The primordia of the sympathetic trunk ganglia were traced on serial sections
of 10 embryos at stage 13 (32 postovulatory days). It was found that in all
embryos, these primordia were present in the thoracic level T4 to T9 and they
appeared as scattered aggregates of cells lying dorsally and laterally to the
dorsal aortae

Grzymisławska, M.

Woźniak, W.

Łupicka, J.

English

Via Medica Journals

Folia Morphol. Vol. 68, No. 4, pp. 215–217Copyright © 2009 Via MedicaISSN 0015–5659www.fm.viamedica.plO R I G I N A L   A R T I C L E215Address for correspondence: Prof. W. Woźniak, Department of Anatomy, Poznań University of Medical Sciences, Święcickiego 6,60–781 Poznań, Poland, tel: +48 61 854 65 64, fax: +48 61 854 65 68, e-mail wwozniak@ump.edu.plThe first appearance of sympatheticganglia in human embryos at stage 13W. Woźniak, M. Grzymisławska, J. ŁupickaDepartment of Anatomy, Poznań University of Medical Sciences, Poznań, Poland[Received 14 July 2009; Accepted 30 September 2009]The primordia of the sympathetic trunk ganglia were traced on serial sectionsof 10 embryos at stage 13 (32 postovulatory days). It was found that in allembryos, these primordia were present in the thoracic level T4 to T9 and theyappeared as scattered aggregates of cells lying dorsally and laterally to thedorsal aortae. (Folia Morphol 2009; 68, 4: 215–217)Key words: human neuroembryology, autonomic nervous system,sympathetic gangliaINTRODUCTIONThe development of the sympathetic nervoussystem can be divided into three overlapping stag-es [6]. First, the precursors of sympathetic neu-rons arise from neural crest cells that migrate ven-trally, aggregate adjacent to the dorsal aorta, andultimately differentiate into catecholaminergicneurons. Second, the cell number is refined whenneurotrophic factors determine the number of neu-rons. The final stage of the sympathetic develop-ment is the establishment and maturation of sym-pathetic connections.The primordia of the sympathetic ganglia appearbefore the fibres of the communicating rami can betraced into them and before formation of the sym-pathetic trunk [13]. According to Mitchell [16], ag-gregation of cells, representing the primordia of thefuture ganglia of the sympathetic trunk, are firstevident in the lower thoracic and upper lumbar re-gions, and they are located on the posterolateralaspects of the aorta. Such aggregations of primor-dial cells are arranged initially in an ill-defined col-umn, and in embryos at the 15 mm stage, they arepresent in all except the cervical region.Kuntz [12] stated that aggregates of cells maybe observed from the caudal cervical to the sacralregion in human embryos 6 mm in length.Pearson and Eckhard [19] found white commu-nicating rami in embryos 6.0–6.5 mm in length.It has to be pointed out that the embryonic ageshould be expressed in developmental stages whichare based on the morphological status of develop-ment. Embryos of 6.0 mm in length may belong todifferent stages [17, 18].The aim of the present study is to trace the earlyformation of the sympathetic ganglia in humanembryos at stage 13.MATERIAL AND METHODSSerial sections of 10 embryos at stage 13(32 postovulatory days) from the Collection of theDepartment of Anatomy, Poznań University of Medi-cal Sciences were studied (Table 1).Coronal, sagittal, and horizontal sections stainedwith haematoxylin and eosin, cresyl violet, accord-ing to the Mallory method, and impregnated withsilver were examined microscopically. The roots ofthe spinal cord and the spinal nerves were carefullytraced and the positions of the sympathetic gangliawere evaluated.RESULTSIn all investigated embryos, the division of scle-rotomes into loose superior and dense inferior zones216Folia Morphol., 2009, Vol. 68, No. 4is observed (Fig. 1). The spinal ganglia are not yetsegregated and the spinal neural crest extends onthe dorsolateral surface of the spinal cord. The spi-nal nerves are already formed and the thick anteriorbranch of these nerves is evident (Fig. 2).The primordia of the sympathetic ganglia arecomposed of scattered cells which are larger thancells of the mesenchyme, and show more intensestaining reaction (Figs. 1, 2). Such aggregates of cellsare found in the thoracic levels T4–T9. They lie alongthe dorsolateral aspects of dorsal aortae. Cells inthese primordia are identical to cells of the spinalganglia. At this stage of development, there are nocommunicating rami.DISCUSSIONPostganglionic sympathetic neurons arise fromthe neural crest, which migrate ventrally from thedorsal surface of the neural tube. Neural crest cellsdevelop at the interface between the non-neuralectoderm (presumptive epidermis/ surface ectoderm)and the dorsal region of the neural plate, a regioncommonly referred to as the neural plate border [3].The sympathetic primordia are near the dorsal aor-tae [7]. Several factors play a role in early develop-ment of the sympathetic ganglia [1, 2, 4, 8–11, 20].The sympathetic trunk and plexuses are madeup of cells that originate from the entire length ofthe neural crest located behind the level of the fifthsomite [14, 15, 18].According to Anderson [1], both catecholamin-ergic neural crest derivatives: adrenal chromaffin cellsand sympathetic neurons, derive from a commonsympathoadrenal progenitor.Table 1. CR length, developmental stage, and postovulatory days of investigated embryosCatalogue number CR length [mm] Developmental stage Age [days] Plane of sectionB171 5.0 13 32 HorizontalB174 4.5 13 32 HorizontalB194 6.0 13 32 HorizontalB202 4.5 13 32 HorizontalB206 5.5 13 32 HorizontalB207 6.0 13 32 FrontalB208 5.5 13 32 FrontalB209 5.0 13 32 HorizontalB218 5.5 13 32 HorizontalI 5.5 13 32 SagittalFigure 2. Horizontal section of embryo at the level of the mainbronchi. Stained with cresyl violet, ¥ 40; a — spinal nerve,b — sympathetic ganglia, c — dorsal aortae, d — oesophagus,e — main bronchus, f — anterior ramus of the spinal nerve.Figure 1. Sagittal section of embryo. Impregnation with Bodian’sprotargol, ¥ 100; a — sympathetic ganglia, b — loose zone ofsclerotome, c — dense zone of sclerotome, d — dorsal aorta,e — spinal cord.217W. Woźniak et al., Development of sympathetic gangliaThe dorsal aorta and notochord regulate the com-mitment to and expression of cell fate by the neuralcrest that settle there. Dorsal aorta and neural tubesinduce noradrenergic traits in neural crest cultures,and adrenergic properties are not expressed in thesympathetic ganglia of notochord-ablated chickenembryos [5].The dorsal aorta-derived factor involves one or moreof the members of the BMP family, which increaseTH expression in migrating neural crest cells [6].The present study revealed that the primordiaof the sympathetic ganglia appear very early inthe thoracic part of the sympathetic trunk. Theyprecede the formation of the communicatingrami. The sympathetic ganglia are related to thedorsal aortae and sclerotomes surrounding thenotochord.Our results are not in accordance with the find-ings of Kuntz [12], who observed such primordia inthe lower thoracic and upper lumbar region. Accord-ing to Kuntz [12], the primordia of the sympathetictrunks grow cranially from the lower cervical region,both by displacement of cells along the dorsal as-pect of the aortae and by local cell division.Streeter [21], investigating nervous system inthe human embryo at the end of the first month(10 mm), found that the neural crest cells destinedto become sympathetic ganglion cells fused togetheron each side of the body to form a longitudinal col-umn situated lateral to the aorta and in front of thedeveloping vertebral bodies.Such an appearance of the sympathetic trunks isobserved in the later stages of development duringthe second month.REFERENCES1. Anderson DJ (2000) Genes, lineages and the neuralcrest: a speculative review. Philos Trans R Soc London BBiol Sci, 355: 953–964.2. Coughlin MD, Dibner MD, Boyer DM, Black JB (1978)Factors regulating development of an embryonic mousesympathetic ganglion. Dev Biol, 66: 513–528.3. Crane JF, Trainor PA (2006) Neural crest stem and pro-genitor cells. Annu Rev Cell Dev Biol, 22: 267–286.4. Ernsberger U (2001) The development of postganglio-nic sympathetic neurons: coordinating neuronal differ-entiation and diversification. Auton Neurosci, 94: 1–13.5. Ernsberger U, Roher H (1996) The development of thenoradrenergic transmitter phenotype in postganglio-noc sympathetic neurons. Neurochem Res, 21: 823–829.6. Francis NJ, Landis SC (1999) Cellular and molecular de-terminants of sympathetic neuron development. AnnuRev Neurosci, 22: 541–566.7. Glebova NO, Ginty DD (2005) Growth and survival sig-nals controlling sympathetic nervous system develop-ment. Annu Rev Neurosci, 28: 191–222.8. Groves AK, George KM, Tissier-Seta J-P, Engel JD,Brunet J-F, Anderson DJ (1995) Differential regulationof transcription factor gene expression and phenotyp-ic markers in developing sympathetic neurons. Deve-lopment, 121: 887–901.9. Hall AK, MacPhedran SE (1995) Multiple mechanismsregulate sympathetic neuronal phenotype. Develop-ment, 121: 2361–2371.10. Howard MJ (2005) Mechanisms and perspectives ondifferentiation of autonomic neurons. Dev Biol, 277:271–286.11. Huang EJ, Reichardt LF (2001) Neurotrophins: roles inneuronal development and function. Annu Rev Neuro-sci, 24: 677–736.12. Kuntz A (1920) The development of the sympatheticnervous system in man. J Comp Neurol, 32: 173–229.13. Kuntz A (1953) The autonomic nervous system. Lea andFebiger, Philadelphia.14. Le Douarin NM, Smith J (1988) Development of theperipheral nervous system from the neural crest. AnnuRev Cell Biol, 4: 375–404.15. Markmam JA, Vaughn JE (1991) Patterns of sympatheticpreganglionic neuronal migration in spinal cord ofembryonic rats. Soc Neurosci, 17: 206.16. Mitchell GAG (1953) Anatomy of the autonomic ner-vous system. Livingstone LTD, Edinburgh, London.17. O’Rahilly R, Müller F (2003) Somites, spinal ganglia,and centra. Cells Tissues Organs, 173: 75–92.18. O’Rahilly R, Müller F (2007) The development of theneural crest in the human. J Anat, 211: 335–351.19. Pearson AA, Eckhard AL (1960) Observations on thegray and white rami communicantes in human embryos.Anat Rec, 138: 115–127.20. Sommer L, Shah N, Rao M, Anderson DJ (1995) Thecellular function of MASH1 in autonomic neurogene-sis. Neuron, 15: 1245–1258.21. Streeter GL (1908) The peripheral nervous system inthe human embryo at the end of the first month(10 mm). Amer J Anat, 8: 285–301.

The first appearance of sympathetic ganglia in human embryos at stage 13

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The first appearance of sympathetic ganglia in human embryos at stage 13

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