Multifunctional features of a gastrodermal sensory cell inHydra: three-dimensional study
Abstract
Computer-assisted, three-dimensional reconstructions of two gastrodermal sensory cells from transmission electron micrographs of serial sections of Hydra revealed a unipolar morphology with the nucleus near an apical cilium and a simple unbranched axon with a widened terminal. The sensory cells were similar in size and shape to a unipolar sensory cell isolated from macerated gastrodermis and examined with scanning electron microscopy. In thin sections, the cells were characterized by the presence of numerous dense-cored vesicles in the axon and its terminal. A few dense-cored vesicles were aligned at electron-dense synaptic foci in the axon terminal of the sensory cell, which formed an axo-axonal synapse with a nearby centrally located ganglion cell and a neuromuscular synapse with the basal myoneme of a digestive cell. The ganglion cell possessed a perikaryal cilium and a slender axon that extended adjacent to the sensory cell terminal, where it formed an en passant axo-axonal synapse in reciprocal arrangement with that of the sensory cell. In addition, the ganglion cell axon formed a neuromuscular synapse in sequence with the sensory cell axo-axonal synapse. The presence of a large number of neurosecretory-like granules, apical cilium and reciprocal interneuronal and neuromuscular synaptic loci suggests that this gastrodermal sensory cell, characterized ultrastructurally for the first time, represents a third type of multifunctional neuron in Hydra. Thus, Hydra may contain primitive stem-like neurons, which are sensory-motor and also function in both neurosecretion and neurotransmission.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Direct sensory-motor neurons innervating muscles can still be observed in cnidarian nervous systems.
“In support of the neuro-myoepithelial cell scenario, direct sensory-motor neurons, innervating muscles, can still be observed in cnidarian nervous systems.”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [62]
These neurons trigger local muscle contractions.
“These neurons trigger local muscle contractions.”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [62]
Direct sensory-motor neurons innervating muscles were described in the tentacles of Hydra and the sea anemone Aiptasia.
“They were described in the tentacles of Hydra [60–63] and the sea anemone Aiptasia [64].”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [62]
Cites
Society for Neuroscience 2007 abstracts
Wishart, T. M., Paterson, J. M., Short, D. M., Meredith, S., Robertson, K., Sutherland, C. D., Cousin, M. A., Dutia, M. B., & Gillingwater, T. H. (2007) · Cited by 2,094 · see citing works
A Modified Method for Lead Staining of Thin Sections
Sato, T. (1968) · Journal of Electron Microscopy · doi:10.1093/oxfordjournals.jmicro.a049610 · Cited by 820 · see citing works
Journal of Embryology and Experimental Morphology
(1953) · Nature · doi:10.1038/172240b0 · Cited by 674 · see citing works
Journal of Embryology and Experimental Morphology
Dr, N. (1953) · Nature · doi:10.1038/171339a0 · Cited by 466 · see citing works
A quantitative method for maceration of hydra tissue
David, C. N. (1973) · Development Genes and Evolution · doi:10.1007/bf00577724 · Cited by 446 · see citing works
Scanning electron microscopy/1976/II.
Johari, O., & Becker, R. P. (1976) · IIT Research Institute eBooks · Cited by 301 · see citing works
Evolution and tumour pathology of the neuroendocrine system
Swaab, D. F. (1985) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(85)90014-0 · Cited by 233 · see citing works
The Elementary Nervous System.
Parkhurst, H. H., & Parker, G. H. (1919) · The Journal of Philosophy Psychology and Scientific Methods · doi:10.2307/2940224 · Cited by 229 · see citing works
The elementary nervous system.
Parker, G. H. (1919) · doi:10.1037/13832-000 · Cited by 200 · see citing works
Ultrastructural evidence for a granule-containing sensory-motor-interneuron in Hydra littoralis
Westfall, J. A. (1973) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(73)90055-5 · Cited by 169 · see citing works
Self-citationThree‐dimensional reconstructions from serial micrographs using the IBM PC
Young, S. J., Royer, S. M., Groves, P. M., & Kinnamon, J. C. (1987) · Journal of Electron Microscopy Technique · doi:10.1002/jemt.1060060211 · Cited by 154 · see citing works
Self-citationA second sensory?motor?interneuron with neurosecretory granules inHydra
Westfall, J. A., & Kinnamon, J. C. (1978) · Journal of Neurocytology · doi:10.1007/bf01176999 · Cited by 140 · see citing works
Self-citationPhysiology of a bidirectional, excitatory, chemical synapse
Anderson, P. A. V. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.3.821 · Cited by 132 · see citing works
Davis, L. E., Burnett, A. L., Haynes, J. F., Osborne, D. G., & Spear, M. L. (1968) · Journal of Experimental Zoology · doi:10.1002/jez.1401670305 · Cited by 123 · see citing works
Lentz, T. L. (1968) · Cited by 119 · see citing works
Schaller, H., & Gierer, A. (1973) · Development · doi:10.1242/dev.29.1.39 · Cited by 119 · see citing works
Co-Ordinating Systems and Behaviour in Hydra
Passano, L. M., & McCullough, C. B. (1965) · Journal of Experimental Biology · doi:10.1242/jeb.42.2.205 · Cited by 110 · see citing works
The nervous system of hydra. I. Types, distribution and origin of nerve elements
Burnett, A. L., & Diehl, N. A. (1964) · Journal of Experimental Zoology · doi:10.1002/jez.1401570205 · Cited by 99 · see citing works
Histologie von Hydra fusca mit besonderer Berücksichtigung des Nervensystems der Hydropolypen
Schneider, K. C. (1890) · Archiv für Mikroskopische Anatomie · doi:10.1007/bf02955882 · Cited by 83 · see citing works
Koizumi, O., Wilson, J. D., Grimmelikhuijzen, C. J. P., & Westfall, J. A. (1989) · Journal of Experimental Zoology · doi:10.1002/jez.1402490105 · Cited by 67 · see citing works
Self-citationUltrastructural evidence for a sensory-motor neuron in Ctenophora
Hernandez‐Nicaise, M. (1974) · Tissue and Cell · doi:10.1016/0040-8166(74)90021-4 · Cited by 64 · see citing works
A three dimensional serial reconstruction of neuronal distributions in the hypostome of a Hydra
Kinnamon, J. C., & Westfall, J. A. (1981) · Journal of Morphology · doi:10.1002/jmor.1051680308 · Cited by 61 · see citing works
Self-citationTypes of neurons and synaptic connections at hypostome‐tentacle junctions in Hydra
Kinnamon, J. C., & Westfall, J. A. (1982) · Journal of Morphology · doi:10.1002/jmor.1051730110 · Cited by 60 · see citing works
Self-citationFunctional organization of battery cell complexes in tentacles of Hydra attenuata
Hufnagel, L. A., Kass‐Simon, G., & Lyon, M. K. (1985) · Journal of Morphology · doi:10.1002/jmor.1051840307 · Cited by 59 · see citing works
Anderson, P. A. V., & Grünert, U. (1988) · Synapse · doi:10.1002/syn.890020605 · Cited by 47 · see citing works
Neurones and neuropeptides in coelenterates.
Grimmelikhuijzen, C. J. P., Graff, D., & MCFARLANE, I. D. (1989) · Archivum histologicum japonicum · doi:10.1679/aohc.52.suppl_265 · Cited by 46 · see citing works
The distribution of nerve cells inHydra attenuata Pall.
EPP, L. G., & Tardent, P. (1978) · Development Genes and Evolution · doi:10.1007/bf00848677 · Cited by 45 · see citing works
Perioral synaptic connections and their possible role in the feeding behavior of Hydra
Westfall, J. A., & Kinnamon, J. C. (1984) · Tissue and Cell · doi:10.1016/0040-8166(84)90055-7 · Cited by 44 · see citing works
Self-citationUltrastructure of Invertebrate Synapses
Westfall, J. A. (1987) · Springer eBooks · doi:10.1007/978-1-4613-1955-9_2 · Cited by 39 · see citing works
Self-citationUltrastructural evidence for the presence of nerve cells in the gastrodermis of Hydra
Davis, L. E. (1972) · Cell and Tissue Research · doi:10.1007/bf00337670 · Cited by 37 · see citing works
A Qualitative and Quantitative Inventory of Nervous Cells in Hydra Attenuata Pall
Tardent, P., & Weber, C. (1976) · Springer eBooks · doi:10.1007/978-1-4757-9724-4_52 · Cited by 34 · see citing works
A possible sensory-motor neuron in Aplysia californica
Coggeshall, R. E. (1971) · Tissue and Cell · doi:10.1016/s0040-8166(71)80010-1 · Cited by 32 · see citing works
FUNCTIONAL ANATOMY OF NEMATOCYTE INNERVATION IN BATTERY CELL COMPLEXES OF THE HYDRA TENTACLE
Hufnagel, L. A., & Kass‐Simon, G. (1988) · Elsevier eBooks · doi:10.1016/b978-0-12-345320-4.50032-8 · Cited by 24 · see citing works
Westfall, J. A. (1988) · Elsevier eBooks · doi:10.1016/b978-0-12-345320-4.50008-0 · Cited by 23 · see citing works
Self-citationTOWARDS A NEUROETHOLOGY OF NEMATOCYST DISCHARGE IN THE TENTACLES OF HYDRA
Kass‐Simon, G. (1988) · Elsevier eBooks · doi:10.1016/b978-0-12-345320-4.50033-x · Cited by 22 · see citing works
Coordination of Juxtaposed Muscle Layers as Seen in Hydra
Kass‐Simon, G. (1976) · Springer eBooks · doi:10.1007/978-1-4757-9724-4_72 · Cited by 21 · see citing works
Note sur le système nerveux de l’Hydre
Gansen, P. V. (1952) · Bulletin de la Classe des sciences · doi:10.3406/barb.1952.69690 · Cited by 18 · see citing works
Scanning electron microscopy of neurons isolated from the pedal disk and body column of Hydra
Westfall, J. A., & EPP, L. G. (1985) · Tissue and Cell · doi:10.1016/0040-8166(85)90085-0 · Cited by 16 · see citing works
Self-citationWestfall, J. A., Argast, D. R., & Kinnamon, J. C. (1983) · Journal of Morphology · doi:10.1002/jmor.1051780202 · Cited by 15 · see citing works
Self-citationDilly, N. (1969) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(69)90031-8 · Cited by 9 · see citing works
Westfall, J. A., & Ra, R. (1990) · PubMed · Cited by 5 · see citing works
Self-citationStructure and Function of the Head Activator in Hydra and in Mammals
Schaller, H., & Bodenmüller, H. (1988) · Advances in metabolic disorders · doi:10.1016/b978-0-12-027311-9.50022-6 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Non-overlapping neural networks in Hydra vulgaris
Dupre, C., & Yuste, R. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.049 · Cited by 197 · see citing works
Neuropeptides regulate swimming depth of Platynereis larvae
Conzelmann, M., Offenburger, S.-L., Asadulina, A., Keller, T., Münch, T. A., & Jékely, G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109085108 · Cited by 136 · see citing works
Origin and early evolution of neural circuits for the control of ciliary locomotion
Jékely, G. (2011) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.2027 · Cited by 103 · see citing works
Stem cells and lineages of the intestine: a developmental and evolutionary perspective
Takashima, S., Gold, D., & Hartenstein, V. (2013) · Development Genes and Evolution · doi:10.1007/s00427-012-0422-8 · Cited by 67 · see citing works
Chemosensory organs as models of neuronal synapses
Shaham, S. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2740 · Cited by 62 · see citing works
Taddei-Ferretti, C., & Musio, C. (2000) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/s1011-1344(00)00041-5 · Cited by 54 · see citing works
Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review
Koizumi, O., Sato, N., & Goto, C. (2007) · Springer eBooks · doi:10.1007/978-1-4020-2762-8_5 · Cited by 37 · see citing works
Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review
Koizumi, O., Sato, N., & Goto, C. (2004) · Hydrobiologia · doi:10.1007/s10750-004-2636-x · Cited by 32 · see citing works
Yamamoto, W. R., & Yuste, R. (2020) · eNeuro · doi:10.1523/eneuro.0539-19.2020 · Cited by 31 · see citing works
Suspected chemoreceptors in coelenterates and ctenophores
Kass‐Simon, G., & Hufnagel, L. A. (1992) · Microscopy Research and Technique · doi:10.1002/jemt.1070220305 · Cited by 28 · see citing works
Santillo, S., Orlando, P., PETROCELLIS, L. D., Cristino, L., Guglielmotti, V., & Musio, C. (2006) · Biosystems · doi:10.1016/j.biosystems.2006.03.008 · Cited by 28 · see citing works
Golz, R., & Thurm, U. (1993) · PROTOPLASMA · doi:10.1007/bf01378858 · Cited by 26 · see citing works
Tension sensitivity of the heart pacemaker neurons in the isopod crustaceanLigia pallasii
Sakurai, A., & Wilkens, J. L. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.00050 · Cited by 19 · see citing works
Origin and Evolution of the Nervous System Considered from the Diffuse Nervous System of Cnidarians
Koizumi, O. (2016) · Springer eBooks · doi:10.1007/978-3-319-31305-4_6 · Cited by 13 · see citing works
The neural net of Hydra and the modulation of its periodic activity
Taddei-Ferretti, C., & Musio, C. (1999) · Lecture notes in computer science · doi:10.1007/bfb0098167 · Cited by 13 · see citing works
Scanning electron microscopy of endodermal sensory cells of Hydra magnipapillata
Murate, M., Takahashi‐Iwanaga, H., Kurosaki, R., Takeda, M., & Koizumi, O. (1996) · Cell and Tissue Research · doi:10.1007/s004410050556 · Cited by 5 · see citing works
Two-photon manipulation of neuronal activity and behavior in Hydra vulgaris
Yamamoto, W. R., & Yuste, R. (2023) · STAR Protocols · doi:10.1016/j.xpro.2023.102453 · Cited by 3 · see citing works
Kass‐Simon, G., & Hufnagel, L. A. (2015) · Wiley eBooks · doi:10.1002/9781118828502.ch11 · Cited by 4 · see citing works
Hartenstein, V., Sprecher, S., & Martinez, P. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00043-9 · Cited by 1 · see citing works
- Authors
- Westfall, J. A., Wilson, J. D., Rogers, R. A., & Kinnamon, J. C.
- Affiliations
- Kansas State University (US)
- University of Colorado Boulder (US)
- ORCID
- Kinnamon, J. C.
- Venue
- Journal of Neurocytology
- Published
- 1991-04
- Volume
- 20
- Issue
- 4
- Pages
- 251-261
- ISSN
- 0300-4864 (ISSN-L)
- 1573-7381
- OpenAlex
- W2025720714
- Cited by
- 19
- References
- 42
- Citations by year
- 2025: 1 · 2023: 1 · 2020: 1 · 2017: 1 · 2016: 1 · 2015: 1 · 2012: 1
- FWCI
- 1.16
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Neurocytology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ns021688-02, 2r01ns010264-15a1)
- National Institute of Neurological Disorders and Stroke (NS21688, NS-10264)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- Hydra, axo-axonal synapses, neuromuscular synapse, dense core vesicles, neurosecretory granules, neurosecretion, neurotransmission, three-dimensional ultrastructure
- MeSH terms
- Animals, Axons, Cilia, Hydra, Microscopy, Electron, Microscopy, Electron, Scanning, Models, Structural
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
