cells associated with PGNs (Ribeiro et al. 2002) have also been reported, though Gagliardo et al. (2003) have observed tight clusters of 6-10 SIF cells associated with capillaries and arterioles, but not in contact with PGNs for the dog's caudal mesenteric ganglion complex.

In addition, Gabella (1995) has classified the SIF cells according to the size of the granular vesicles contained in their cytoplasm. Type I SIF cells have vesicles measuring 80-100 nm, whereas type II SIF cells have vesicles of 150- 300 nm diameter. However, Mascorro et al. (1994) have reported that when a small granule containing cell (SGC) occurs alone, its granules are less dense and smaller than those seen in the clustered variety. Additionally, the same authors have reported that the granularity of SIF cells be- comes most evident at the ultrastructural level. However, these cells are clearly evident at the light microscopic level, where the identification is based on small clusters al- ways associated with at least one blood vessel (Matthews and Raisman 1968, 1969; Matthews 1989; Mascorro et al. 1994).

Although authors have reported the presence of capillaries inside the prevertebral ganglia (Gabella et al. 1988; Gabella 1995), the vascular organization has now been studied from an overall perspective, focusing on its relation with other ganglionic elements such as connective tissue, nerve cells, neuropil, and mainly the vascular distribution along the ganglionic units. Therefore, in the rabbit's celiac-mesenteric ganglion complex the small capillaries were placed inside the ganglionic units (intraganglionic and intraunit) and large capillaries and arterioles surrounded each ganglionic unit as vascular rings (intraganglionic and interunit). Moreover, capillaries in the ganglionic capsule were also observed. A similar vascular arrangement was reported by Ribeiro et al. (2002) for the canine celiac-mesenteric ganglionic complex.

Ganglionic connective capsules have been reported by

$udhakar and Rao (1979) (buffaloes); Bhamburkar and Prakash (1993) (goats) Ribeiro et al. (2000 a) (buffaloes); (2000 b) (cats).

Ribeiro et al. (2000 a, 2002) and Gagliardo et al. (2003) using the picrosirius stain technique observed that the ganglionic capsule had predominantly type I collagen fibers and further elastic ones. The same capsular components were observed in rabbits, except the presence of the elastic fibers which were not studied on this occasion.

In relation to the intraganglionic connective tissue organization, type I collagen and type III collagen (reticular) fibers were found in the capsular septa in buffaloes (Ribeiro et al. 2000a) and in dogs (Ribeiro et al. 2002; Gagliardo et al. 2003). However, in the present study the reticular fibers were more frequently distributed inside the ganglion units and yet, they were not components of the capsular connective septa where type I collagen fibers predominated.

In conclusion, the celiac-mesenteric ganglion complex has several ganglionic units that are distributed in distinct morphological segments. As with Szurszewski and Miller (1994) three major cell types are constantly present in each unit of this complex: principal ganglion neuron (PGN), glial cell or satellite cell and chromaffin cell or SIF cell.

Therefore, the Ganglionic Unit is the morphologic support for the microstructural organization of the Rabbit Celiac-Mesenteric Ganglion Complex.

Moreover, since each Ganglionic Unit is constituted by a cellular triad, as quoted above, we can assume that SIF cell, glial cell and PGN are the cytologic basis for each Ganglionic Unit. The same microstructural pattern was reported by Ribeiro et al. (2002) for the canine celiac-mesenteric ganglion and by Gagliardo et al. (2003) for the canine Caudal Mesenteric ganglion complex.

Hence, it suggests a specific pattern for large mammals, and additional investigations on these prevertebral ganglia should be pursued to shed light on other possible allometric-related structural adaptations.

These units may play a role in the extrinsic innervation of a particular target organ. For instance, the studies of Ming-Zi and Masuko (1997), using a retrograde tracer into the walls of the distal colon and the rectum of the dog demonstrated a group of neurons distributed at the emergence of lumbar colonic nerve from the caudal mesenteric ganglion.

Moreover, Wasowicz et al. (1998) noted a uterine region in the inferior mesenteric ganglion of pigs after the application of a fluorescent retrograde neurotracer. The neurons were located close to the output of intermesen- teric and colonic nerves.

Thus, further investigations are necessary to elucidate the existence of spacial differences in the distribution of the ganglionic units in relation to the target and to those in relation to the vasomotor fibers.

The use of neurotracers and anatomical investigations may explain the morphological adaptation of prevertebral ganglia as a result of their territory of innervation.

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Acknowledgements. We thank Silvia Helena Gerbasi for her ex- cellent artistic drawings. This work was supported and approved by Bioethical Commission of Silo Paulo State Research Support Foundation (FAPESP) (Application number: 00/05123-3).

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Accepted April 23, 2003

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Macro and microstructural organization of the rabbit's celiac-mesenteric ganglion complex ( Oryctolagus cuniculus)

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