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. 2016 Jan 11;228(5):805–811. doi: 10.1111/joa.12436

Histological verification of the prehypogastric and ovarian ganglia confirms a bilaterally symmetrical organization of the ganglia comprising the aortic plexus in female human cadavers

Tyler S Beveridge 1,2, Marjorie Johnson 1,2, Nicholas E Power 2,3,4,†, Brian L Allman 1,2,†,✉
PMCID: PMC4831348  PMID: 26750570

Abstract

The aortic plexus is a network of sympathetic nerves positioned along the infrarenal abdominal aorta. Recently, we characterized the aortic plexus and its ganglia (inferior mesenteric, left/right spermatic, and prehypogastric ganglion) in males; however, the literature minimally describes its anatomy in females. In the present study, we conducted the first histological examination of the left and right ovarian ganglia, while also investigating whether females, like males, exhibit a prehypogastric ganglion. The ganglia were dissected from embalmed (n = 32) and fresh (n = 1) human cadavers, and H&E staining was used to confirm the presence of a left ovarian ganglion in 31/31 specimens, a right ovarian ganglion in 29/29 specimens and a prehypogastric ganglion in 25/28 specimens. Comparable to the topographic arrangement in males, there is a bilateral organization of the ganglia comprising the aortic plexus in females. More specifically, the left and right ovarian ganglia were positioned in close relation to their respective ovarian artery, whereas the prehypogastric ganglion was positioned within the right cord of the aortic plexus, contralateral to the inferior mesenteric ganglion. Using immunohistochemistry, it was shown that all ganglia from the fresh cadaver stained positive for tyrosine hydroxylase, thereby confirming their sympathetic nature. Having provided the first topographical and histological characterization of the ovarian and prehypogastric ganglia in females, future studies should seek to determine their specific function.

Keywords: aortic plexus, comparative anatomy, inferior mesenteric ganglion, intermesenteric plexus, lumbar splanchnic nerve, ovarian ganglion, prehypogastric ganglion, superior hypogastric plexus

Introduction

The aortic plexus is a complex network of sympathetic nerves overlying the infrarenal abdominal aorta containing significant innervation to the hindgut and pelvic organs. In males, disruption of the aortic plexus during retroperitoneal surgery is commonly associated with loss of antegrade ejaculation, and thus fertility (Flynn & Price, 1984; Jewett et al. 1988; Jewett & Groll, 2007; Katz & Eggener, 2009; Veroux et al. 2010; Heidenreich & Pfister, 2012; Hsiao et al. 2012). Although nerve‐sparing surgical procedures are currently recommended, the normal anatomy of the aortic plexus and its ganglia have not been described in significant detail. Motivated by this, our group recently published the first detailed anatomical description of the aortic plexus and its ganglia in human males through dissection, followed by a histological examination of fresh frozen cadavers (Beveridge et al. 2015). Importantly, our study characterized the prehypogastric ganglion, a novel structure which we suggested could be the right‐sided equivalent of the well‐acknowledged inferior mesenteric ganglion. Ultimately, characterization of the prehypogastric ganglion revealed that the topography of the aortic plexus in males is bilaterally symmetrical, organized around the four constituent prevertebral ganglia (left/right spermatic ganglia, prehypogastric ganglion, and inferior mesenteric ganglion) as seen in Fig. 1 (Beveridge et al. 2015). These findings contrast the classical characterization of the aortic plexus as a variable, convoluted network of nerves (Kuntz, 1945; Spalteholz, 1967; Hollinshead, 1974; Mirilas & Skandalakis, 2010; Netter, 2011).

Figure 1.

Figure 1

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Adapted from Beveridge et al. (2015), this illustration schematically demonstrates the organization of the human aortic plexus around the four constituent ganglia: the right/left spermatic (ovarian ♀) ganglia, prehypogastric ganglion and the inferior mesenteric ganglion. It is important to note that this bilateral arrangement around the four ganglia of the aortic plexus has only ever been demonstrated in males. This study aims to examine the homologous ganglia, if present, in females.

Because our previous study only examined males, it remains uncertain whether females also exhibit the newly described prehypogastric ganglion. Moreover, although the existence of the inferior mesenteric ganglion in females is well‐established (Jänig & McLachlan, 1987; Choi & Novembre, 1999), the current literature does not contain any primary reports of homologous structures to the male spermatic ganglia in humans. Although the existence of ovarian ganglia has been alluded to in two classical human anatomy textbooks (Kuntz, 1945; Crosby et al. 1962), to our knowledge the only scientific investigations demonstrating these structures were conducted on pigs, cats and rats (Langley & Anderson, 1896; McNeill & Burden, 1986; Klein & Burden, 1988a,b; Czaja et al. 2001).

Therefore, through gross cadaveric dissection and histological tissue verification, the present study investigated in females the possible existence of: (1) a prehypogastric ganglion as the right‐sided equivalent structure to the inferior mesenteric ganglion, and (2) ovarian ganglia as homologous structures to the left and right spermatic ganglia in males. Collectively, these results would confirm whether the aortic plexus in females exhibits a topographical arrangement of ganglia consistent with that of males (Fig. 1).

Materials and methods

In a population of 33 female cadavers (one fresh frozen, 32 embalmed; mean age = 78.2, SD = 12.5), the structures suspected to be the right ovarian, left ovarian and prehypogastric ganglia were dissected, and then excised for histological verification. Because the abdomen of the embalmed cadavers had been previously dissected by medical students at our institution, we excluded specimens where the complete aortic plexus was grossly over‐dissected (n = 1) or specific portions of the aortic plexus were damaged, in which case only ganglia from the regions that remained intact were examined (n = 6). All cadaveric specimens were acquired and dissected in accordance with the Anatomy Act of Ontario. The ganglia were identified during dissection within the left or right cords of the aortic plexus near the intersections of the infrarenal lumbar splanchnic nerves. Most commonly, the ganglia were identified as focal swellings or regions of nerve containing slightly darker matter, which has been suggested as a marker of neuron cell bodies likely due to the accumulation of lipofuscin (Beveridge et al. 2015). If no obvious ganglion was present, a small portion of tissue was excised from the expected location in case the ganglion was too small to be observed macroscopically.

To verify whether the acquired tissues were ganglia, 5‐μm sections were stained with Hematoxylin and Eosin (H&E) using standard regressive procedures, and then examined for the presence of neuron cell bodies. If no neuron cell bodies were observed, subsequent serial sections at varying depths were examined throughout the tissue. The specimens obtained from the single fresh, frozen cadaver were additionally used to verify the adrenergic nature of the neurons through staining with anti‐tyrosine hydroxylase antibody (anti‐TH) following a previously published protocol (Beveridge et al. 2015). Scaled micrographs were taken using a Zeiss AxioCam MRc microscope camera.

Results

Through dissection and examination of the 32 female cadavers included in this study, 26 had intact aortic plexuses and macroscopic identification of the left ovarian, right ovarian and prehypogastric ganglia was attempted. In the remaining six specimens, partial over‐dissection of the aortic plexus was present as a result of medical students' laboratory exercises at our institution. In these six cases, only the area of the aortic plexus which remained intact was examined. Collectively, tissue suspected to be the left ovarian ganglia (n = 31), right ovarian ganglia (n = 29) and prehypogastric ganglia (n = 28) were collected for histological examination with H&E staining to verify whether the obtained specimens truly contained neuron cell bodies and could thus be classified as ganglia.

Topography of the ganglia

In all of the specimens examined, the ovarian ganglia were located just inferior to the left renal vein, near the origin of the ovarian arteries. They were identified during dissection as the slightly enlarged portion of neural tissue near the junction of the intermesenteric nerve descending from the aorticorenal/superior mesenteric plexuses as it intersected with the first infrarenal lumbar splanchnic nerve. The prehypogastric ganglion was located at approximately the level of the inferior mesenteric artery, within the right cord of the aortic plexus – the same position as described in males. It was most easily identified by landmarking the position of the second infrarenal lumbar splanchnic nerve on the right side as it intersects the right cord of the aortic plexus. Figure 2 illustrates the position of the examined ganglia in situ during the dissection of the fresh cadaver.

Figure 2.

Figure 2

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A photograph of the aortic plexus taken from the left side of the body. The left cord of the aortic plexus is featured in the foreground, clearly illustrating the connections of the left ovarian and inferior mesenteric ganglia with that of the first and second infrarenal lumbar splanchnic nerves (LSN) extending from the sympathetic chain. In the background, the right cord of the aortic plexus is visible, with the prehypogastric ganglion identifiable. Given the perspective of the photo, the right ovarian ganglion is not clearly seen, but a label has been placed to illustrate the approximate location of the structure.

Histology of the ganglia

Abundant collections of neuron cell bodies (not uncommonly amounting to more than 100 neurons per histological section) were observed in all excised ovarian ganglia and 25/28 prehypogastric ganglia. The remaining 3/28 ‘prehypogastric ganglia’ were inconclusive in their histological examinations since they were not completely devoid of neuron cell bodies, yet they contained a notable lack of these cells compared with the other examined tissues. This distinction is shown in Fig. 3. Specifically, Fig. 3A demonstrates a typical micrograph from a tissue specimen confirmed to be a prehypogastric ganglion by the presence of satellite cells surrounding numerous neuron cell bodies with eccentrically placed nucleoli and abundant cytoplasmic lipofuscin. Alternatively, Fig. 3B demonstrates a micrograph of tissue which was not classified as being a prehypogastric ganglion due to the unusually low number of neuron cell bodies.

Figure 3.

Figure 3

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Panel A demonstrates histology from a typical prevertebral ganglion of the aortic plexus. Specifically, this is a photomerge of the prehypogastric ganglion from specimen #14. Panel B demonstrates a photomerge of the tissue thought to be a prehypogastric ganglion at the time of excision (Specimen #21); however, only nine neuron cell bodies were seen in this section clustered at the location indicated by the arrowhead. Neuron cell bodies were not observed in any other examined depths of the tissue.

The three inconclusive samples underwent subsequent sectioning to ensure the actual ganglionic portion of the tissue was not positioned at a different depth. By sectioning two to three slices at four different depths, approximately 40–50 neurons were observed in the first sample (Specimen 24C; Supporting Information Appendix S4), whereas a total of nine neurons were counted throughout the second sample (Specimen 21C; Appendix S3). In the last sample, sectioning at six different depths revealed a scant three neuron cell bodies in total (Specimen 20C; Appendix S3). Limited by the cremation of our specimens shortly after dissection, we were not able to revisit the cadavers to determine whether the low number of neuron cell bodies observed was an indication of (1) identification error during dissection, in that only a small portion of the prehypogastric ganglion was excised and the rest remained in situ, (2) an anatomical variation whereby the prehypogastric ganglion was truly not present in these specimens, but rather a microganglion was excised instead, or (3) some disease or process of aging had occurred, resulting in atrophy of the prehypogastric ganglion, leaving only a small minority of neurons. Given that the ovarian ganglia from these three cadavers appeared normal (see Specimens 20–21 & 24, columns A & B; Appendices S3,4), the third possibility is unlikely. Based on the histology, we suspect that the prehypogastric ganglion was incorrectly excised and only a piece of it was obtained, which explains why only a few neurons were present at the edge of the sectioned tissue. Nevertheless, we must acknowledge that we are not certain of this and the variable presence of the prehypogastric ganglion may still be a possibility. Therefore, given the drastically smaller number of neuron cell bodies in these three samples, it remains inconclusive whether these cadavers contained a prehypogastric ganglion. A summary of the complete histological examination is shown in Table 1. Photomicrographs of the ganglia from each specimen are provided in the Appendices S1–S5.

Table 1.

A summary of the results from the H&E staining used to verify the macroscopically identified ganglia. All excised specimens were microscopically confirmed to be ganglia with the exception of three ‘prehypogastric ganglia’. No tissues were completely devoid of neuron cell bodies

Right ovarian ganglion Left ovarian ganglion Prehypogastric ganglion
No. excised (total) 29 31 28
No. confirmed as ganglia (abundant neuron cell bodies) 29 31 25
No. inconclusive (notable lack of neurons throughout the tissue) 0 0 3
No. devoid of neurons 0 0 0
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In the single fresh, frozen cadaver, subsequent staining on the left ovarian, right ovarian and prehypogastric ganglia were immunopositive for tyrosine hydroxylase, thereby confirming the cells were adrenergic sympathetic neurons (Fig. 4). Immunohistochemical staining of the inferior mesenteric ganglion from the same specimen is also shown, as it represents the positive control for the immunohistochemical experiment.

Figure 4.

Figure 4

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Immunohistochemical staining of the right/left ovarian and prehypogastric ganglia were positive for tyrosine hydroxylase, indicating the adrenergic nature of the constituent neurons. Staining of the inferior mesenteric ganglion was used as positive control tissue. Tissue‐specific negative controls (− ctrl), which underwent identical procedures save the application of the primary antibody, are also presented.

Discussion

In the present study, dissection and histological analysis of cadaveric specimens were used to identify the left ovarian, right ovarian and prehypogastric ganglia as constituent structures of the aortic plexus in human females. Consistent with previous scientific reports of ovarian ganglia in pigs, cats and rats (Langley & Anderson, 1896; McNeill & Burden, 1986; Klein & Burden, 1988a,b; Czaja et al. 2001), histological examination of the excised tissue obtained during dissection revealed that all examined specimens contained right (n = 29) and left (n = 31) ovarian ganglia in similar topographic locations as the spermatic ganglia in males (Motoc et al. 2010; Beveridge et al. 2015). Thus, the present study provides histological verification of the ovarian ganglia in humans, which to our knowledge had only been alluded to in two classical textbooks (Kuntz, 1945; Crosby et al. 1962). In rats, it was shown that the nerves of the ovarian ganglia and plexuses mainly innervate the vasculature of the ovary. This is in contrast to the fibers coming from the celiac plexus via the superior ovarian nerve which innervate both ovarian vasculature and interstitial tissue (Lawrence & Burden, 1980; Aguado, 2002). Furthermore, it has been suspected that visceral afferent fibers traveling via the ovarian plexuses account for the intermenstrual pain (Mittelschmerz) some women associate with ovulation (Davidson, 1934; Crosby et al. 1962). More recently, Czaja et al. (2001) identified a major population of sympathetic neurons in the ovarian ganglia of pigs which innervate the ipsilateral ampulla and isthmus of the oviduct. Although the purpose of the sympathetic innervation from the ovarian ganglia to the oviduct remains unknown, a possible vasoconstrictive role and/or a role in smooth muscle contraction is likely.

In addition, the present study revealed using histology that the vast majority (25/28) of cadavers had a prehypogastric ganglion. Importantly, these findings provide the first reported evidence of the prehypogastric ganglion in females. In each cadaver, the prehypogastric ganglion was positioned in the same position as demonstrated in males (Beveridge et al. 2015). Taken together, these results confirm that the recently discovered prehypogastric ganglion is a consistent structure of the human aortic plexus.

Collectively, our results demonstrate that female cadavers exhibit ovarian and prehypogastric ganglia in positions that are consistent with that of the homologous structures in males (Motoc et al. 2010; Beveridge et al. 2015); findings which further confirm that the aortic plexus is organized in a bilaterally symmetrical manner. Given the demonstrated symmetry of the four ganglia of the aortic plexus in males and now females (as schematized in Fig. 1), one could ask whether the prehypogastric ganglion is in fact the right‐sided developmental equivalent structure to the inferior mesenteric ganglion because of its chiral anatomy within the contralateral (right) cord of the aortic plexus. Although it is generally accepted that humans possess one well‐defined inferior mesenteric ganglion (Jänig & McLachlan, 1987) with the possibility of variable accessory inferior mesenteric ganglia (Kuntz & Jacobs, 1955; O'Rahilly, 1986; Beveridge et al. 2015), dissection and histological examination of the inferior mesenteric plexus of human fetuses revealed the possibility of two well‐defined inferior mesenteric ganglia, supplied by the respective right and left lumbar splanchnic nerves (Fig. 4 in Southam, 1959). Based on Southam's (1959) developmental observations, it is reasonable to suggest that a right and left inferior mesenteric ganglion could develop in humans, with the former becoming what we have identified as the prehypogastric ganglion in the adult and the latter becoming the inferior mesenteric ganglion proper.

Considering the possibility that the prehypogastric ganglion develops from the fetal right inferior mesenteric ganglion, the anatomy of the human aortic plexus becomes congruent with the known anatomy of other species such as the cat, guinea pig, rabbit, dog (Jänig & McLachlan, 1987) and pig, where it is generally accepted that a right‐ and a left‐sided inferior mesenteric ganglion exist in both male (Kaleczyc et al. 1995; Ragionieri et al. 2013; Pidsudko, 2014) and female adults (Majewski & Heym, 1991). In the context of this comparative anatomy, it appears that the prehypogastric ganglion and the inferior mesenteric ganglion proper of humans are equivalent to the right and left inferior mesenteric ganglia of other mammals, respectively. Although a clear similarity in these ganglia exists across species, the differences in the current nomenclature importantly acknowledges the topographical and morphological differences in their anatomy. Conventionally, the nomenclature of the prevertebral ganglia are given according to the plexus to which they are associated (O'Rahilly, 1986), thus, the nomenclature of the prehypogastric ganglion describes its anatomy distinct from the inferior mesenteric artery (Fig. 2) with seemingly more significant communications with the superior hypogastric plexus (Beveridge et al. 2015). This is in contrast to the anatomy of the left and right inferior mesenteric ganglia of non‐primate mammals, such as the pig, where it is well established that they are positioned bilaterally, immediately adjacent to the inferior mesenteric artery (Kaleczyc et al. 1995; Pidsudko, 2014) in an orientation resembling the anatomy of the bi‐lobed celiac ganglia positioned around the base of the celiac artery in humans (see Plate 302 in Netter, 2011; Figure 1136 in Dwight et al. 1930). Ultimately, the anatomical distinction of the prehypogastric ganglion from the inferior mesenteric ganglion is of importance for surgeons tasked with navigating the intricacies of the aortic plexus during retroperitoneal procedures; especially since the function of the prehypogastric ganglion remains unclear.

In the original description of the prehypogastric ganglion in males, our group hypothesized it might be a structure which, if damaged, results in anejaculation because of its apparent contribution to the superior hypogastric plexus and potential risk for surgical damage due to its position distinct from arterial branches of the aorta (Beveridge et al. 2015). Given that anejaculation is characterized by a loss of seminal emission, it appears unlikely that this would be the sole function of a structure that has now been identified in females. Rather, our revised suggestion is that the prehypogastric ganglion is instead and/or additionally responsible for contraction of the internal urethral sphincter, a function common to both sexes. This hypothesis is particularly compelling since contraction of the internal urethral sphincter functions in both sexes to retain urine in the bladder; however, it is also imperative for antegrade ejaculation in males (Jung et al. 2012).

In conclusion, the present study provides histological verification of the left ovarian, right ovarian and prehypogastric ganglia in females. Although several suggestions about the possible role of these ganglia have been proposed based on their anatomy, it is important to note that their exact purpose, particularly in humans, remains unknown. Ultimately, future studies are needed to elucidate the specific function(s) of the ovarian and prehypogastric ganglia in humans.

Author contributions

T.S.B.: study conception; data acquisition and analysis; illustrations. T.S.B. and B.L.A.: data interpretation, writing and critical revision of the manuscript. All authors contributed to the overall study design as well as providing edits and approval of the final version of the manuscript.

Supporting information

Appendix S1–S5. A compilation of photomicrographs showing the histology with H&E of all examined tissues in the study. Columns A, B and C show histology from the left ovarian ganglia, right ovarian ganglia and prehypogastric ganglia, respectively.

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Acknowledgements

The authors would like to thank: the donors and their families, because this research would not be possible without their generosity; the supervisors of the HAASE anatomy lab at Western University, Haley Linklater and Kevin Walker, for their help with the cadaveric dissections; and, Linda Jackson from the Department of Pathology for her technical expertise in histology. The authors have no conflict of interest with the content of the manuscript.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Appendix S1–S5. A compilation of photomicrographs showing the histology with H&E of all examined tissues in the study. Columns A, B and C show histology from the left ovarian ganglia, right ovarian ganglia and prehypogastric ganglia, respectively.

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Click here for additional data file. (8.4MB, jpg)

 

Click here for additional data file. (4.9MB, jpg)

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