Microstructure of the nerve plexus of the muscular membrane of the gut of domestic ducks (Anas platyrhynchos domesticus) of different ages

  • М. М. Kushch Kharkiv State Zooveterinary Academy
  • D. S. Makhotyna Kharkiv State Zooveterinary Academy
  • I. A. Fesenko Kharkiv State Zooveterinary Academy
  • M. M. Savenko Kharkiv State Zooveterinary Academy
  • A. Y. Ulianytska Kharkiv State Zooveterinary Academy
Keywords: birds; intestine; ontogenesis; histologic structure; enteric nervous system; myenteric nervous plexus; neurons.

Abstract

As evidenced by the publications of recent years, contrary to the existing dogma about the immutability of the state of the enteric nervous system during the postnatal period of ontogenesis, the population of intestinal neurons is a dynamic formation, decreasing with age and changing due to the action of environmental factors. The current article presents the results of study of the microscopic structure of the nerve plexus of the muscular membrane of the enteric nervous system of domestic ducks (Anas platyrhynchos domesticus) of the black white–breasted breed, of nine age groups of 1–365 days of age. The topography, number, area of nerve nodes, as well as the density of neurons in them were determined on transverse sections of the duodenum, jejunum, ileum, caecum and rectum. For the purpose of a generalized assessment of the morphofunctional state of the nerve plexuses, two parameters were determined: the average age indicator of the gut and intestines. The average age indicator of a certain structure of each intestine was determined as the arithmetical average of its nine age indicators. The average age indicator of a certain gut structure was determined as the arithmetic average of the average age indicator of the structure of all five intestines. It has been established that the nerve plexus of the muscular membrane (myenteric, plexus Auerbachi) of the gut of domestic ducks, in contrast to mammals, is not located between the layers of the muscular membrane, but in its outer layer. On a transverse section of the gut wall, the myenteric ganglia and cords that connect have a predominantly elliptical shape. Despite a significant increase with age in the diameter and thickness of the gut wall, the total number of myenteric ganglia changed little, increasing or decreasing with varying degrees of reliability relative to the previous age. In the gut of ducks, during the first year of the postnatal period of ontogenesis, the smallest number of myenteric ganglia was found in the cecum, and the largest – in the ileum. The general pattern of the dynamics of the size of the myenteric ganglia of the gut of ducks was an increase in their area with age. Moreover, this indicator reached the greatest value at different ages of ducks: at 30 days of age in the ileum and cecum, at 180 days of age – in the rectum and at 365 days of age – in the duodenum. The smallest area of the myenteric ganglia was found in the jejunum, and the largest – in the duodenum and ileum. The smallest number of neurons in the ganglion was found in the cecum, and the largest – in the rectum, the lowest density of neurons in the ganglion was found in the cecum, and the largest – in the jejunum. The general quantitative pattern of neurons in the ganglion was the decrease in their density with age. Changes in the morphometric parameters of the ganglia of the nerve plexus of the muscular membrane of the ducks’ gut indicate the plasticity of the enteric nervous system, its ability to dynamically respond to the action of factors of the internal and external environment. It is promising to study the state of the submucous nerve plexus, as well as the cellular composition of the population of neurons of the enteric nervous system of domestic and wild poultry.

References

Aisa, J., Parra, P., & Azanza, M. J. (1990). Ultrastructural characteristics of anterior gut innervation of Gallus gallus. Histology and Histopathology, 5(3), 281–287.

Ali, H. A., & McLelland, J. (1978). Avian enteric nerve plexuses. A histochemical study. Cell and Tissue Research, 189(3), 537–548.

Amaral, P. F. G. P., Santos, G. R., Urano, T. K., Diniz, K. da S., Gonçalves, T. dos S. A., Serenini, G. de F., Otutumi, L. K., & Germano, R. de M. (2010). Salmonella heidelberg reduces nitrergic neurons in the myenteric plexus of the duodenum of broilers. African Journal of Microbiology Research, 11(33), 1315–1320.

Ameku, T., Beckwith, H., Blackie, L., & Miguel-Aliaga, L. (2020). Food, microbes, sex and old age: On the plasticity of gastrointestinal innervation. Current Opi-nion in Neurobiology, 62, 83–91.

Bor-Seng-Shu, E., Chadi, G., Bor-Jiun-Shu, F., Ferraz-de-Carvalho, C. A., & de-Souza, R. R. (1994). Myenteric neurons of the mouse small intestine. Morphometry and acetylcholinesterase activity. Brazilian Journal of Medical and Biological Research, 27(1), 101–108.

Burns, A. J., & Thapar, N. (2006). Advances in ontogeny of the enteric nervous system. Journal of Neurogastroenterology and Motility, 18(10), 876–887.

De Souza, R. R., Moratelli, H. B., Borges, N., & Liberti, E. A. (1993). Age-induced nerve cell loss in the myenteric plexus of the small intestine in man. Gerontology, 39(4), 183–188.

Faller, A., Schuenke, M., & Schuenke, G. M. (2004). The human body. Stuttgart, NewYork, Thieme.

Freem, L. J., Delalande, J. M., Campbell, A. M., Thapar, N., & Burns, A. J. (2012). Lack of organ specific commitment of vagal neural crest cell derivatives as shown by back-transplantation of GFP chicken tissues. The International Journal of Developmental Biology, 56(4), 245–254.

Gabella, G., & Halasy, K. (1987). On the nerve plexus of the chicken gizzard. Anatomy and Embryology, 177(2), 97–103.

Gonkowski, S., Gajęcka, M., & Makowska, K. (2020). Mycotoxins and the enteric nervous system. Toxins, 12(461), 1–28.

Ippolito, C., Segnani, C., De Giorgio, R., Blandizzi, C., Mattii, L., Castagna, M., Moscato, S., Dolfi, A., & Bernardini, N. (2009). Quantitative evaluation of myenteric ganglion cells in normal human left colon: Implications for histopathological analysis. Cell and Tissue Research, 336(2), 191–201.

Joseph, N. M., He, S., Quintana, E., Kim, Y., Núñez, G., & Morrison, S. J. (2011). Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. The Journal of Clinical Investigation, 121(9), 3398–3411.

Kabouridis, P. S., & Pachnis, V. (2015). Emerging roles of gut microbiota and the immune system in the development of the enteric nervous system. The Journal of Clinical Investigation, 125(3), 956–964.

Karaosmanoglu, T., Aygun, B., Wade, P. R., & Gershon, M. D. (1996). Regional differences in the number of neurons in the myenteric plexus of the guinea pig small intestine and colon: An evaluation of markers used to count neurons. The Anatomical Record, 244(4), 470–480.

Kuder, T., Nowak, E., Szczurkowski, A., & Kuchinka, J. (2003). The comparative analysis of the myenteric plexus in pigeon and hen. Comparative study. Anatomia, Histologia, Embryologia, 32(1), 1–5.

Kulkarni, S., Ganz, J., Bayrer, J., Becker, L., Bogunovic, M., & Rao, M. (2018). Advances in enteric neurobiology: The “brain” in the gut in health and disease. Journal of Neuroscience, 38(44), 9346–9354.

Kulkarni, S., Micci, M.-A., Leser, J., Shin, C., Tang, S.-C., Fu, Y.-Y., Liu, L., Li, Q., Saha, M., Li, C., Enikolopov, G., Becker, L., Rakhilin, N., Anderson, M., Shen, X., Dong, X., Butte, M. J., Song, H., Southard-Smith, E. M., Kapur, R. P., Bogunovic, M., & Pasricha, P. J. (2017). Neurogenesis and turnover of adult enteric neurons. Proceedings of the National Academy of Sciences, 114(18), 3709–3718.

Kushch, M. M., Kushch, L. L., Byrka, E. V., Byrka, V. V., & Yaremchuk, O. S. (2019). Morphological features of the jejunum and ileum of the middle and heavy goose breeds. Ukrainian Journal of Ecology, 9(4), 690–694.

Ling, I. T. C., & Sauka-Spengler, T. (2019). Early chromatin shaping predetermines multipotent vagal neural crest into neural, neuronal and mesenchymal lineages. Nature Cell Biology, 21(12), 1504–1517.

Logvinova, V. V., Oliyar, A. V., & Lieshchova, M. A. (2020). Formation of immune structures in small intestine of Muscovy ducks (Cairina moschata). Theoretical and Applied Veterinary Medicine, 8(1), 50–55.

Maifrino, L. B., Prates, J. C., De-Souza, R. R., & Liberti, E. A. (1997). Morphometry and acetylcholinesterase activity of the myenteric plexus of the wild mouse Calomys callosus. Brazilian Journal of Medical and Biological Research, 30(5), 627–632.

Mandić, P., Filipović, T., Gasić, M., Djukić-Macut, N., Filipović, M., & Bogosavljević, I. (2016). Quantitative morphometric analysis of the myenteric nervous plexus ganglion structures along the human digestive tract. Vojnosani-tetski Pregled, 73(6), 559–565.

Margolis, K. G., Gershon, M. D., & Bogunovic, M. (2016). Cellular organization of neuroimmune interactions in the gastrointestinal tract. Trends in Immunology, 37(7), 487–501.

Maruccio, L., Lucini, C., Russo, F., Antonucci, R., & Castaldo, L. (2008). The development of avian enteric nervous system: Distribution of artemin immunoreactivity. Acta Histochemica, 110(2), 163–171.

Mirabella, N., Squillacioti, C., Genovese, A., Germano, G., & Paino, G. (2003). Topography and neurochemistry of the enteric ganglion in the proventriculus of the duck (Anas platyrhynchos). Anatomy and Embryology, 207(2), 101–108.

Nagy, N., & Goldstein, A. M. (2017). Enteric nervous system development: A crest cell’s journey from neural tube to colon. Seminars in Cell and Developmental Biology, 66, 94–106.

Pawolski, V., & Schmidt, M. H. H. (2020). Neuron – glia interaction in the developing and adult enteric nervous system. Cells, 10(1), 47.

Phillips, R. J., Kieffer, E. J., & Powley, T. L. (2004). Loss of glia and neurons in the myenteric plexus of the aged Fischer 344 rat. Anatomy and Embryology, 209(1), 19–30.

Phillips, R. J., Rhodes, B. S., & Powley, T. L. (2006). Effects of age on sympathetic innervation of the myenteric plexus and gastrointestinal smooth muscle of Fischer 344 rats. Anatomy and Embryology, 211(6), 673–683.

Popov, J., Bandura, J., Markovic, F., Borojevic, R., Anipindi, V. C., Pai, N., & Ratcliffe, E. M. (2020). Influence of bacterial components on the developmental programming of enteric neurons. Physiological Reports, 8(21), e14611.

Román, V., Krecsmarik, M., Bagyánszki, M., & Fekete, E. (2001). Evaluation of the total number of myenteric neurons in the developing chicken gut using cuprolinic blue histochemical staining and neurofilament immunocytochemistry. Histochemistry and Cell Biology, 116(3), 241–246.

Santer, R. M., & Baker, D. M. (1988). Enteric neuron numbers and sizes in Auerbach’s plexus in the small and large intestine of adult and aged rats. Journal of the Autonomic Nervous System, 25(1), 59–67.

Spencer, N. J., & Hu, H. (2020). Enteric nervous system: Sensory transduction, neural circuits and gastrointestinal motility. Nature Reviews Gastroenterology and Hepatology, 17(6), 338–351.

Timmermans, J. P., Hens, J., & Adriaensen, D. (2001). Outer submucous plexus: An intrinsic nerve network involved in both secretory and motility processes in the intestine of large mammals and humans. The Anatomical Record, 262(1), 71–78.

Wester, T., O’Briain, D. S., & Puri, P. (1999). Notable postnatal alterations in the myenteric plexus of normal human bowel. Gut, 44(5), 666–674.

Xiao, J., Neylon, C. B., Hunne, B., & Furness, J. B. (2003). Oligophrenin-1, a Rho GTPase-activating protein (RhoGAP) involved in X-linked mental retardation, is expressed in the enteric nervous system. The Anatomical Record, 273A(2), 671–676.

Yang, P., Gandahi, J. A., Zhang, Q., Zhang, L., Bian, X., Wu, L., Liu, Y., & Chen, Q. (2013). Quantitative changes of nitrergic neurons during postnatal development of chicken myenteric plexus. Journal of Zhejiang University – Science B, 14(10), 886–895.

Yu, Y., Daly, D. M., Adam, I. J., Kitsanta, P., Hill, C. J., Wild, J., Shorthouse, A., Grundy, D., & Jiang, W. (2016). Interplay between mast cells, enterochromaffin cells, and sensory signaling in the aging human bowel. Journal of Neurogastroenterology and Motility, 28(10), 1465–1479.

Zanesco, M. C., & de Souza, R. R. (2011). Morphoquantitative study of the submucous plexus (of Meissner) of the jejunumileum of young and old guinea pigs. Arquivos de Neuro-Psiquiatria, 69(1), 85–90.

Zhang, D., Rollo, B. N., Nagy, N., Stamp, L., & Newgreen, D. F. (2019). The enteric neural crest progressively loses capacity to form enteric nervous system. Developmental Biology, 446(1), 34–42.

Published
2021-02-15
How to Cite
KushchМ. М., Makhotyna, D. S., Fesenko, I. A., Savenko, M. M., & Ulianytska, A. Y. (2021). Microstructure of the nerve plexus of the muscular membrane of the gut of domestic ducks (Anas platyrhynchos domesticus) of different ages . Regulatory Mechanisms in Biosystems, 12(1), 3-8. https://doi.org/10.15421/022101

Most read articles by the same author(s)