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

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(Oc) and very intense in Oc-Oc. Using an in vitro assay of an explant of mature ovary, it was shown that 5-HT was able to enhance ovarian estradiol-17β (E) and progesterone (P) 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.

Insights on Molecular Mechanisms of Ovarian Development in Decapod Crustacea: Focus on Vitellogenesis-Stimulating Factors and Pathways

“…Meeratana et al ( 46 ) reported that serotonin-primed thoracic ganglion medium accelerated ovarian development in M. rosenbergii , indicating an indirect effect of serotonin on reproduction. The localization of serotonin-immunoreactive cells in the X-organ neurons and fibers innervating the sinus gland tissue and in other parts of the central nervous system of various decapod crustaceans ( 57 , 63 ) support the suggested regulatory role of serotonin in the synthesis and release of other neurohormones from the XO/SG complex such as CHH ( 64 , 65 ) and probably other neuropeptides of the CHH-family ( 56 ). However, the presence of serotonin immunoreactivity was also observed in crustacean gonads ( 46 , 56 , 57 , 63 ) and its stimulatory effects on gonad maturation confirmed, thereby further advocating an autocrine/paracrine mode of receptor-mediated action for serotonin in the control of crustacean oocyte maturation.…”

“…Increasing levels of serotonin were observed in the ovaries of P. monodon ( 50 ), L. vannamei ( 56 ), and M. rosenbergii ( 52 ) during the early ovarian maturation stages, reaching maximum levels at the mature ovarian stages. In support of this observation, Soonthornsumrith et al ( 57 ) also suggested that serotonin in both the central nervous system and ovary act in harmony to control oocyte maturation. A combination of spiperone (a dopamine antagonist) and serotonin was shown to induce ovarian maturation in M. rosenbergii ( 58 ) together with enhanced spawning in L. vannamei and Litopenaeus stylirostris ( 59 ) compared with the injection of serotonin alone.…”

“…Sathyanandam et al ( 64 ) reported that serotonin injection resulted in hyperglycemia by triggering the release of CHH in P. indicus . A recent report by Soonthornsumrith et al ( 57 ) indicated that serotonin enhanced the secretion of ovarian steroids (estradiol and progesterone) in mature ovarian explants from M. rosenbergii and suggested that serotonin-regulated ovarian maturation via the induction of female sex steroid hormone release in turn stimulated vitellogenesis.…”

Expression pattern of olfactory receptor genes in human cumulus cells as an indicator for competent oocyte selection

“…Taken together, it is concluded that the activation of OR10H2 through serotonin promotes successful fertilization by preventing cumulus cell senescence and improving oocyte survival. Furthermore, it is likely that the serotonin-mediated OR10H2 stimulation and the subsequent OMP activation in competent oocytes trigger an OR-dependent signal transduction cascade between the nervous and endocrine systems to help ovarian steroid secretion and to enhance oocyte quality (Kang et al, 2015;Soonthornsumrith et al, 2018). Given the previous findings, serotonin could also regulate progesterone secretion by granulosa cells (Yang et al, 2015).…”

“…bind to the secreted serotonin and maintain the oocyte development and fertilization potential through the activation of AC3 and cAMP production in cumulus cells (Doty and Kamath, 2014;Soonthornsumrith et al, 2018). Giacomo et al have shown that cAMP elevation prevents cumulus cell apoptosis and allows them to preserve oocyte fertilizability through exerting protective effects on oocyte (Di Giacomo et al, 2016).…”