Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Invertebrate Neuroscience

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Antonsen BL, Paul DH (2001) Serotonergic and octopaminergic systems in the squat lobster Munida quadrispina (Anomura, Galatheidae). J Comp Neurol 439:450–468

    Article  PubMed  CAS  Google Scholar 

  • Beltz BS, Kravitz EA (1983) Mapping of serotonin-like immunoreactivity in the lobster nervous system. J Neurosci 3:585–602

    Article  PubMed  CAS  Google Scholar 

  • Coccia E, Lisa ED, Cristo CD, Cosmo AD, Paolucci M (2010) Effects of estradiol and progesterone on the reproduction of the freshwater crayfish Cherax albidus. Biol Bull 218:36–47

    Article  PubMed  CAS  Google Scholar 

  • Edwards DH Drummond JM (1998) Effect of social experience on reflex responses of serotonergic neurons in crayfish. Fifth international congress of neuroethology abstract, vol 208

  • Edwards DH, Kravitz EA (1997) Serotonin, social status and aggression. Curr Opin Neurobiol 7:812–819

    Article  PubMed  CAS  Google Scholar 

  • Elson R (1996) Neuroanatomy of a crayfish thoracic ganglion: sensory and motor roots of the walking-leg nerves and possible homologies with insects. J Comp Neurol 365:1–17

    Article  PubMed  CAS  Google Scholar 

  • Fairs N, Quinlan P, Goad L (1990) Changes in ovarian unconjugated and conjugated steroid titers during vitellogenesis in Penaeus monodon. Aquaculture 89:83–99

    Article  CAS  Google Scholar 

  • Fanenbruck M, Harzsch S, Wägele JW (2004) The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proc Natl Acad Sci USA 101:3868–3873

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ghosh D, Ray AK (1993) 17β-Hydroxysteroid dehydrogenase activity of ovary and hepato-pancreas of Macrobrachium rosenbergii: relation to ovarian condition and estrogen treatment. Gen Comp Endocrinol 89:248–254

    Article  PubMed  CAS  Google Scholar 

  • Glanzman DL, Krasne FB (1983) Serotonin and octopamine have opposite modulatory effects on the crayfish lateral giant escape reaction. J Neurosci 3:2263–2269

    Article  PubMed  CAS  Google Scholar 

  • Harris-Warrick RM, Kravitz EA (1984) Cellular mechanisms for modulation of posture by octopamine and serotonin in the lobster. J Neurosci 4:1976–1993

    Article  PubMed  CAS  Google Scholar 

  • Huber R, Panksepp JB, Yue Z, Delago A, Moore P (2001) Dynamic interactions of behavior and amine neurochemistry in acquisition and maintenance of social rank in crayfish. Brain Behav Evol 57:271–282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Khornchatri K, Kornthong N, Saetan J, Tinikul Y, Chotwiwatthanakun C, Cummins SF, Hanna PJ, Sobhon P (2015) Distribution of serotonin and dopamine in the central nervous system of the female mud crab, Scylla olivacea (Herbst). Acta Histochem 117:196–204

    Article  PubMed  CAS  Google 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 76:572–587

    Article  PubMed  CAS  Google Scholar 

  • Kulkarni GK, Nagabhushanam R, Amaldoss G, Jaiswal RG, Fingerman M (1992) In vivo stimulation of ovarian development in the red swamp crayfish, Procambarus clarkii (Girard), by 5-hydroxytryptamine. Invertebr Reprod Dev 21:231–240

    Article  CAS  Google Scholar 

  • Ma PM, Beltz BS, Kravitz EA (1992) Serotonin-containing neurons in lobsters: their role as gain-setters in postural control mechanisms. J Neurophysiol 68:36–54

    Article  PubMed  CAS  Google Scholar 

  • Meeratana P, Sobhon P (2007) Classification of differentiating oocytes during ovarian cycle in the giant freshwater prawn, Macrobrachium rosenbergii De Man. Aquaculture 270:249–258

    Article  Google Scholar 

  • Meeratana P, Withyachumnarnkul B, Damrongphol P, Wongprasert K, Suseangtham A, Sobhon P (2006) Serotonin induces ovarian maturation in giant freshwater prawn broodstock, Macrobrachium rosenbergii de Man. Aquaculture 260:315–325

    Article  CAS  Google 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 59:166–175

    Article  CAS  Google Scholar 

  • Moreau X, Benzid D, De Jong L, Barthélémy RM, Casanova JP (2002) Evidence for the presence of serotonin in Mysidacea (Crustacea, Peracarida) as revealed by fluorescence immunohistochemistry. Cell Tissue Res 310:359–371

    Article  PubMed  CAS  Google Scholar 

  • Müller M, Homberg U, Kühn A (1997) Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell Tissue Res 288:159–176

    Article  PubMed  Google Scholar 

  • Mulloney B, Tschuluun N, Hall WM (2003) Architectonics of crayfish ganglia. Microsc Res Tech 60:253–265

    Article  PubMed  Google Scholar 

  • Ngernsoungnern P, Ngernsoungnern A, Kavanaugh S, Sobhon P, Sower SA, Sretarugsa P (2008) The presence and distribution of gonadotropin releasing hormone-like factor in the central nervous system of the black tiger shrimp, Penaeus monodon. Gen Comp Endocrinol 155:613–622

    Article  PubMed  CAS  Google Scholar 

  • Parameswaran R (1956) Neurosecretory cells of the central nervous system of the crab, Paratelphusa hydrodromous. Q J Microsc Sci 97:75–82

    Google Scholar 

  • Quackenbush LS (1992) Yolk synthesis in the marine shrimp, Penaeus-vannamei. Comp Biochem Physiol A Mol Integr Physiol 103:711–714

    Article  Google 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 7:29

    Article  PubMed  PubMed Central  Google 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 11:77–86

    Google 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 353:493–510

    Article  PubMed  CAS  Google Scholar 

  • Sandeman DC, Sandeman RE, Aitken AR (1988) Atlas of serotonin-containing neurons in the optic lobes and brain of the crayfish Cherax destructor. J Comp Neurol 269:465–478

    Article  PubMed  CAS  Google Scholar 

  • Sandeman D, Sandeman R, Derby C, Schmidt M (1992) Morphology of the brain of the crayfish, crabs and spiny lobsters: a common nomenclature for homologous structures. Biol Bull 183:304–326

    Article  PubMed  CAS  Google Scholar 

  • Sandeman DC, Benton JL, Beltz BS (2009) An identified serotonergic neuron regulates neurogenesis in the crayfish brain. Dev Neurobiol 69:530–545

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santhoshi S, Sugumar V, Munuswamy N (2008) Histological and immunocytochemical localization of serotonin-like immunoreactivity in the brain and optic ganglia of the Indian white shrimp, Fenneropenaeus indicus. Microsc Res Tech 71:186–195

    Article  PubMed  CAS  Google Scholar 

  • Sarojini R, Nagabhushanam R, Fingerman M (1995) Dopaminergic and enkephalinergic involvement in the regulation of blood glucose in the red swamp crayfish, Procambarus clarkii. Gen Comp Endocrinol 97:160–170

    Article  PubMed  CAS  Google Scholar 

  • Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea and Hexapoda). Arthropod Str Dev 34:257–299

    Article  Google Scholar 

  • Schmidt M, Ache BW (1997) Immunocytochemical analysis of glomerular regionalization and neuronal diversity in the olfactory deutocerebrum of the spiny lobster. Cell Tissue Res 287:541–563

    Article  PubMed  CAS  Google Scholar 

  • Serrano-Pinto V, Vazquez-Boucard C, Villarreal-Colmenares H (2003) Yolk proteins during ovary and egg development of mature female freshwater crayfish (Cherax quadricarinatus). Comp Biochem Physiol A Mol Integr Physiol 134:35–45

    Article  Google Scholar 

  • Soonklang N, Wanichanon C, Stewart MJ, Stewart P, Meeratana P, Hanna PJ, Sobhon P (2012) Ultrastructure of differentiating oocyte and vitellogenesis in the giant fresh water prawn, Macrobrachium rosenbergii (de man). Microsc Res Tech 75:1402–1415

    Article  PubMed  CAS  Google 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 25:1704

    Google Scholar 

  • Sosa M, Baro D (2002) The role of amines and aminergic receptors in mediating dominance in the giant tropical freshwater prawn. In: WieseK SchmidtM (ed) Physiology of the crustacean nervous system. Springer, Berlin, pp 143–155

    Chapter  Google Scholar 

  • Sosa MA, Spitzer N, Edward DH, Baro DJ (2004) A crustacean serotonin receptor: cloning and distribution in the thoracic ganglia of crayfish and freshwater prawn. J Compar Neurol 473:526–537

    Article  CAS  Google Scholar 

  • Sullivan JM, Benton JL, Beltz BS (2000) Serotonin depletion in vivo inhibits the branching of olfactory projection neurons in the lobster deutocerebrum. J Neurosci 20:7716–7721

    Article  PubMed  CAS  Google 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 455:50–60

    Article  CAS  Google Scholar 

  • Thongbuakaew T, Siangcham T, Suwansa-ard S, Elizur A, Cummins SF, Sobhon P, Sretarugsa P (2016b) Steroids and genes related to steroid biosynthesis in the female giant freshwater prawn, Macrobrachium rosenbergii. Steroids 107:149–160

    Article  PubMed  CAS  Google Scholar 

  • Tierney AJ, Mangiamele LA (2001) Effects of serotonin and serotonin analogs on posture and agonistic behavior in crayfish. J Comp Physiol A 187:757–767

    Article  PubMed  CAS  Google 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 82:1007–1022

    Article  Google Scholar 

  • Tinikul Y, Mercier AJ, Sobhon P (2009b) Distribution of dopamine and octopamine in the central nervous system and ovary during the ovarian maturation cycle of the giant freshwater prawn, Macrobrachium rosenbergii. Tissue Cell 41:430–442

    Article  PubMed  CAS  Google 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 343:579–593

    Article  PubMed  CAS  Google 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 345:103–124

    Article  PubMed  CAS  Google Scholar 

  • Tomy S, Saikrithi P, James N, Balasubramanian CP, Panigrahi A, Otta SK, Subramoniam T, Ponniah AG (2016) Serotonin induced changes in the expression of ovarian gene network in the Indian white shrimp, Penaeus indicus. Aquaculture 452:239–246

    Article  CAS  Google Scholar 

  • Tsukimura B (2001) Crustacean vitellogenesis: its role in oocyte development. Am Zool 41:465–476

    CAS  Google Scholar 

  • Vaca A, Alfaro J (2000) Ovarian maturation and spawning in the white shrimp, Penaeus vannamei, by serotonin injection. Aquaculture 182:373–385

    Article  CAS  Google Scholar 

  • Warrier SR, Tirumalai R, Subramoniam T (2001) Occurrence of vertebrate steroids, estradiol 17beta and progesterone in the reproducing females of the mud crab Scylla serrata. Comp Biochem Physiol A Mol Integr Physiol 130:283–294

    Article  PubMed  CAS  Google Scholar 

  • Wongprasert K, Asuvapongpatana S, Poltana P, Tiensuwan M, Withyachumnarnkul B (2006) Serotonin stimulates ovarian maturation and spawning in the black tiger shrimp Penaeus monodon. Aquaculture 261:1447–1454

    Article  CAS  Google Scholar 

  • Yano I (1985) Induced ovarian maturation and spawning in greasyback shrimp, Metapenaeus ensis, by progesterone. Aquaculture 47:223–229

    Article  Google Scholar 

  • Yano I (1987) Effect of 17-hydroxy progesterone on vitellogenin secretion in kuruma prawn Penaeus japonicus. Aquaculture 61:49–57

    Article  CAS  Google Scholar 

  • Yano I, Chinzei Y (1987) Ovary is the site of vitellogenin synthesis in kuruma prawn, Penaeus japonicus. Compar Biochem Physiol Part B Compar Biochem 86:213–218

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Department of Anatomy, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand

    Boworn Soonthornsumrith, Thanapong Kruangkum, Tipsuda Thongbuakaew, Thanyaporn Senarai, Ronnarong Palasoon, Prasert Sobhon & Prapee Sretarugsa

  2. Department of Anatomy, Faculty of Science, Prince of Songkla University, Songkhla, 90110, Thailand

    Jirawat Saetan

  3. Center of Excellence for Shrimp Molecular Biology and Biotechnology (CENTEX Shrimp), Mahidol University, Bangkok, 10400, Thailand

    Thanapong Kruangkum

  4. School of Medicine, Walailak University, Thasala District, Nakhonsrithammarat, 80161, Thailand

    Tipsuda Thongbuakaew

  5. Anatomy Unit, Department of Medical Sciences, Faculty of Science, Rangsit University, Muang Ake, Pathumthani, 12000, Thailand

    Ronnarong Palasoon

  6. Faculty of Allied Health Sciences, Burapha University, Muang, Chonburi, 20131, Thailand

    Prasert Sobhon

Authors
  1. Boworn Soonthornsumrith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jirawat Saetan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thanapong Kruangkum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tipsuda Thongbuakaew
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thanyaporn Senarai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ronnarong Palasoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Prasert Sobhon
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Prapee Sretarugsa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Prapee Sretarugsa.

Ethics declarations

Conflict of interest

We declare that this work has no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MP4 17206 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soonthornsumrith, B., Saetan, J., Kruangkum, T. et al. 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. Invert Neurosci 18, 5 (2018). https://doi.org/10.1007/s10158-018-0209-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10158-018-0209-3

Keywords

Search

Navigation