Abstract
In Hydra vulgaris, physiological and pharmacological evidence exists for a hypostomal circumferential neuro-effector pathway that initiates ectodermal pacemaker activity at tentacular-hypostomal loci coordinating body and tentacle contractions. Here, we describe an ectodermal nerve ring that runs below and between the tentacles, and an anti-GABAB receptor antibody-labeled ring coincident with it. The location of this ring is consistent with the physiology of the hypostomal pacemaker systems of hydra. We also describe a distally located, ectodermal ring of nerve fibers that is not associated with anti-GABAB receptor antibody labeling. The neurites and cell bodies of sensory cells contribute to both rings. The location of the distal ring and its sensory cell neurites suggests an involvement in the behavior of the mouth. Between the two rings is a network of anastomosing sensory and ganglion cell bodies and their neurites. Phase contrast, darkfield, and antibody-labeled images reveal that the mouth of hydra comprises five or six epithelial folds whose endoderm extensively labels with anti-GABAB receptor antibody, suggesting that endodermal metabotrobic GABA receptors are also involved in regulating mouth behavior.








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References
Anctil M (2009) Chemical transmission in the sea anemone Nematostella vectensis: a genomic perspective. Comp Biochem Physiol D 4:268–289
Beams HW, Kessel RG, Shih C-Y (1973) The surface features of hydra as revealed by scanning electron microscopy. Trans Am Microsc Soc 92:161–175
Bellis SL, Kass-Simon G, Rhoads DE (1992) Partial characterization and detergent solubilization of the putative glutathione receptor from hydra. Biochemistry 31:9838–9843
Bode PM, Awad TA, Koizumi O, Makashima Y, Grimmelikhuijzen CJP, Bode HR (1988) Development of the two-part pattern during regeneration of the head in hydra. Development 102:223–235
Bullock TH, Horridge GA (1965) Coelenterata and Ctenophora. In: Bullock TH, Horridge GA (eds) Structure and function in the nervous systems of invertebrates, vol 1. Freemann, San Francisco, pp 459–534
Burnett AL, Diehl NA (1964) The nervous system of Hydra. I. Types, distribution and origin of nerve elements. J Exp Zool 157:217–226
Campbell RD (1987) Structure of the mouth of Hydra spp. A breach in the epithelium that disappears when it closes. Cell Tissue Res 249:189–197
Carter JA, Hyland C, Steele RE, Collins E-M S (2016) Dynamics of mouth opening in Hydra. Biophys J 110:1191–1201
Cristino L, Guglielmotti V, Musio C, Santillo S (2007) Diffuse nerve net of Hydra revealed by NADPH-diaphorase histochemical labeling. In: Mele F, Ramella G, Santillo S, Ventriglia F (eds) Advances in brain, vision, and artificial intelligence. Lecture Notes in Computer Science, vol 4729. Springer, Berlin, pp 11-20
David CN (1973) A quantitative method for maceration of hydra tissue. Wilhelm Roux Arch 171:259–268
Davis LE, Burnett AL, Haynes JF (1968) A histological and ultrastructural study of the muscular and nervous system in Hydra. II. Nervous system. J Exp Zool 167:295–332
Dunne JF, Javois LC, Huang LW, Bode HR (1985) A subset of cells in the nerve net of Hydra oligactis defined by a monoclonal antibody: its arrangement and development. Dev Biol 109:41–53
Erskine ME (1989) The immunocytochemical identification of nerve cells of the tentacles of Hydra oligactis with the light and electron microscope. MS Thesis, University of Rhode Island
Garm A, Ekstrom P, Boudes M, Nilsson D-E (2006) Rhopalia are integrated part of the central nervous system in box jellyfish. Cell Tissue Res 325:333–343
Garm A, Poussart Y, Parkfelt L, Ekstrom P, Nilsson D-E (2007) The ring nerve of the box jellyfish Tripedalia cystophora. Cell Tissue Res 329:147–157
Grimmelikhuijzen CJP (1985) Antisera to the sequence Arg-Phe-amide visualize neuronal centralization in hydroid polyps. Cell Tissue Res 241:171–182
Grimmelikhuijzen CJP, Graff D, McFarlane ID (1989) Neurones and neuropeptides in coelenterates. Arch Histol Cytol 52 (Suppl):265–278
Grosvenor W, Rhoads DE, Kass-Simon G (1996) Chemoreceptive control of feeding processes in hydra. Chem Senses 21:313–321
Guertin S, Kass-Simon G (2015) Extraocular photosensitivity in the tentacles of Hydra vulgaris. Comp Biochem Physiol A Mol Integr Physiol 184:163–170
Hadzi J (1909) Ueber das Nervensystem von Hydra. Arb Zool Inst Wien 17:225–268
Hertwig O, Hertwig R (1879) Die Actinien. Jena Z Naturwiss 13:457–517
Hufnagel L, Kass-Simon G (1988) Functional anatomy of nematocyte innervation in battery cell complexes of the Hydra tentacle. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 519–531
Kass-Simon G (1972) Longitudinal conduction of contraction burst pulses from hypostomal excitation loci in Hydra attenuata. J Comp Physiol 80:20–49
Kass-Simon G (1973) Transmitting systems in Hydra. Pbl Seto Mar Biol Lab 20:583–594
Kass-Simon G, Hufnagel LA (2015) Nervous systems: morphology and physiology of Cnidarian conducting systems. In: Woodley C, Downs C, Bruckner A, Porter J, Galloway S (eds) Diseases of corals. Wiley-Blackwell, Boston, pp 164–191
Kass-Simon G, Passano LM (1978) A neuropharmacological analysis of the pacemakers and conducting tissues of Hydra attenuata. J Comp Physiol 128:71–79
Kass-Simon G, Scappaticci AA (2004) Glutamatergic and GABAnergic control in tentacle effector systems of Hydra vulgaris. Hydrobiology 530:67–71
Kass-Simon G, Pannaccionne A, Pierobon P (2003) GABA and glutamate receptors are involved in modulating pacemaker activity in hydra. Comp Biochem Physiol A 136:329–342
Kinnamon JC, Westfall JA (1981a) A three dimensional serial reconstruction of neuronal distributions in the hypostome of a Hydra. J Morphol 168:321–329
Kinnamon JC, Westfall JA (1981b) Types of neurons and synaptic connections at hypostome-tentacle junctions in Hydra. J Morphol 173:119–128
Kinnamon JC, Westfall JA (1984) High voltage electron stereomicroscopy of the cilium-stereociliary complex of perioral sensory cells in Hydra. Tissue Cell 16:345–352
Koizumi O (2007) Nerve ring of the hypostome in hydra: is it an origin of the central nervous system of bilaterian animals? Brain Behav Evol 69:151–159
Koizumi O, Itazawa M, Mizumoto H, Minobe S, Javois L, Grimmelikhuijzen C, Bode H (1992) Nerve ring of the hypostome in Hydra. I. Its structure, development, and maintenance. J Comp Neurol 326:7–21
Koizumi O, Sato N, Goto C (2004) Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review. Hydrobiology 530:41–47
Koizumi O, Hamada S, Minobe S, Hamaguchi-Hamada K, Kurumata-Shigeto M, Nakamua M, Namikwa H (2015) The nerve ring in cnidarians: its presence and structure in hydrozoan medusae. Zoology 118:79–88
Lauro BM (2015) Effects of GABAB ligands on the GSH-induced electrical activity of the hypostome in hydra. MS Thesis, University of Rhode Island, Open Access Master’s thesis paper 538
Lenhoff HM (1961) Activation of the feeding reflex in Hydra littoralis. I. Role played by reduced glutathione, and quantitative assay of the feeding reflex. J Gen Physiol 46:331–344
Loomis WF (1955) Glutathione control of the specific feeding reactions of Hydra. Ann N Y Acad Sci 62:209–228
Matsuno T, Kageyama T (1984) The nervous system in the hypostome of Pelmatohydra robusta: the presence of a circumhypostomal nerve ring in the epidermis. J Morphol 182:153–168
Munro B (2014) Immunohistochemical localization of the neuropeptide RFamide in the hypostomal nerve net of Hydra vulgaris. MS thesis, University of Rhode Island, Open Access Master’s thesis paper 371
Muscatine L, Lenhoff HM (1965) Symbiosis of hydra and algae. I. Effects of some environmental cations on growth of symbioticand aposymbiotic hydra. Biol Bull 128:415–424
Passano LM, McCullough CB (1962) Light response and the rhythmic potentials of Hydra. Proc Natl Acad Sci U S A 48:1376–1382
Passano LM, McCullough CB (1964) Co-ordinating systems and behaviour in hydra. I. Pacemaker system of the periodic contractions. J Exp Biol 41:643–664
Passano LM, McCullough CB (1965) Co-ordinating systems and behaviour in hydra. II. The rhythmic potential system. J Exp Biol 42:205–231
Pierobon P, Concas A, Santoro G, Marino G, Minei R, Pannaccione A, Mostallino MC, Biggio G (1995) Biochemical and functional identification of GABA receptors in Hydra vulgaris. Life Sci 56:1485–1497
Plachetzki DC, Fong CR, Oakley TH (2012) Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biol 10:17
Roberts A, Mackie GO (1980) The giant axon escape system of a hydrozoan medusa, Aglantha digitale. J Exp Biol 84:303–318
Rushforth NB, Burke DS (1971) Behavioral and electrophysiological studies of Hydra. II. Pacemaker activity of isolated tentacles. Biol Bull 140:502–519
Rushforth NB, Hofman F (1972) Behavioral and electrophysiological studies of Hydra. III. Components of feeding behavior. Biol Bull 142:110–131
Satterlie RA, Spencer AN (1983) Neuronal control of locomotion in hydrozoan medusae: a comparative study. J Comp Physiol 150:195–206
Scappaticci AA, Kass-Simon G (2008) NMDA and GABAB receptors are involved in controlling nematocyst discharge in hydra. Comp Biochem Physiol A 150:415–422
Singla CL (1978a) Locomotion and neuromuscular system of Aglantha digitale. Cell Tissue Res 188:317–327
Singla CL (1978b) Fine structure of the neuromuscular system of Polyorchis penicillatus (Hydromedusae, Cnidaria). Cell Tissue Res 193:163–174
Spencer AN, Arkett SA (1984) Radial symmetry and the organization of central neurons in hydrozoan jellyfish. J Exp Biol 110:69–90
Taddei-Ferretti C, Musio C (2000) Photobehavior of hydra (Cnidaria, Hydrozoa) and correlated mechanisms: a case of extraocular photosensitivity. J Photochem Photobiol B Biol 55:88–101
Takahashi T, Kobayakawa Y, Muneoka Y, Fujisawa Y, Mohri S, Hatta M, Shimizu H, Fujisawa T, Sugiyama T, Takahara M, Yanagi K, Koizumi O (2003) Identification of a new member of the GLWamide peptide family: physiological activity and cellular localization in cnidarian polyps. Comp Biochem Physiol B 135:309–324
Technau U, Holstein TW (1995) Boundary cells of endodermal origin define the mouth of Hydra vulgaris (Cnidaria). Cell Tissue Res 280:235–242
Watanabe H, Fujisawa T, Holstein TW (2009) Cnidarians and the evolutionary origins of the nervous system. Dev Growth Differ 51:167–183
Westfall JA (1973) Ultrastructural evidence for a granule-containing sensory-motor-interneuorn in Hydra litoralis. J Ultrastruct Res 42:268–282
Westfall JA, Townsend JW (1976) Stereo SEM applied to the study of feeding behavior in hydra. In: Johari O, Becker RP (eds) Scanning electron microscopy/1976/II. IIT Research Institute, Chicago, pp 563–568
Wood RL (1979a) The fine structure of the hypostome and mouth of hydra. I. Scanning electron microscopy. Cell Tissue Res 199:307–317
Wood RL (1979b) The fine structure of the hypostome and mouth of hydra. II. Transmission electron microscopy. Cell Tissue Res 199:319–338
Yu SM, Westfall JA, Dunne JF (1985) Light and electron microscopic localization of a monoclonal antibody in neurons in situ in the head region of Hydra. J Morphol 184:183–193
Yu SM, Westall JA, Dunne JF (1986) Use of a monoclonal antibody to classify neurons isolated from the head region of hydra. J Morphol 188:79–90
Acknowledgments
We thank Jarren Kay and Vandana Nandivada for maintaining the hydra, and Paul Johnson for help with the fluorescence microscope.
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This work was funded in part by University of Rhode Island Undergraduate Research Awards to: Shirley Acevedo, Rebecca Boisvert, Chelsea Danella, Caitlin DelSesto, Crisostomo Gomez, Rebecca Kilmer, Joseph Marcotte, Danielle Tetreault, Bethany Soucy, Kathy Su. This research is based in part upon work conducted using the Rhode Island Genomics and Sequencing Center, which is supported in part by the National Science Foundation under EPSCoR Grants (nos. 0554548 and EPS-1004057).
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Hufnagel, L.A., Kass-Simon, G. The two nerve rings of the hypostomal nervous system of Hydra vulgaris—an immunohistochemical analysis. Cell Tissue Res 366, 255–269 (2016). https://doi.org/10.1007/s00441-016-2447-1
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DOI: https://doi.org/10.1007/s00441-016-2447-1


