Three-dimensional organization of the brain and distribution of serotonin in the brain and ovary, and its effects on ovarian steroidogenesis in the giant freshwater prawn, Macrobrachium rosenbergii
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The giant freshwater prawn, Macrobrachium rosenbergii, is an economically important crustacean species which has also been extensively used as a model in neuroscience research. The crustacean central nervous system is a highly complex structure, especially the brain. However, little information is available on the brain structure, especially the three-dimensional organization. In this study, we demonstrated the three-dimensional structure and histology of the brain of M. rosenbergii together with the distribution of serotonin (5-HT) in the brain and ovary as well as its effects on ovarian steroidogenesis. The brain of M. rosenbergii consists of three parts: protocerebrum, deutocerebrum and tritocerebrum. Histologically, protocerebrum comprises of neuronal clusters 6–8 and prominent anterior and posterior medial protocerebral neuropils (AMPN/PMPN). The protocerebrum is connected posteriorly to the deutocerebrum which consists of neuronal clusters 9–13, medial antenna I neuropil, a paired lateral antenna I neuropils and olfactory neuropils (ON). Tritocerebrum comprises of neuronal clusters 14–17 with prominent pairs of antenna II (AnN), tegumentary and columnar neuropils (CN). All neuronal clusters are paired structures except numbers 7, 13 and 17 which are single clusters located at the median zone. These neuronal clusters and neuropils are clearly shown in three-dimensional structure of the brain. 5-HT immunoreactivity (-ir) was mostly detected in the medium-sized neurons and neuronal fibers of clusters 6/7, 8, 9, 10 and 14/15 and in many neuropils of the brain including anterior/posterior medial protocerebral neuropils (AMPN/PMPN), protocerebral tract, protocerebral bridge, central body, olfactory neuropil (ON), antennal II neuropil (Ann) and columnar neuropil (CN). In the ovary, the 5-HT-ir was light in the oocyte step 1(Oc1) and very intense in Oc2–Oc4. Using an in vitro assay of an explant of mature ovary, it was shown that 5-HT was able to enhance ovarian estradiol-17β (E2) and progesterone (P4) secretions. We suggest that 5-HT is specifically localized in specific brain areas and ovary of this prawn and it plays a pivotal role in ovarian maturation via the induction of female sex steroid secretions, in turn these steroids may enhance vitellogenesis resulting in oocyte growth and maturation.
KeywordsBrain Three-dimensional organization Histology Serotonin Macrobrachium rosenbergii Steroid release
This work is financially supported by a Distinguished Research Professor Grant (co-funded by the Thailand Research Fund, The Commission on Higher Education and Mahidol University) to Prof. Prasert Sobhon and Prof. Prapee Sretarugsa; Scholarship from M.D., Ph.D. Program, Mahidol University to Boworn Soonthornsumrith.
Compliance with ethical standards
Conflict of interest
We declare that this work has no conflict of interest.
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- Edwards DH Drummond JM (1998) Effect of social experience on reflex responses of serotonergic neurons in crayfish. Fifth international congress of neuroethology abstract, vol 208Google Scholar
- Kruangkum T, Chotwiwatthanakun C, Vanichviriyakit R, Tinikul Y, Anuracpreeda P, Wanichanon C, Hanna PJ, Sobhon P (2013) Structure of the olfactory receptor organs, their GABAergic neural pathways, and modulation of mating behavior, in the giant freshwater prawn, Macrobrachium rosenbergii. Microsc Res Tech 76:572–587CrossRefPubMedGoogle Scholar
- Merlin J, Mohanlal DL, Balasubramanian CP, Sherly T, Subramoniam T, Syamadayal J, Ravichandran P, Ponniah AG, Gopal C, Vijayan KK (2015) Induction of vitellogenesis and reproductive maturation in tiger shrimp, Penaeus monodon by 17ß-estradiol and 17α-hydroxyprogesterone: in vivo and in vitro studies. Invertebr Reprod Dev 59:166–175CrossRefGoogle Scholar
- Parameswaran R (1956) Neurosecretory cells of the central nervous system of the crab, Paratelphusa hydrodromous. Q J Microsc Sci 97:75–82Google Scholar
- Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G, Stach T, Vogt L, Wanninger A, Brenneis G, Doring C, Faller S, Fritsch M, Grobe P, Heuer C, Kaul S, Moller O, Muller C, Rieger V, Rothe B, Stegner M, Harzsch S (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7:29CrossRefPubMedPubMedCentralGoogle Scholar
- Ruttanakorn S, Meeratana P, Chetawan K, Hanna P (2013) Induction of ovarian development and sex differentiation in the giant freshwater prawn Macrobrachium rosenbergii, by serotonin, methyl farnesoate, and phytoecdysone. J Sci Technol Hum 11:77–86Google Scholar
- Saetan J, Senarai T, Tamtin M, Weerachatyanukul W, Chavadej J, Hanna PJ, Parhar I, Sobhon P, Sretarugsa P (2013) Histological organization of the central nervous system and distribution of a gonadotropin-releasing hormone-like peptide in the blue crab, Portunus pelagicus. Cell Tissue Res 353:493–510CrossRefPubMedGoogle Scholar
- Sosa MA, Baro DJ (1999) Comparison of 5-HT receptor mRNA expression in the ventral nerve cord of the male morphotypes of the giant tropical freshwater prawn. Soc Neurosci Abstr 25:1704Google Scholar
- Thongbuakaew T, Saetan J, Suwansa-ard S, Kankoun W, Sumpownon C, Parhar I, Meeratana P, Sobhon P, Sretarugsa P (2016a) The existence of kisspeptin-like peptides and effects on ovarian development and maturation in the giant freshwater prawn, Macrobrachium rosenbergii. Aquaculture 455:50–60CrossRefGoogle Scholar
- Tinikul Y, Soonthornsumrith B, Phoungpetchara I, Meeratana P, Poljaroen J, Duangsuwan P, Soonklang N, Mercier AJ, Sobhon P (2009a) Effects of serotonin, dopamine, octopamine, and spiperone on ovarian maturation and embryonic development in the giant freshwater prawn, Macrobrachium rosenbergii (De Man, 1879). Crustaceana 82:1007–1022CrossRefGoogle Scholar
- Tinikul Y, Poljaroen J, Nuurai P, Anuracpreeda P, Chotwiwatthanakun C, Phoungpetchara I, Kornthong N, Poomtong T, Hanna PJ, Sobhon P (2011a) Existence and distribution of gonadotropin-releasing hormone-like peptides in the central nervous system and ovary in the Pacific white shrimp, Litopenaeus vannamei. Cell Tissue Res 343:579–593CrossRefPubMedGoogle Scholar
- Tinikul Y, Poljaroen J, Kornthong N, Chotwiwatthanakun C, Anuracpreeda P, Poomtong T, Hanna PJ, Sobhon P (2011b) Distribution and changes of serotonin and dopamine levels in the central nervous system and ovary of the Pacific white shrimp, Litopenaeus vannamei, during ovarian maturation cycle. Cell Tissue Res 345:103–124CrossRefPubMedGoogle Scholar
- Tsukimura B (2001) Crustacean vitellogenesis: its role in oocyte development. Am Zool 41:465–476Google Scholar