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Presynaptic serotonergic modulation of spontaneous and miniature synaptic activity in frog lumbar motoneurons

  • Comparative and Ontogenic Physiology
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Abstract

The effects of serotonin (5-HT, 30 μM) on spontaneous and miniature synaptic activity in lumbar motoneurons from the isolated Rana ridibunda spinal cord were investigated using intracellular recording. 5-HT increased the frequency of spontaneous (sPSPs) and miniature postsynaptic potentials (mPSPs). The effect of 5-HT on different subpopulations of mPSPs was multidirectional: it increased the frequency of glutamatergic excitatory mPSPs by 18% and decreased the frequency of glycinergic inhibitory mPSPs by 28%, but had no effect on the frequency of GABAergic inhibitory mPSPs. The amplitude and kinetic parameters of any subpopulation of mPSPs did not change. The data obtained show that 5-HT regulates the probability of glutamate and glycine release from the presynaptic terminals ending at frog spinal motoneurons. 5-HT shifts the balance between synaptic excitation and inhibition in the spinal neural network toward excitation. Thus, 5-HT participates in control of motor output and provides its facilitation.

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Abbreviations

AMPA:

α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid

D-AP5:

D-2-amino-pentanoic acid

EPSP:

excitatory postsynaptic potential

IPSP:

inhibitory postsynaptic potential

sPSP:

spontaneous postsynaptic potential

mPSP:

miniature postsynaptic potential

GABA:

γ-aminobutyric acid

KA:

kainic acid

MP:

membrane potential

NMDA:

N-methyl-D-aspartate

AP:

action potential

TTX:

tetrodotoxin

5-HT:

5-hydroxytryptamine (serotonin)

References

  1. Jacobs, B.L. and Azmitia, E.C., Structure and function of the brain serotonin system, Physiol. Rev., 1992, vol. 72, pp. 165–229.

    CAS  PubMed  Google Scholar 

  2. Ciranna, L., Serotonin as a modulator of glutamate- and GABA-mediated neurotransmission: implications in physiological functions and in pathology, Current Neuropharmacol., 2006, vol. 4, pp. 101–114.

    Article  CAS  Google Scholar 

  3. Schmidt, B.J. and Jordan, L.M., The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord, Brain Res. Bull., 2000, vol. 53, pp. 689–710.

    Article  CAS  PubMed  Google Scholar 

  4. Törk, I., Anatomy of the serotonergic system, Ann. N. Y. Acad. Sci., 1990, vol. 600, pp. 9–34, Discussion, pp. 34–35.

    Article  PubMed  Google Scholar 

  5. Baumgarten, H.G. and Gothert, M., Serotoninergic neurons and 5-HT receptors in the CNS, Handbook of Experimental Pharmacology, Berlin, 1997, vol. 129.

  6. Soller, R.W., Monoaminergic inputs to frog motoneurons: an anatomical study using fluorescence histochemical and silver degeneration techniques, Brain Res., 1977, vol. 122, pp. 445–458.

    Article  CAS  PubMed  Google Scholar 

  7. Soller, R.W. and Erulkar, S.D., The bulbo-spinal indoleaminergic pathway in the frog, Brain Res., 1979, vol. 172, pp. 277–293.

    Article  CAS  PubMed  Google Scholar 

  8. Alvarez, F.J., Pearson, J.C., Harrington, D., Dewey, D., Torbeck, L., and Fyffe, R.E.W., Distribution of 5-hydroxytryptamine-immunoreactive boutons on a-motoneurons in the lumbar spinal cord of adult cats, J. Comp. Neurol., 1998, vol. 393, pp. 69–83.

    Article  CAS  PubMed  Google Scholar 

  9. Rekling, J.C., Funk, G.D., Bayliss, D.A., Dong, X.-W., and Feldman, J.L., Synaptic control of motoneuronal excitability, Physiol. Rev., 2000, vol. 80 (2), pp. 767–852.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Basbaum, A.I. and Fields, H.L., Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry, Annu. Rev. Neurosci., 1984, vol. 7, pp. 309–338.

    Article  CAS  PubMed  Google Scholar 

  11. Bell, J.A. and Matsumiya, T., Inhibitory effects of dorsal horn and excitant effects of ventral horn intraspinal microinjections of norepinephrine and serotonin in the cat, Life Sci., 1981, vol. 29, pp. 1507–1514.

    Article  CAS  PubMed  Google Scholar 

  12. Jacobs, B.L. and Fornal, C.A. 5- and motor control: a hypothesis, Trends Neurosci., 1993, vol. 16, pp. 346–352.

    Article  CAS  PubMed  Google Scholar 

  13. Wallis, D.I., 5-HT receptors involved in initiation or modulation of motor patterns: opportunities for drug development, Trends Pharmacol. Sci., 1994, vol. 15, pp. 288–292.

    Article  CAS  PubMed  Google Scholar 

  14. Wallis, D.I., Connell, L.A., and Kvaltinova, Z., Further studies on the action of 5-hydroxytryptamine on lumbar motoneurones in the rat isolated spinal cord, Naunyn Schmiedeberg’s Arch. Pharmacol., 1991, vol. 343, pp. 344–352.

    Article  CAS  Google Scholar 

  15. Fink, K.B. and Gothert, M., 5-HT receptor regulation of neurotransmitter release, Pharmacol. Rev., 2007, vol. 59, pp. 360–417.

    Article  CAS  PubMed  Google Scholar 

  16. Hannon, J. and Hoyer, D., Molecular biology of 5-HT receptors, Behav. Brain Res., 2008, vol. 195, pp. 198–213.

    Article  CAS  PubMed  Google Scholar 

  17. Perrier, J.-F. and Cotel, F., Serotonergic modulation of spinal motor control, Curr. Opin. Neurobiol., 2015, vol. 33, pp. 1–7.

    Article  CAS  PubMed  Google Scholar 

  18. El Manira, A., Zhang, W., Svensson, E., and Bussieres, N.K., 5-HT inhibits calcium current and synaptic transmission from sensory neurons in lamprey, J. Neurosci., 1997, vol. 17, pp. 1786–1794.

    CAS  PubMed  Google Scholar 

  19. Sillar, K.T. and Simmers, A.J., Presynaptic inhibition of primary afferent transmitter release by 5-hydroxytryptamine at a mechanosensory synapse in the vertebrate spinal cord, J. Neurosci., 1994, vol. 74, pp. 2636–2647.

    Google Scholar 

  20. Perrier, J.-F. and Cotel, F., Serotonin differentially modulates the intrinsic properties of spinal motoneurons from the adult turtle, J. Physiol., 2008, vol. 586, pp. 1233–1238.

    Article  CAS  PubMed  Google Scholar 

  21. Xie, D.-J., Uta, D., Feng, P.-Y., Wakita, M., Shin, M.-C., Furue, H., and Yoshimura, M., Identification of 5-HT receptor subtypes enhancing inhibitory transmission in the rat spinal dorsal horn in vitro, Mol. Pain., 2012, vol. 8, p. 58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kurchavyi, G.G., Kalinina, N.I., and Veselkin, N.P., The influence of GABA and glycine on postsynaptic potentials in frog motoneurons, Zh. Evol. Biokh. Fiziol., 2005, vol. 41, pp. 522–531.

    Google Scholar 

  23. Kalinina, N.I., Kurchavyi, G.G., and Veselkin, N.P., Inhibitory regulation of responses of glutamate receptors in frog motoneurons, Sechenov Ross. Fiziol. Zh., 2012, vol. 98, pp. 575–587.

    CAS  Google Scholar 

  24. Polina, Yu.A., Amakhin, D.V., Kozhanov, V.M., Kurchavyi, G.G., and Veselkin, N.P., Three types of inhibitory miniature potentials in frog spinal cord motoneurons: possible GABA and glycine cotransmission, Sechenov Ross. Fiziol. Zh., 2006, vol. 92, pp. 18–26.

    CAS  Google Scholar 

  25. Jonas, P., Bischofberger, J., and Sandkühler, J., Corelease of two fast neurotransmitters at a central synapse, Science, 1998, vol. 281, pp. 419–424.

    Article  CAS  PubMed  Google Scholar 

  26. Hori, Y., Endo, K., and Takahashi, T., Long-lasting synaptic facilitation induced by serotonin in superficial dorsal horn neurones of the rat spinal cord, J. Physiol., 1996, vol. 492, pp. 867–876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Jacobs, B.L. and Fornal, C.A., Serotonin and motor activity, Curr. Opin. Neurobiol., 1997, vol. 7, pp. 820–825.

    Article  CAS  PubMed  Google Scholar 

  28. Berger, A.J. and Huynh, P., Activation of 5HT1B receptors inhibits glycinergic synaptic inputs to mammalian motoneurons during postnatal development, Brain Res., 2002, vol. 956, pp. 380–384.

    Article  CAS  PubMed  Google Scholar 

  29. Mizutani, H., Hori, T., and Takahashi, T., 5-HT1B receptor-mediated presynaptic inhibition at the calyx of Held of immature rats, Eur. J. Neurosci., 2006, vol. 24, pp. 1946–1954.

    Article  PubMed  Google Scholar 

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Correspondence to N. I. Kalinina.

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Original Russian Text © N.I. Kalinina, G.G. Kurchavyi, A.V. Zaitsev, N.P. Veselkin, 2016, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2016, Vol. 52, No. 5, pp. 328—336.

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Kalinina, N.I., Kurchavyi, G.G., Zaitsev, A.V. et al. Presynaptic serotonergic modulation of spontaneous and miniature synaptic activity in frog lumbar motoneurons. J Evol Biochem Phys 52, 359–368 (2016). https://doi.org/10.1134/S0022093016050045

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  • DOI: https://doi.org/10.1134/S0022093016050045

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