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Synaptic and electotonic contacts on primary afferent axons in the lamprey Lampetra fluviatilis spinal cord

  • Comparative and Ontogenic Physiology
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Abstract

Distribution of GABA and glycine immunoreactivity was studied in synapses on primary afferent axons of the lamprey Lampetra fluviatilis spinal cord using a double labelling technique. Approximately 25% of synapses exhibit GABA immunoreactivity, while more than 70% are immunoreactive to both neurotransmitters. As in other vertebrates, axo-axonal contacts represent three-component synaptic complexes, the so-called triads, where the immunoreactive terminal make synaptic contact simultaneously with the afferent axon and the dendrite contacting this afferent. Contact zones with gap junction-like cell membrane specializations were found between adjacent afferents suggesting the presence of electrotonic interaction between them. This interaction appears to serve for the synchronization of the afferent flow and represents a structural correlate of the mechanism of rapid interneuronal communication between functionally uniform neurons, which is an important element in the organization of coordinated locomotor acts. Besides, our studies provide evidence that afferent–afferent interaction may be mediated not only electrotonically but also with the aid of chemical synapses. This finding suggests that glutamate-induced depolarization of primary afferents results not only from autoreception but also from the direct effect of glutamate on the afferent’s cell membrane.

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References

  1. Kappers, A.C.U., Huber, G.C., and Crosby, E.C., The Comparative Anatomy of Central Nervous System of Vertebrates, Including Man, New York, 1960.

    Google Scholar 

  2. Nieuwenhuys, R., Comparative anatomy of spinal cord, Progr. Brain Res., 1964, vol. 11, pp. 1–57.

    Article  CAS  Google Scholar 

  3. Brodin, L., Christenson, J., and Grillner, S., Single sensory neurons activate excitatory amino acid receptors in the lamprey spinal cord, Neurosci. Lett., 1987, vol. 75, pp. 75–79.

    Article  CAS  PubMed  Google Scholar 

  4. Fernandez-Lopez, B., Villar-Cervino, V., Valle-Maroto, S.M., Barreiro-Iglesias Anadon, R., and Rodicio, M.C., The glutamatergic neurons in the spinal cord of the sea lamprey: an in situ hybridization and immunohistochemical study, PLoS ONE, 2012, vol. 7, pp. 1–15.

    Google Scholar 

  5. Christenson, J., Shupliakov, O., Cullheim, S., and Grillner, S., Possible morphological substrates for GABA-mediated presynaptic inhibition in the lamprey spinal cord, J. Comp. Neurol., 1993, vol. 328, pp. 463–472.

    Article  CAS  PubMed  Google Scholar 

  6. Adanina, V.O., Rio, J.-P., Repérant, J., and Vesselkin, N.P., Immunoreactivity of synapses on the primary afferent axons and sensory neurons in the spinal cord of Lampetra fluviatilis, Tsitol., 2008, vol. 50, pp. 947–952.

    CAS  Google Scholar 

  7. Christenson, J. and Grillner, S., Primary sensory transmission is modulated through activation of presynaptic GABAB receptors in the spinal cord, Eur. J. Neurosci., 1989, Suppl. 2, 53. 4.

    Google Scholar 

  8. Alford, S. and Grillner, S., The involvement of GABAB receptors and coupled G-proteins in spinal GABA-ergic presynaptic inhibition, J. Neurosci., 1991, vol. 11, pp. 3718–3726.

    CAS  PubMed  Google Scholar 

  9. Batueva, I.V., Tsvetkov, E.A., Sagatelian, A.K., Buchanan, J.T., Vesselkin, N.P., Adanina, V.O., Suderevskaya, E.I., Rio, J.-P., and Repérant, J., Physiological and morphological corellates of presynaptic inhibition in primary afferents of the lamprey spinal cord, J. Neurosci., 1999, vol. 88, pp. 975–987.

    Article  CAS  Google Scholar 

  10. Stuart, G.J. and Redman, S.J., The role of GABAA and GABAB receptors in presynaptic inhibition of 1a EPSPs in cat spinal motoneurones, J. Physiol., 1992, vol. 447, pp. 675–692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Liu, H., Wang, H., Sheng, M., Jan, L.Y., Jan, Y.N., and Basbaum, A.I., Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn, Proc. Natl. Acad Sci. USA., 1994, vol. 91, pp. 8383–8387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kerchner, G.A., Wilding, T.J., Li, P., Zhuo, M., and Huettner, J.E., Presynaptic kainate receptors regulate spinal sensory transmission, J. Neurosci., 2001, vol. 21, pp. 59–66.

    CAS  PubMed  Google Scholar 

  13. Lee, C.J., Bardoni, R., Tong, C.K., Engelman, H.S., Joseph, D.L., and MacDermot, A.B., Functional expression of AMPA receptors on central terminals of rat dorsal root ganglion neurons and presynaptic inhibition of glutamate release, Neuron, 2002, vol. 35, pp. 135–146.

    Article  CAS  PubMed  Google Scholar 

  14. Lu, Ch.-R., Hwang, S.J., Phend, K.D., Rustioni, A., and Valtschanoff, A., Primary afferent terminals in spinal cord express presynaptic AMPA receptors, J. Neurosci., 2002, vol. 22, pp. 9522–9529.

    CAS  PubMed  Google Scholar 

  15. Adams, J.C., Heavy metal identification of DABbased HRP reaction product, J. Histochem. Cytochem., 1981, vol. 29, p. 775.

    Article  CAS  PubMed  Google Scholar 

  16. Gray, E.G., A morphological basis for pre-synaptic inhibition, Nature (Lond.), 1962, vol. 193, pp. 82–83.

    Article  CAS  Google Scholar 

  17. Lamotte D’Incamps, B., Destombes, J., Thiesson, D., Hellio, R., Lasserre, X., Kouchtir-Devanne, N., Jami, L., and Zytnicki, D., Indication for GABA-immunoreactive axo-axonic contacts on the intraspinal arborization of a 1b fiber in cat: a confocal microscope study, J. Neurosci., 1998, vol. 18, pp. 10030–10036.

    PubMed  Google Scholar 

  18. Maxwell, D.J. and Riddell, J.S., Axo-axonic synapses on terminals of group 1a muscle spindle afferent axons in the spinal cord of the cat, Eur. J. Neurosci., 1999, vol. 11, pp. 2151–2159.

    Article  CAS  PubMed  Google Scholar 

  19. Watson, A.H., Hughes, D.I., and Bazzaz, A.A., Synaptic relationships between hair follicle afferents and neurones expressing GABA and glycinelike immunoreactivity in the spinal cord of the rat, J. Comp. Neurol., 2002, vol. 452, pp. 367–380.

    Article  CAS  PubMed  Google Scholar 

  20. Adanina, V.O., Rio, J.-P., Adanina, A.S., Repérant, J., and Vesselkin, N.P., GABA- and glycine immunoreactive synapses in the spinal cord of the frog Rana temporaria, Tsitol., 2010, vol. 4, pp. 380–390.

    Google Scholar 

  21. Eccles, J.C., Schmidt, R.F., and Willis, W.D., Pharmacological studies on presynaptic inhibition, J. Physiol. (Lond.), 1963, vol. 168, pp. 500–530.

    Article  CAS  Google Scholar 

  22. Nishi, S., Minota, S., and Karczmar, A.G., Primary afferent neurons: the ionic mechanism of GABA-mediated depolarization, Neuropharmacology, 1974, vol. 13, pp. 215–219.

    Article  CAS  PubMed  Google Scholar 

  23. Levy, R.A., The role of GABA in primary afferent depolarization, Prog. Neurobiol., 1977, vol. 9, pp. 211–267.

    Article  CAS  PubMed  Google Scholar 

  24. Rudomin, P. and Schmidt, R.F., Presynaptic inhibition in the vertebrate spinal cord revisited, Exp. Brain Res., 1999, vol. 129, pp. 1–37.

    Article  CAS  PubMed  Google Scholar 

  25. Grunewald, B. and Geis, C., Measuring spinal presynaptic inhibition in mice by dorsal root potential recording in vivo, J. Vis. Exp., 2014, vol. 85. doi: 10.3791/51473.

  26. Watson, A.H. and Bazzaz, A.A., GABA and glycine like immunoreactivity at axo-axonic synapses on 1a muscle afferent terminals in the spinal cord of the rat, J. Comp. Neurol., 2001, vol. 433, pp. 335–348.

    Article  CAS  PubMed  Google Scholar 

  27. Sutherland, F.I., Bannatyne, B.A., Kerr, R., Riddell, J.S., and Maxwell, D.J., Inhibitory amino acid transmitters associated with axons in presynaptic apposition to cutaneous primary afferent axons in the cat spinal cord, J. Comp. Neurol., 2002, vol. 452, pp. 154–162.

    Article  CAS  PubMed  Google Scholar 

  28. Reichenberger, L. and Dieringer, N., Colocalization of glycine and glutamate immunoreactivity in frog and rat vestibular afferents, J. Comp. Neurol., 1994, vol. 349, pp. 603–614.

    Article  CAS  PubMed  Google Scholar 

  29. Dumba, J.S., Irish, P.S., Anderson, N.L., and Westrum, L.E., Electron microscopic analysis of gamma-aminobutyric acid and glycine colocalization in rat trigeminal subnucleus caudalis, Brain Res., 1998, vol. 806, pp. 16–25.

    Article  CAS  PubMed  Google Scholar 

  30. Tebecis, A.K. and Phillis, J.W., The use of convulsants in studying possible functions of amino acids in the toad spinal cord, Comp. Biochem. Physiol., 1969, vol. 28, pp. 1303–1315.

    Article  CAS  PubMed  Google Scholar 

  31. Thomson, A.M., Glycine is a co-agonist at the NMDA receptor/ channel complex, Prog. Neurobiol., 1990, vol. 35, pp. 53–74.

    Article  CAS  PubMed  Google Scholar 

  32. Danysz, W. and Parsons, C.G., Glycine and NMethyl- d-Aspartate receptors: physiological significance and possible therapeutic applications, Pharmacol. Rev., 1998, vol. 50, pp. 597–664.

    CAS  PubMed  Google Scholar 

  33. Rovainen, C.M., Synaptic interactions of identified nerve cells in the spinal cord of the sea lamprey, J. Comp. Neurol., 1974, vol. 154, pp. 189–206.

    Article  CAS  PubMed  Google Scholar 

  34. Christensen, B.N., Morphological correlates of synaptic transmission in lamprey spinal cord, J. Neurophysiol., 1976, vol. 39, pp. 197–212.

    CAS  PubMed  Google Scholar 

  35. Christenson, J. and Grillner, S., Primary afferents evoke excitatory amino acid receptor-mediated EPSPs that are modulated by presynaptic GABAb receptors in lamprey, J. Neurophysiol., 1991, vol. 66, pp. 2141–2149.

    CAS  PubMed  Google Scholar 

  36. Adanina, V.O., Vesselkin, N.P., Rio, J.-P., and Repérant, J., Organization of motoneurons in the sturgeon spinal cord, Zh. Evol. Biokhim. Fiziol., 1996, vol. 32, pp. 605–612.

    Google Scholar 

  37. Sotelo, C. and Taxi, J., Ultrastructural aspects of electrotonic junctions in the spinal cord of the frog, Brain Res., 1970, vol. 17, pp. 137–141.

    Article  CAS  PubMed  Google Scholar 

  38. Matthews, M.A., Willis, W.D., and Williams, V., Dendrite bundles in lamina IX of cat spinal cord: a possible source for electrical interaction between motoneurons, Anat. Rec., 1971, vol. 171, pp. 313–328.

    Article  CAS  PubMed  Google Scholar 

  39. Grinnell, A.D., A study of interaction between motoneurones in the frog spinal cord, J. Physiol., 1966, vol. 182, pp. 612–648.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Nelson, P.G., Interaction between spinal motoneurons of the cat, J. Neurophysiol., 1966, vol. 29, pp. 275–287.

    CAS  PubMed  Google Scholar 

  41. Sonnhof, U., Richter, D.W., and Taugner, R., Electrotonic coupling between frog spinal motoneurons. An electrophysiological and morphological study, Brain Res., 1977, vol. 138, pp. 197–215.

    Article  CAS  PubMed  Google Scholar 

  42. Shapovalov, A.I. and Shiryaev, B.I., A study of synaptic interaction of individual motoneurons in the frog spinal cord, Neirofiziol., 1984, vol. 16, pp. 619–630.

    CAS  Google Scholar 

  43. Karamyan, A.I. and Suderevskaya, E.I., Synaptic interactions of individual motoneurons in the carp spinal cord, Neirofiziol., 1986, vol. 18, pp. 262–266.

    Google Scholar 

  44. Auerbach, A.A. and Bennett, M.V.L., A rectifying electrotonic synapse in the central nervous system of a vertebrate, J. Gen. Physiol., 1969, vol. 53, pp. 211–237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Perrins, R. and Roberts, A., Cholinergic and electrical synapses between synergistic spinal motoneurones in the Xenopus laevis embryo, J. Physiol., 1995, vol. 485, pp. 135–144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bennett, M.V. and Zukin, R.S., Electrical coupling and neuronal synchronization in the mammalian brain, Neuron, 2004, vol. 41, pp. 495–511.

    Article  CAS  PubMed  Google Scholar 

  47. Connors, B.W. and Long, M.A., Electrical synapses in the mammalian brain, Annu Rev. Neurosci., 2004, vol. 27, pp. 393–418.

    Article  CAS  PubMed  Google Scholar 

  48. Barker, J.L. and Nicoll, R.A., The pharmacology and ionic dependency of amino acid responses in the frog spinal cord, J. Physiol. (Lond.), 1973, vol. 228, pp. 259–277.

    Article  CAS  Google Scholar 

  49. Puil, E., S-glutamate: its interactions with spinal neurons, Brain Res. Rev., 1981, vol. 3, pp. 229–322.

    Article  CAS  Google Scholar 

  50. Shefner, S.A. and Levy, R.A., The contribution of increases in extracellular potassium to primary afferent depolarization in the bullfrog spinal cord, Brain Res., 1981, vol. 205, pp. 321–335.

    Article  CAS  PubMed  Google Scholar 

  51. Curtis, D.R., Phillis, J.W., and Watkins, J.C., Actions of amino-acids on the isolated hemisected spinal cord of the toad, Br. J. Pharmacol., 1961, vol. 16, pp. 262–283.

    CAS  Google Scholar 

  52. Schmidt, R.F., Pharmacological studies on the primary afferent depolarization of the toad spinal cord, Pfl gers Arch. Ges. Physiol., 1963, vol. 277, pp. 325–346.

    Article  CAS  Google Scholar 

  53. Evans, R.H., Evidence supporting the indirect depolarization of primary afferent terminals in the frog by excitatory amino acids, J. Physiol. (Lond.), 1980, vol. 298, pp. 25–35.

    Article  CAS  Google Scholar 

  54. Shapovalov, A.I., Shiriaev, B.I., and Tamarova, Z.A., Differential sensitivity of individual primary afferents to glutamic and gamma-aminobutyric acids in the amphibian spinal cord in vitro, Exp. Brain Res., 1983, vol. 49, pp. 140–142.

    Article  CAS  PubMed  Google Scholar 

  55. Davies, J., Evans, R.H., Francis, A.A., and Watkins, J.C., Excitatory amino acid receptors and synaptic excitation in the mammalian central nervous system, J. Physiol. (Lond.), 1979, vol. 75, pp. 641–654.

    CAS  Google Scholar 

  56. Agrawal, S.G. and Evans, R.H., The primary afferent depolarizing action of kainate in the rat, Br. J. Pharmacol., 1986, vol. 87, pp. 345–355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Evans, R.H., Evans, S.J., Pook, P.C., and Sunter, D.C., A comparison of excitatory amino acid antagonists acting at primary afferent C fibres and motoneurones of the isolated spinal cord of the rat, Br. J. Pharmacol., 1987, vol. 91, pp. 531–537.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Cochilla, A.J. and Alford, S., Glutamate-receptormediated synaptic excitation in axons of the lamprey, J. Physiol. (Lond.), 1997, vol. 499, pp. 443–457.

    Article  CAS  Google Scholar 

  59. Cochilla, A.J. and Alford, S., Metabotropic glutamate receptor-mediated control of neurotransmitter release, Neuron, 1998, vol. 20, pp. 1007–1016.

    Article  CAS  PubMed  Google Scholar 

  60. Cochilla, A.J. and Alford, S., NMDA receptormediated control of presynaptic calcium and neurotransmitter release, J. Neurosci., 1999, vol. 19, pp. 193–205.

    CAS  PubMed  Google Scholar 

  61. Coggeshall, R.E. and Carlton, S.M., Receptor localization in the mammalian dorsal horn and primary afferent neurons, Brain Res. Rev., 1997, vol. 24, pp. 28–66.

    Article  CAS  PubMed  Google Scholar 

  62. Hwang, S.J., Pagliardini, S., Rustioni, A., and Valtschanoff, J.G., Presynaptic kainate receptors in primary afferents to the superficial laminae of the rat spinal cord, J. Comp. Neurol., 2001, vol. 436, pp. 275–289.

    Article  CAS  PubMed  Google Scholar 

  63. Krieger, P. and El Manira, A., Group III mGluRmediated depression of sensory synaptic transmission, Brain Res., 2002, vol. 937, pp. 41–44.

    Article  CAS  PubMed  Google Scholar 

  64. Rustioni, A., Modulation of sensory input to the spinal cord by presynaptic ionotropic glutamate receptors, Arch. Ital. Biol., 2005, vol. 143, pp. 103–112.

    CAS  PubMed  Google Scholar 

  65. Vesselkin, N.P., Adanina, V.O., Rio, J.-P., Repérant, J., Ultrastructural study of glutamate- and GABA-immunoreactive terminals contacting the primary afferent fibers in the frog spinal cord. A double postembedding immunocytochemical study, Brain Res., 2003, vol. 960, pp. 267–272.

    Article  CAS  PubMed  Google Scholar 

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  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    V. O. Adanina & N. P. Vesselkin

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  1. V. O. Adanina
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Correspondence to V. O. Adanina.

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Original Russian Text © V.O. Adanina, N.P. Vesselkin, 2016, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2016, Vol. 52, No. 5, pp. 354—361.

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Adanina, V.O., Vesselkin, N.P. Synaptic and electotonic contacts on primary afferent axons in the lamprey Lampetra fluviatilis spinal cord. J Evol Biochem Phys 52, 388–396 (2016). https://doi.org/10.1134/S0022093016050070

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