Brain ventricle development in H. huso (Beluga sturgeon) larvae S. H. Tavighi, Z. Saadatfar, B. Shojaei & M. Behnam Rassouli Anatomical Science International ISSN 1447-6959 Anat Sci Int DOI 10.1007/s12565-015-0307-9 1 23 Your article is protected by copyright and all rights are held exclusively by Japanese Association of Anatomists. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Anat Sci Int DOI 10.1007/s12565-015-0307-9 ORIGINAL ARTICLE Brain ventricle development in H. huso (Beluga sturgeon) larvae 1 1 2 3 S. H. Tavighi • Z. Saadatfar • B. Shojaei • M. Behnam Rassouli Received: 10 February 2015 / Accepted: 5 October 2015 Ó Japanese Association of Anatomists 2015 Abstract The development of ventricles in the brain of with age, extending laterally from 6 days old. The con- H. huso (Beluga sturgeon) from 1 to 54 days old is pre- nection of the cerebellar ventricle to the fourth ventricle in sented in this study. The components observed in the the medulla oblongata was visible from 6 days old. Upon 1-day-old ventricular system were the telencephalic, tectal, dividing the ventricular system into three regions (fore- and cerebellar ventricles. These ventricles were not brain, midbrain, and hindbrain), stereological studies per- observed to have any recess or sulcus. They were sur- formed utiizing Cavalieri’s principle indicated that the rounded by copious ependymal and embryonic cells. Two forebrain ventricular region had the smallest volume while different parts were detected in the 6-day-old telencephalic the hindbrain ventricular region had the largest. ventricle: the olfactory and lateral ventricle. The olfactory ventricle was observed as a cranial extension of the Keywords H. huso Á Brain Á Ventricle Á Development Á telencephalic ventricle from 6 days old, as was the inner Stereological cell layer of the olfactory bulb (ic) adjacent to this exten- sion. In the preoptic region, the lateral ventricle was con- Abbreviations nected to the preoptic recess from 15 days old, and this Caq Cerebral aqueduct recess was connected by the interventricular foramen to the cc Central canal third ventricle in the diencephalon. At 6 days old, the third co Commissural organ ventricle in the diencephalon was visible at the caudal part cp Choroid plexus of the lateral ventricle, and the third ventricle had a recess Crc Crown cell near to the inferior lobe of the hypothalamus. At 6 days old, Crv Cerebellar ventricle the tectal ventricle was observed to have bilateral exten- D Diencephalon sions which proceeded to grow with age. The cerebellar ECrv Extension of cerebellar ventricle ventricle, situated between the two lobes of the cerebellum, EM Embryonic cell was observed from 1 day old. The cerebellar ventricle grew EOTV Extension of tectal ventricle ep Ependymal cell Etv Extension of telencephalic ventricle & Z. Saadatfar FV Fourth ventricle [email protected]; [email protected] h Habenula 1 Hypr Hypothalamic recess Department of Basic Science, Faculty of Veterinary Hypv Hypothalamic ventricle Medicine, Ferdowsi University of Mashhad, 91779-48974 Mashhad, Iran ic Inner cell layer of olfactory bulb ivf Interventricular foramen 2 Department of Basic Sciences, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, lr Lateral recess of ventricle Iran Lav Lateral ventricle 3 Department of Physiological Science, Faculty of Biology, Ma Mauthner cell Ferdowsi University of Mashhad, Mashhad, Iran MO Medulla oblongata 123 Author's personal copy S. H. Tavighi et al. NAT Anterior tuberal nucleus of its brain ventricles. However, despite all of the research NLT Lateral tuberal nucleus that has been performed on brain ventricles, there have NRP Nucleus of posterior recess been few studies on the morphology and evolution of the Olb Olfactory bulb brain ventricles in H. huso larvae. Olv Olfactory ventricle The central nervous system grows from a hollow tube OT Optic tectum during the embryonic period. The walls of this tube thicken OTV Tectal ventricle and form the brain and the spinal cord. The hollow tube Phr Posthabenular recess fills with the CSF of the ventricular system. This system POR Posterior recess develops laterally and forms different parts of the brain in PR Preoptic region all vertebrates, including the olfactory bulb, telencephalic PRr Preoptic recess hemispheres, midbrain, and hindbrain or cerebellum (But- pvopa Anterior part of the paraventricular organ ler and Hodos 2005). Septa Subependymal arteries In most vertebrates, the ventricular system of the brain SHypv Sulcus hypothalamicus extends laterally within the telencephalic hemispheres, Sih Sulcus intrahabenularis forming a region known as the lateral ventricle. This SlH Sulcus limitans of HIS ventricle connects to the interventricular foramen (Butler Slt Sulcus limitans telencephali and Hodos 2005), which in turn links to the third ventricle, SPR Sulcus preopticus which is a median ventricular space in the diencephalon. In Ssh Sulcus subhabenularis the dorsal region of this ventricle, the tectal ventricle SV Saccus vasculosus occupies the midbrain space. In the caudal part of the third T Telencephalon ventricle is a thin canal called the cerebral aqueduct, which TH Telencephalic hemisphere connects to the fourth ventricle in the hindbrain (Butler and thv Third ventricle Hodos 2005). The fourth ventricle extends caudally to the Tpp Periventricular nucleus of the posterior central canal of the spinal cord. tuberculum The walls of the ventricles are completely covered with tv Telencephalic ventricle a thin ependymal layer and meninx, which form the tela VC Valvula cerebelli chorioidea or choroid plexus. This structure consists of VIIv Facial viscerosensory lobe blood vessels and produces cerebrospinal fluid (CSF) in Vnl Vagal viscerosensory lobe the ventricular system (Broglio et al. 2003). CSF circu- lates in the ventricular system, protecting the brain against physical trauma and other damage (Butler and Hodos 2005). Introduction While there have been studies of ventricular develop- ment in the teleost brain (Ekstrom et al. 2001), the evo- H. huso (Beluga sturgeon) is an especially long-lived sea- lution of the CNS in sturgeons (Von Kupffer 1906), the dwelling fish species that is well-known commercially due ontogenesis of the brain in A. ruthenus (Nieuwenhuys to the high value of H. huso caviar (Birstein et al. 1998), 1962 and 1963), and brain development in A. naccari although it is also an important source of valuable fish (Vazquez et al. 2002), there has been no research into the meat. Adult H. huso are not deep-sea fish (they usually live evolution of the brain ventricles in H. huso larvae. in the middle depths), these pelagic fishes require a rela- Therefore, in the research reported in the present paper, tively low-light environment and make use of special we studied ventricular morphogenesis and volume in 1- to senses; for instance, they can perceive the Earth’s magnetic 54-day-old H. huso larvae. Ventricular volumes were field and without using other environmental factors to estimated by Cavalieri’s principle, which is often used in navigate while migrating (Kimley et al. 2002). Other stereological research to estimate organ volumes (Gun- sturgeon species are normally benthic—they swim along dersen and Jensen 1987). In this approach, sections of the the sea bottom (Bergquist 1932). Obviously, this difference organ are prepared and then sampled at regular intervals. between the behavior of H. huso and that of other sturgeon A point grid is then applied to each sampled section, and species is reflected in differences in brain development the number of grid points that occur within the section is between these species (Bemis et al. 1997). noted. Knowledge of the number of grid points within The brain structure of a ray-finned fish changes during each section as well as the interval between sections the development of the fish (Northcutt 1978 and 1996), and allows the volume of the organ of interest to be estimated these changes correlate with key points in the development (Howard and Reed 1998). 123 Author's personal copy Brain ventricle development in H. huso (Beluga sturgeon) larvae Materials and methods The olfactory ventricle was seen as a cranial extension of the telencephalic ventricle that was covered with a thin For this research, we obtained 40 samples of H. huso layer of ependymal cells (Fig. 2). Its expansion to the larvae aged 1, 3, 6, 15, 21, and 54 days post-hatch (dph) olfactory bulb developed with age. Adjacent to this from the Shahid Marjani Aghghela propagation station in extension, the inner cell layer of the olfactory bulb (ic) Gorgan. Six larvae of each age were fixed in 10 % neutral (Fig. 2) was observed from 6 days old. The olfactory buffered formalin, dehydrated with an ethanol series to ventricle was followed by the lateral ventricle at the caudal 100 %, cleared in xylene, and embedded in paraffin. part of the telencephalon; these were situated inside the Because the larval brains were very small, each head was telencephalic hemispheres. fixed and sited in paraffin blocks. Blocks were cut fron- From 15 days old, the sulcus limitans telencephali tally into serial sections six microns thick from the start to appeared in the caudomedial part of the lateral ventricle the end of the specimen using a microtome. Tissue sec- and the caudal part of the pallium (Fig.