A second sensory?motor?interneuron with neurosecretory granules inHydra
Abstract
Using serial-sectioning techniques for conventional transmission and high-voltage electron microscopy, we characterized the ultrastructural features and synaptic contacts of the sensory cell in tentacles of Hydra. The sensory cell has an apical specialization characterized by a recessed cilium surrounded by three rodlike stereocilia. This ciliary--stereociliary complex constitutes the receptive or dendritic pole of the sensory cell. The dense filamentous cores of the stereocilia project proximally into a narrow circumciliary cytoplasmic region connected by septate junctions to marginal processes of an enveloping epitheliomuscular cell. The central cilium has a characteristic marginal flare midway along its length and a dense filamentous substructure at its base. Pairs of branched, striated rootlets extend from the axial centriole into a mitochondria-rich region of the cell. Pigment-like granules are present in the cytoplasm around the circumciliary space. The perikaryon is characterized by an elongate nucleus surrounded by a narrow rim of cytoplasm containing prominent Golgi complexes, assorted vacuoles and dense-cored vesicles, free ribosomes, short segments of rough endoplasmic reticulum, microtubules, glycogen particles, and lipid droplets. Generally, one or two thin, naked axons extend laterally from the perikaryon into the nerve net region above the myonemes of the large epitheliomuscular cells. Within the axons are found occasional aggregates of dense-cored vesicles and en passant synapses characterized by the presence of clear or dense-cored vesicles in contact with paramembranous densities and associated intracleft cross filaments. Using these ultrastructural criteria, we demonstrated for the first time that the granule-containing sensory cells have synaptic contacts with other neurons, nematocytes, and epitheliomuscular cells hence, we considered these cells to be sensory--motor--interneurons with neurosecretory granules. We hypothesize that this unique, apparently multifunctional neuron may be a modern representative of a primitive stem cell that give rise evolutionarily to the sensory cells, motor neurons, interneurons, and neurosecretory cells of higher animals.
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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 [61]
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 [61]
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 [61]
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Self-citationHibberd, T. J., Travis, L., Wiklendt, L., Costa, M., Brookes, S. J., Hu, H., Keating, D. J., & Spencer, N. J. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00234.2017 · 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-citationYu, S., Westfall, J. A., & Dunne, J. F. (1985) · Journal of Morphology · doi:10.1002/jmor.1051840208 · Cited by 23 · see citing works
Self-citationImmunocytochemical evidence for an NMDA1 receptor subunit in dissociated cells of Hydra vulgaris
Scappaticci, A. A., Jacques, R. O., Carroll, J. E., Hufnagel, L. A., & Kass‐Simon, G. (2004) · Cell and Tissue Research · doi:10.1007/s00441-004-0879-5 · Cited by 22 · see citing works
TOWARDS 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
Neuropeptides in Invertebrates
Grimmelikhuijzen, C. J. P., Graff, D., Groeger, A., & McFarlane, I. D. (1987) · Springer eBooks · doi:10.1007/978-1-4613-1955-9_6 · Cited by 22 · see citing works
Neural pathways and innervation of cnidocytes in tentacles of sea anemones
Westfall, J. A. (2004) · Hydrobiologia · doi:10.1007/s10750-004-2678-0 · Cited by 21 · see citing works
Self-citationNeurons and Their Peptide Transmitters in Coelenterates
Grimmelikhuijzen, C. J. P., Graff, D., Koizumi, O., Westfall, J. A., & McFarlane, I. D. (1989) · Springer eBooks · doi:10.1007/978-1-4899-0921-3_7 · Cited by 20 · see citing works
Self-citationFine structure of touch-plates in the scyphomedusan Aurelia aurita
Hündgen, M., & Biela, C. (1982) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(82)90016-8 · Cited by 20 · see citing works
Multifunctional features of a gastrodermal sensory cell inHydra: three-dimensional study
Westfall, J. A., Wilson, J. D., Rogers, R. A., & Kinnamon, J. C. (1991) · Journal of Neurocytology · doi:10.1007/bf01235543 · Cited by 19 · see citing works
Self-citationTension 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
Matsuno, T., & Kageyama, T. (1984) · Journal of Morphology · doi:10.1002/jmor.1051820204 · Cited by 18 · see citing works
Bode, H. R., & Steele, R. E. (1989) · Science · doi:10.1126/science.243.4890.549 · 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-citationThe photobiology of Hydra’s periodic activity
Taddei-Ferretti, C., Musio, C., Santillo, S., & Cotugno, A. (2004) · Hydrobiologia · doi:10.1007/s10750-004-2680-6 · Cited by 15 · see citing works
Westfall, J. A., & Sayyar, K. L. (1997) · Journal of Morphology · doi:10.1002/(sici)1097-4687(199705)232:2 · Cited by 15 · see citing works
Self-citationNielsen, S. K. D., Koch, T. L., Wiisbye, S. H., Grimmelikhuijzen, C. J. P., & Garm, A. L. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25133 · Cited by 14 · see citing works
Nerve net formation in the primitive nervous system of Hydra — an overview
Koizumi, O., Mizumoto, H., Sugiyama, T., & Bode, H. R. (1990) · Neuroscience Research Supplements · doi:10.1016/0921-8696(90)90046-6 · Cited by 15 · see citing works
Westfall, J. A., Argast, D. R., & Kinnamon, J. C. (1983) · Journal of Morphology · doi:10.1002/jmor.1051780202 · Cited by 15 · see citing works
Self-citationA single layer of microtubules is part of a complex cytoskeleton in mature nematocytes of hydra
Stidwill, R. P., & Honegger, T. G. (1989) · Tissue and Cell · doi:10.1016/0040-8166(89)90062-1 · Cited by 15 · see citing works
The Discovery, Proof and Reproof of Neurosecretion: (Speidel, 1917; Scharrer and Scharrer, 1934)
Sarnat, H. B. (1983) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100044954 · Cited by 14 · 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
- Authors
- Westfall, J. A., & Kinnamon, J. C.
- Affiliations
- Kansas State University (US)
- ORCID
- Kinnamon, John C.
- Venue
- Journal of Neurocytology
- Published
- 1978-06
- Volume
- 7
- Issue
- 3
- Pages
- 365-379
- ISSN
- 0300-4864 (ISSN-L)
- 1573-7381
- OpenAlex
- W2355562841
- Cited by
- 140
- References
- 31
- Citations by year
- 2025: 1 · 2023: 4 · 2021: 2 · 2019: 1 · 2017: 2 · 2016: 2 · 2015: 4 · 2014: 2 · 2013: 1 · 2012: 2
- FWCI
- 7.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Neurocytology (publishedVersion)
- PubMed (publishedVersion)
- 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 › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
- Keywords
- Hydra, neurosecretory granules, stereocilia, synaptic connectivity, nematocytes, epitheliomuscular cells, nerve net, dense core vesicles, cnidarian nervous system
- MeSH terms
- Animals, Axons, Cilia, Cytoplasmic Granules, Biological Evolution, Hydra, Interneurons, Microscopy, Electron, Synaptic Transmission, Neurosecretion, Synapses
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