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The synaptic organization of the prepacemaker nucleus in weakly electric knifefish,Eigenmannia: A quantitative ultrastructural study

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Journal of Neurocytology

Summary

Weakly electric knifefish (Eigenmannia sp.) produce continuous electric organ discharges at very constant frequencies. Modulations of the discharges occur during social interactions and are under control of the diencephalic prepacemaker nucleus. Abrupt frequency modulations, or ‘chirps’, which are observed predominantly during the breeding season, can be elicited by stimulation of neurons in a ventro-lateral portion of the prepacemaker nucleus, the so-called PPn-C. The PPn-C consists of approximately 100 loosely scattered large multipolar neurons which send dendrites into three territories, called ‘dorso-medial’, ‘dorso-lateral’, and ‘Ventral’. In the present ultrastructural investigation, the synaptic organization of these neurons, identified by retrograde labelling with horseradish peroxidase, was studied quantitatively.

Somata and dendrites of the PPn-C receive input from two classes of chemical synapses. Class-1 boutons contain predominantly agranular, round vesicles and are believed to be excitatory. Class-2 boutons display predominantly flattened or pleiomorphic vesicles and are probably inhibitory. The action of the agranular vesicles in the synaptic boutons of these two classes may be modulated by the content of large dense-core vesicles. These comprise approximately 1% of the total vesicle population and are found predominantly in regions distant from the active zone of the synaptic bouton.

The density of chemical synapses exhibits marked topographic differences. Class-1 boutons occur typically at densities of 3–12 synapses per 100 μm of profile length on dendrites and cell bodies. No significant differences in density of class-1 boutons could be found between distal dendrites of the three territories, proximal dendrites and cell bodies. The density of class-2 synapses, on the other hand, increases significantly from usually less than 1 synapse per 100 μm of profile length on distal dendrites to 2–3 synapses per 100 μm of profile length on proximal dendrites and cell bodies.

Such a topographic organization could enable the proximal elements to ‘veto’ the depolarizing response of distal dendrites to excitatory inputs. The growth of dendrites in the dorso-medial territory during the breeding season, as shown in a previous study, and the concurrent doubling of excitatory input received by class-1 synapses, could overcome the inhibition caused on somata and proximal dendrites by class-2 synapses and thus account for the dramatic increase in the fish's propensity to chirp in the context of sexual maturity.

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References

  • Adams, J. C. (1981) Heavy metal intensification of DAB-based HRP reaction product.Journal of Histochemistry and Cytochemistry 29, 775.

    Google Scholar 

  • Bastian, J. &Yuthas, J. (1984) The jamming avoidance response ofEigenmannia: properties of a diencephalic link between sensory processing and motor output.Journal of Comparative Physiology A 154, 895–908.

    Google Scholar 

  • Bennett, M. V. L. (1971) Electric organs. InFish Physiology, Volume 5 (edited byHoar, W. S. &Randall, D. J.) pp. 347–491. New York: Academic Press.

    Google Scholar 

  • Bennett, M. V. L., Pappas, G. D., Giménez, M. &Nakajima, Y. (1967) Physiology and ultrastructure of electrotonic junctions. IV. Medullary electromotor nuclei in gymnotid fish.Journal of Neurophysiology 30, 236–300.

    Google Scholar 

  • Bodian, D. (1966) Synaptic types on spinal motoneurons: an electron microscopic study.Bulletin of the Johns Hopkins Hospital 119, 16–45.

    Google Scholar 

  • Carrer, H. F. &Aoki, A. (1982) Ultrastructural changes in the hypothalamic ventromedial nucleus of ovariec-tomized rats after estrogen treatment.Brain Research 240, 221–33.

    Google Scholar 

  • Chan-Palay, V. (1978) The paratrigeminal nucleus: I. Neurons and synaptic organization.Journal of Neurocytology 7, 405–18.

    Google Scholar 

  • Colonnier, M. (1974) Spatial interrelationships as physiological mechanisms in the central nervous system. InEssays on the Nervous System (edited byBellairs, R. &Gray, E. G.) pp. 344–66. Oxford: Clarendon Press.

    Google Scholar 

  • Colonnier, M. (1981) The electron-microscopic analysis of the neuronal organization of the cerebral cortex. InThe Organization of the Cerebral Cortex (edited bySchmitt, F. O., Worden, F. O., Adelman, G. &Dennis, S. G.) pp. 125–55. Cambridge: The MIT Press.

    Google Scholar 

  • Dye, J. C. (1988) Anin vitro physiological preparation of a vertebrate communicatory behavior: chirping in the weakly electric fish,Apteronotus.Journal of Comparative Physiology A 163, 445–58.

    Google Scholar 

  • Dye, J. C. &Meyer, J. H. (1986) Central control of the electric organ discharge in weakly electric fish. InElectroreception (edited byBullock, T. H. &Heiligenberg, W.) pp. 71–102. New York: John Wiley & Sons.

    Google Scholar 

  • Dye, J., Heiligenberg, W., Keller, C. H. &Kawasaki, M. (1989) Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus.Proceedings of the National Academy of Sciences (USA) 86, 8993–7.

    Google Scholar 

  • Elekes, K. &Szabo, T. (1985) Synaptology of the medullary command (pacemaker) nucleus of the weakly electric fish(Apteronotus leptorhynchus) with particular reference to comparative aspects.Experimental Brain Research 60, 509–20.

    Google Scholar 

  • Ellis, D. B. &Szabo, T. (1980) Identification of different cell types in the command (pacemaker) nucleus of several gymnotiform species by retrograde transport of horseradish peroxidase.Neuroscience 5, 1917–29.

    Google Scholar 

  • Goldsmith, P. C. (1977) Ultrastructural localization of some hypothalamic hormones.Federation Proceedings 36, 1968–72.

    Google Scholar 

  • Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study.Journal of Anatomy 93, 420–33.

    Google Scholar 

  • Gray, E. G. (1969a) Electron microscopy of excitatory and inhibitory synapses: a brief review.Progress in Brain Research 31, 141–4.

    Google Scholar 

  • Gray, E. G. (1969b) Round and flat synaptic vesicles in the fish central nervous system. InCellular Dynamics of the Neuron. Symposia of the International Society for Cell Biology, Volume 8 (edited byBarondes, S. H.) pp. 211–27. New York: Academic Press.

    Google Scholar 

  • Hagedorn, M. (1986) The ecology, courtship, and mating of gymnotiform electric fish. InElectroreception (edited byBullock, T. H. &Heiligenberg, W.) pp. 497–525. New York: John Wiley & Sons.

    Google Scholar 

  • Hagedorn, M. &Heiligenberg, W. (1985) Court and spark: electric signals in the courtship and mating of gymnotid fish.Animal Behaviour 33, 254–65.

    Google Scholar 

  • Heiligenberg, W., Finger, T., Matsubara, J. &Carr, C. (1981) Input to the medullary pacemaker nucleus in the weakly electric fish,Eigenmannia (Sternopygidae, Gymnotiformes).Brain Research 211, 418–23.

    Google Scholar 

  • Heiligenberg, W., Keller, C. H., Metzner, W. &Kawasaki, M. (1991) Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fishEigenmannia: detection and processing of electric signals in social communication.Journal of Comparative Physiology A, in press.

  • Hökfelt, T., Johansson, O., Ljungdahl, A., Lundberg, J. M. &Schultzberg, M. (1980a) Peptidergic neurons.Nature 284, 515–21.

    Google Scholar 

  • Hökfelt, T., Lundberg, J. M., Schultzberg, M., Johansson, O., Ljungdahl, Å., &Rehfeld, K. (1980b) Coexistence of peptides and putative transmitters in neurons. InNeural Peptides and Neuronal Communication (edited byCosta, E. &Trabucchi, M.) pp. 1–23. New York: Raven Press.

    Google Scholar 

  • Hopkins, C. D. (1974) Electric communication: functions in the social behavior ofEigenmannia virescens.Behaviour 50, 270–305.

    Google Scholar 

  • Hopkins, C. D. (1988) Neuroethology of electric communication.Annual Review of Neuroscience 11, 497–535.

    Google Scholar 

  • Johnston, S. A., Maler, L. &Tinner, B. (1990) The distribution of serotonin in the brain ofApteronotus leptorhynchus: an immunohistochemical study.Journal of Chemical Neuroanatomy 3, 429–65.

    Google Scholar 

  • Kandel, E. R. &Schwartz, J. H. (1982) Molecular biology of learning: modulation of transmitter release.Science 218, 433–43.

    Google Scholar 

  • Kawasaki, M. &Heiligenberg, W. (1988) Individual prepacemaker neurons can modulate the pacemaker cycle of the gymnotiform electric fish,Eigenmannia.Journal of Comparative Physiology A 162, 13–21.

    Google Scholar 

  • Kawasaki, M., Maler, L., Rose, G. J. &Heiligenberg, W. (1988) The anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus.Journal of Comparative Neurology 276, 113–31.

    Google Scholar 

  • Keller, C. H. (1988) Stimulus discrimination in the diencephalon ofEigenmannia: the emergence and sharpening of a sensory filter.Journal of Comparative Physiology A 162, 747–57.

    Google Scholar 

  • Keller, C. H. &Heiligenberg, W. (1989) From distributed sensory processing to discrete motor representations in the diencephalon of the electric fish,Eigenmannia.Journal of Comparative Physiology A 164, 565–76.

    Google Scholar 

  • Keller, C. H., Maler, L. &Heiligenberg, W. (1990) Structural and functional organization of a diencephalic sensory-motor interface in the gymnotiform fish,Eigenmannia.Journal of Comparative Neurology 293, 347–76.

    Google Scholar 

  • Koch, C., Marroquin, J. &Yuille, A. (1986) Analog ‘neuronal’ networks in early vision.Proceedings of the National Academy of Sciences (USA) 83, 4263–7.

    Google Scholar 

  • Krieger, D. T. (1983) Brain peptides: what, where, and why?Science 222, 975.

    Google Scholar 

  • Lamprecht, J. (1988) Aufbereitung und Darstellung wissenschaftlicher Ergebnisse. InPraktische Verhaltensbiologie (edited byZupanc, G. K. H.) pp. 243–54. Berlin: Verlag Paul Parey.

    Google Scholar 

  • Larramendi, L. M. H. &Victor, T. (1967) Synapses on the Purkinje cell spines in the mouse. An electron microscope study.Brain Research 5, 15–30.

    Google Scholar 

  • Lundberg, J. M. &Hökfelt, T. (1983) Coexistence of peptides and classical neurotransmitters.Trends in Neurosciences 6, 325–33.

    Google Scholar 

  • Lundquist, J. &Josefsson, J. (1971) Sensitive method for determination of peroxidase activity in tissue by means of coupled oxidation reaction.Analytical Biochemistry 41, 567–77.

    Google Scholar 

  • Maler, L. &Ellis, W. G. (1987) Inter-male aggressive signals in weakly electric fish are modulated by monoamines.Behavioural Brain Research 25, 75–81.

    Google Scholar 

  • Maler, L., Boland, M., Patrick, J. &Ellis, W. (1984) Localization of zinc in the pacemaker nucleus of highfrequency gymnotid fish. InThe Neurobiology of Zinc, Part A: Physiochemistry, Anatomy, and Techniques (edited byFrederickson, C. J., Howell, G. A. &Kasarskis, E. J.) pp. 199–212. New York: Alan R. Liss.

    Google Scholar 

  • Mannen, H. (1966) Contribution to the morphological study of dendritic arborization in the brain stem. InCorrelative Neurosciences (edited byTokizane, T. &Schade, J. P.) pp. 131–62. New York: Elsevier.

    Google Scholar 

  • McLaughlin, B. J., Wood, H. G., Saito, K., Barber, R., Roberts, E. &Wu, J. -Y. (1974) Fine structural localization of glutamic acid decarboxylase in adult and developing cerebellum in rodents.Anatomical Record 178, 407–8.

    Google Scholar 

  • Mintz, J., Gotow, T., Triller, A. &Korn, H. (1989) Effect of serotonergic afferents on quantal release at central inhibitory synapses.Science 245, 190–2.

    Google Scholar 

  • Pelletier, G., Labrie, F., Arimura, A. &Schally, A. V. (1974) Electron microscopic immunohistochemical localization of growth hormone-release inhibiting hormone (somatostatin) in the rat median eminence.American Journal of Anatomy 140, 445–50.

    Google Scholar 

  • Peters, A., Palay, S. L. &Webster, H. deF. (1976)The Fine Structure of the Nervous System. The Neurons and Supporting Cells. Philadelphia: W. B. Saunders.

    Google Scholar 

  • Pickel, V. M., Beckley, S. C., Joh, T. H. &Reis, D. J. (1981) Ultrastructural immunocytochemical localization of tyrosine hydroxylase in the neostriatum.Brain Research 225, 373–85.

    Google Scholar 

  • Reynolds, E. S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.Journal of Cell Biology 17, 208–12.

    Google Scholar 

  • Sas, E. &Maler, L. (1991) Somatostatin-like immunoreactivity in the brain of an electric fish (Apteronotus leptorhynchus) identified with monoclonal antibodies.Journal of Chemical Neuroanatomy 4, 155–86.

    Google Scholar 

  • Scheller, R. H., Kaldany, R. -R., Kreiner, T., Mahon, A. C., Nambu, J. R., Schaefer, M. &Taussig, R. (1984) Neuropeptides: mediators of behavior inAplysia.Science 225, 1300–8.

    Google Scholar 

  • Schumacher, M., Coirini, H. &McEwen, B. S. (1989) Regulation of high-affinity GABAa receptors in specific brain regions by ovarian hormones.Neuroendocrinology 50, 315–20.

    Google Scholar 

  • Shepherd, G. M. (1988)Neurobiology 2nd ed. New York: Oxford University Press.

    Google Scholar 

  • Siegel, S. (1956)Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill.

    Google Scholar 

  • Snyder, S. H. &Innis, R. B. (1979) Peptide neurotransmitters.Annual Review of Biochemistry 48, 755–82.

    Google Scholar 

  • Sossin, W. S., Kirk, M. D. &Scheller, R. H. (1987) Peptidergic modulation of neuronal circuitry controlling feeding inAplysia.Journal of Neuroscience 7, 671–81.

    Google Scholar 

  • Szabo, T. &Enger, P. S. (1964) Pacemaker activity of the medullary nucleus controlling electric organs in highfrequency gymnotid fish.Zeitschrift für vergleichende Physiologie 49, 285–300.

    Google Scholar 

  • Szabo, T., Heiligenberg, W. &Ravaille-Veron, M. (1989) HRP labeling and ultrastructural localization of prepacemaker terminals within the medullary pacemaker nucleus of the weakly electric gymnotiform fishApteronotus leptorhynchus.Journal of Comparative Neurology 284, 169–73.

    Google Scholar 

  • Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat.Nature 207, 642–3.

    Google Scholar 

  • Uchizono, K. (1967) Inhibitory synapses on the stretch receptor neurone of the crayfish.Nature 214, 833–4.

    Google Scholar 

  • Uchizono, K. (1968) Axon identification in the cerebellar cortex of the cat.Archivum Histologicum Japonicum 29, 399–124.

    Google Scholar 

  • Uchizono, K. (1969) Synaptic organization of the mammalian cerebellum. InNeurobiology of Cerebellar Evolution and Development.Proceedings of the First International Symposium of the Institute for Biomedical Research — American Medical Association/Education & Research Foundation (edited byLlinás, R. R.) pp. 549–83. Chicago: American Medical Association.

    Google Scholar 

  • Uchizono, K. (1975)Excitation and Inhibition. Synaptic Morphology. Tokyo: Igaku Shoin; Amsterdam: Elsevier.

    Google Scholar 

  • Walberg, F. (1966) The fine structure of the cuneate nucleus in normal cats and following interruption of afferent fibers.Experimental Brain Research 2, 107–28.

    Google Scholar 

  • Weld, M. M. &Maler, L. (1991) Substance P-like immunoreactivity in the brain of the gymnotiform fishApteronotus leptorhynchus: presence of sex differences.Journal of Chemical Neuroanatomy, in press.

  • Whittaker, V. P. &Gray, E. G. (1962) The synapse: biology and morphology.British Medical Bulletin 18, 223–8.

    Google Scholar 

  • Zieglgänsberger, W. &Champagnat, J. (1979) Cat spinal motoneurones exhibit topographic sensitivity to glutamate and glycine.Brain Research 160, 95–104.

    Google Scholar 

  • Zupanc, G. K. H. &Heiligenberg, W. (1989) Sexual maturity-dependent changes in neuronal morphology in the prepacemaker nucleus of adult weakly electric knifefish,Eigenmannia.Journal of Neuroscience 9, 3816–27.

    Google Scholar 

  • Zupanc, G. K. H., Maler, L. &Heiligenberg, W. (1991) Somatostatin-like immunoreactivity in the region of the prepacemaker nucleus in weakly electric knifefish, Eigenmannia:A quantitative analysis.Brain Research, in press.

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  1. Department of Neurosciences, School of Medicine, and Neurobiology Unit, Scripps Institution of Oceanography, University of California at San Diego, 92093-0202, La Jolla, California, USA

    G. K. H. Zupanc

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Zupanc, G.K.H. The synaptic organization of the prepacemaker nucleus in weakly electric knifefish,Eigenmannia: A quantitative ultrastructural study. J Neurocytol 20, 818–833 (1991). https://doi.org/10.1007/BF01191733

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