Summary
This study was made to identify the inhibitory interneurons belonging to the spinal circuitry activated by the Mauthner axons in the tench (Tinea tinea L.). The histological investigations were focused on a segmentai pair of commissural interneurons that were reconstructedin toto from their distinguishing topographical and ultrastructural features. These features are: (a) the adendritic soma located 100–150 μm dorsal to the central canal; (b) the first node of Ranvier which is precommissural and connected to the ipsilateral Mauthner axon via gap junction; (c) the second node of Ranvier, from which two first-order branches arise postcommissurally each supplying roughly the rostral and caudal half of the contralateral spinal cord segment; (d) their second-order branches, which arise at intervals that correspond closely to those of the Mauthner axon collaterals; (e) the postsynaptic targets of the second-order branches, which are exclusively all the motoneurons and interneurons innervated by the contralateral Mauthner axon; (f) the axon terminals of these branches, which contain F-type vesicles, form Gray type-2 synapses, and abut either on the initial segment or on the first node of Ranvier of the target neurons. Thus, it appears that this segmental interneuron has all the appropriate features that could provide the structural basis for the reciprocal fast-acting inhibitory coupling underlying the startle reflex elicited by the Mauthner neurons in response to auditory stimuli.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson, P., Eccles, J. C. &Voorhoeve, P. E. (1963) Inhibitory synapses on somas of Purkinje cells in the cerebellum.Nature 199, 655–6.
Auerbach, A. A. &Bennett, M. V. L. (1969) Chemically mediated transmission of a giant fibre synapse in the central nervous system of a vertebrate.Journal of General Physiology 53, 183–237.
Barets, A. (1961) Contribution a l'étude des systèmes moteurs ‘lents’ et ‘rapides’ du muscle latéral des téléostéens.Archives d'Anatomie Microscopique et de Morphologie Expérimentale 50, 91–187.
Baumann, I. R. &Yasargil, G. M. (1979) Action of strychnine on a postsynaptic inhibition in tench spinal cord.Experientia 35, 916.
Bennett, M. V. L. (1977) Electric transmission: a functional analysis and comparison to chemical transmission. InHandbook of Physiology, the Nervous System (edited byBrookhart, I. J. M. &Mountcastle, V. B.) pp. 357–416. Bethesda, MD: American Physiological Society.
Celio, M. R., Gray, E. G. &Yasargil, G. M. (1976) Ultrastructure of the Mauthner axon collateral and its synapses in the goldfish spinal cord.Journal of Neurocytology 8, 19–29.
Cobb, J. L. S., Fraser, K. &Heitler, W. J. (1985) Comparative ultrastructure of identified electrical synapses in the crayfish.Journal of Physiology 367, 87.
Diamond, J. (1971) The Mauthner cell. InFish Physiology (edited byHoar, W. S. &Randall, D. J.) Vol.5, pp. 265–346. New York: Academic Press.
Diamond, J. &Yasargil, G. M. (1969) Synaptic function in fish spinal cord: dendritic integration.Progress in Brain Research 31, 201–9.
Emre, M. (1983) Histology and electrophysiology of a fast-operating inhibitory pathway in the spinal cord of the Tench (Tinea tinea L.). MD Thesis, University of Zürich.
Emre, M., Saydam, B. &Yasargil, G. M. (1983) Morphological correlates of spinal pathways mediating the Mauthner-cell-induced excitation and inhibition of spinal motoneurons.Experientia 39, 632.
Faber, D. S. &Korn, H. (1978) Electrophysiology of the Mauthner Cell: Basic properties, synaptic mechanisms and associated networks. InNeurobiology of the Mauthner cell (edited byFaber, D. S. &Korn, H.) pp. 47–131. New York: Raven Press.
Fetcho, J. R. &Faber, D. S. (1987) Spinal interneurons that may mediate the crossed inhibition during a Mauthner-initiated escape behaviour in goldfish.Society of Neuroscience Abstracts 13, 823.
Fetcho, J. R. &Faber, D. S. (1988) Identification of motoneurons and interneurons in the spinal network for escapes initiated by the Mauthner cell in goldfish.Journal of Neurosciences 8, 4192–213.
Furukawa, T. &Furshpan, E. J. (1963) Two inhibitory mechanisms in the Mauthner neurons of goldfish.Journal of Neurophysiology 26, 140–76.
Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex. An electron microscope study.Journal of Anatomy 93, 420–33.
Gray, E. G. (1969) Round and flat synaptic vesicles in the fish central nervous system. InSymposium of the International Society for Cell Biology (edited byS. H. Barondes) Vol. 8, pp. 211–27. New York: Academic Press.
Greeff, N. G. (1977) Passive elektrische Eigenschaften einer markhaltigen Riesennervenfaser im Zentralnervensystem (Mauthner-Axon der Schleie). MD Thesis, University of Zürich.
Hackett, J. T. &Faber, D. S. (1983) Mauthner axon networks mediating supra-spinal components of the startle response in the goldfish.Neuroscience 8, 317–33.
Highstein, S. M. &Bennett, M. V. L. (1975) Fatigue and recovery of transmission at the Mauthner fibre-giant fibre synapse of the hatchet fish.Brain Research 98, 229–42.
Horridge, A. (1961) The organization of the primitive central nervous system as suggested by examples of inhibition and the structure of neuropile. InNervous Inhibition (edited byFlorey, E.) pp. 395–409. Oxford: Pergamon Press.
Korn, H., Triller, A. &Faber, D. S. (1978) Structural correlates of recurrent collateral interneurons producing both electrical and chemical inhibitions of the Mauthner cell.Proceedings of the Royal Society of London 202, 533–8.
Moor, H. &Muehlethaler, K. (1963) Fine structure in frozen-etched yeast cells.Journal of Cell Biology 17, 609–28.
Mugnaini, E. &Maler, L. (1987) Cytology and immunochemistry of the nucleus of the lateral line lobe in the electric fishGnathonemus petersii (Mormyridae): evidence suggesting that GABAergic synapses mediate an inhibitory corollary discharge.Synapse 1, 32–56.
Peters, A., Palay, S. L. &Webster, H. deF. (1976) The fine structure of the nervous system: The neurons and supporting cells. Philadelphia: Saunders.
Roberts, A. &Clarke, J. D. (1982) The neuroanatomy of an amphibian embryo spinal cord.Philosophical Transactions of the Royal Society of London B296, 192–212.
Rossi, A. &Palombi, F. (1969) A neurofibrillar body in the perikaryon of nervus terminalis ganglion cells in teleosts.Zeitschrift für Zellforschung und mikroskopische Anatomie 93, 395–403.
Sotelo, C. &Palay, S. L. (1968) The fine structure of the lateral vestibular nucleus in the rat. I. Neurons and neuroglial cells.Journal of Cell Biology 36, 151–79.
Stewart, W. W. (1978) Functional connections between cells as revealed by dye-coupling with highly fluorescent naphtalamide tracer.Cell 14, 741–59.
Stefanelli, A. (1951) The Mauthnerial apparatus in the Ichthyopsida; its nature and function and correlated problems of neurohistogenesis.Quarterly Review of Biology 26, 17–34.
Stolinski, C., Breathnach, A. S., Martin, B., Thomas, P. K., King, R. H. M. &Gabriel, G. (1981) Associated particle aggregates in juxtaparanodal axolemma and adaxonal Schwann cell membrane of rat peripheral nerve.Journal of Neurocytology 10, 679–91.
Tasaki, I. (1953)Nervous transmission. Springfield, Illinois: Charles C. Thomas, pp. 81–85.
Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat.Nature 207, 642–43.
Yasargil, G. M. &Diamond, J. (1968) Startle-response in teleost fish: an elementary circuit for neural discrimination.Nature 220, 241–3.
Yasargil, G. M. &Sandri, C. (1987) Morphology of the Mauthner axon inhibitory system in tench (Tinea tinea L.) spinal cord.Neuroscience Letters 81, 63–8.
Yasargil, G. M., Akert, K. &Sandri, C. (1986) Further morphological (freeze-fracture) evidence for an impulse generating function of Mauthner axon collaterals in the tench (Tinea tinea L.) spinal cord.Neuroscience Letters 71, 43–7.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Yasargil, G.M., Sandri, C. Topography and ultrastructure of commissural interneurons that may establish reciprocal inhibitory connections of the Mauthner axons in the spinal cord of the tench,Tinca tinca L. . J Neurocytol 19, 111–126 (1990). https://doi.org/10.1007/BF01188443
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01188443