Investigation of Changes in Membrane Potential and Rhythmic Activity of the Retzius Neuron upon Stimulation of the Sensory P-Neuron

It was found that in "natural neural networks", ganglia of the nervous system of a leech, the frequency of rhythmic excitation (a series of nerve impulses, RE) of one neuron is modulated upon activation of other neurons. Changes in the electrophysiological characteristics of the leech Retzius cell in response to electrical stimulation of one of the sensory neurons (P-cells) were revealed. Registration of changes in the membrane potential of neurons, as well as electrical stimulation of the P-cell was carried out using microelectrodes introduced into the cells. It was found that during electrical stimulation, P-cells increase the frequency of spontaneous RE of Retzius cells, the membrane potential of P-cells increases, but Retzius cells do not change. With an increase in the duration of stimulation, the RE frequency increases in both the P-cell and the Retzius cell. It has been found that RE Retzius cells, upon stimulation of P-cells, arise against the background of RE of the Retzius cell. Thus, during RE of sensory neurons and synaptic transmission to the Retzius cell, RE frequency modulation occurs. According to the authors, changes in the frequency of spontaneous RE of the Retzius neuron in the "natural neural network" are associated not only with a change in the RE frequency during excitation along nerve fibers from skin receptors, but also with the transformation of RE both between cells of one ganglion and between cells in different ganglia leech nerve chain

This work was financially supported by the RSF (grant RSF no. 19-79-30062)

Литература

[1] Groome J.R., Vaughan D.K. Glutamate as a transmitter in the sensory pathway from prostomial lip to serotonergic Retzius neurons in the medicinal leech Hirudo. Invert Neurosci., 1996, vol. 2, no. 2, pp. 121--128. DOI: https://doi.org/10.1007/BF02214115

[2] Kazakova T., Erofeev A., Gorelkin P., et al. Neurotransmitter vesicles redistribution during the activation of the neuron acetylcholine receptor. FEBS Open Bio, 2019, vol. 9, iss. S1, art. P-06-018, pp. 127--128. DOI: https://doi.org/10.1002/2211-5463.12675

[3] Kazakova T.A., Yusipovich A.I., Pirutin S.K., et al. Changes in the frequency of rhythmic excitation of Retzius cells during thermal stimulation of leech skin. Bull. Exp. Biol. Med., 2020, vol. 168, pp. 378--380. DOI: https://doi.org/10.1007/s10517-020-04713-z

[4] Zhukov O.A., Kazakova T.A., Maksimov G.V., et al. Cost of auditory sharpness: model-based estimate of energy use by auditory brainstem "octopus" neurons. J. Theor. Biol., 2019, vol. 469, pp. 137--147. DOI: https://doi.org/10.1016/j.jtbi.2019.01.043

[5] Lent C.M., Zundel D., Freedman E., et al. Serotonin in the leech central nervous system: anatomical correlates and behavioral effects. J. Comp. Physiol. A, 1991, vol. 168, no. 2, pp. 191--200. DOI: https://doi.org/10.1007/BF00218411

[6] Nicholls J.G., Purves D. A comparison of chemical and electrical synaptic transmission between single sensory cells and a motoneurone in the central nervous system of the leech. J. Physiol., 1972, vol. 225, iss. 3, pp. 637--656. DOI: https://doi.org/10.1113/jphysiol.1972.sp009961

[7] Burgin A.M., Szczupak L. Network interactions among sensory neurons in the leech. J. Comp. Physiol. A, 2003, vol. 189, no. 1, pp. 59--67. DOI: https://doi.org/10.1007/s00359-002-0377-8

[8] Velazquez-Ulloa N., Blackshaw S.E., Szczupak L., et al. Convergence of mechanosensory inputs onto neuromodulatory serotonergic neurons in the leech. J. Neurobiol., 2003, vol. 54, iss. 4, pp. 604--617. DOI: https://doi.org/10.1002/neu.10184

[9] Angstadt J.D., Grassmann J.L., Theriault K.M., et al. Mechanisms of post inhibitory rebound and its modulation by serotonin in excitatory swim motor neurons of the medicinal leech. J. Comp. Physiol. A, 2005, vol. 191, no. 8, pp. 715--732. DOI: https://doi.org/10.1007/s00359-005-0628-6

[10] Angstadt J.D., Friesen W.O. Modulation of swimming behavior in the medicinal leech. I. Effects of serotonin on the electrical properties of swim-gating cell 204. J. Comp. Physiol. A, 1993, vol. 172, no. 2, pp. 223--234. DOI: https://doi.org/10.1007/BF00189398

[11] De-Miguel F.F., Nicholls J.G. Release of chemical transmitters from cell bodies and dendrites of nerve cells. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2015, vol. 370, iss. 1672, pp. 1--7. DOI: https://doi.org/10.1098/rstb.2014.0181

[12] Kerkut G.A., Walker R.J. The action of acetylcholine, dopamine and 5-hydro-xytryptamine on the spontaneous activity of the cells of Retzius of the leech, Hirudo Medicinalis. Br. J. Pharmacol. Chemother., 1967, vol. 30, iss. 3, pp. 644--654. DOI: https://dx.doi.org/10.1111%2Fj.1476-5381.1967.tb02171.x

[13] Kristan W.B., French K.A., Szczupak L. Developmental regulation of segment-specific cholinergic receptors on Retzius neurons in the medicinal leech. J. Neurosci., 1993, vol. 13, iss. 4, pp. 1577--1587. DOI: https://doi.org/10.1523/jneurosci.13-04-01577.1993

[14] Lent C.M., Dickinson M.H., Marshall C.G. Serotonin and leech feeding behavior: obligatory neuromodulation. Am. Zool., 1989, vol. 29, iss. 4, pp. 1241--1254. DOI: https://doi.org/10.1093/icb/29.4.1241

[15] Marszalec W., Yeh J.Z., Narahashi T. Desensitization of nicotine acetylcholine receptors: modulation by kinase activation and phosphatase inhibition. Eur. J. Pharmacol., 2005, vol. 514, iss. 2--3, pp. 83--90. DOI: https://doi.org/10.1016/j.ejphar.2005.03.017

[16] Mashanskii V.F., Bazanova I.S., Maiorov V.N. Protective role of serotonin against acetylcholine-induced changes in ultrastructure of the Retzius neuron. Neurosci. Behav. Physiol., 1988, vol. 18, no. 2, pp. 122--126. DOI: https://doi.org/10.1007/BF01192246

[17] Moshtagh-Khorasani M., Miller E.W., Torre V. The spontaneous electrical activity of neurons in leech ganglia. Physiol. Rep., 2013, vol. 1, iss. 5, pp. 1--16. DOI: https://doi.org/10.1002/phy2.89

[18] Nicholls D.G., Budd S.L. Mitochondria and neuronal survival. Physiol. Rev., 2000, vol. 80, no. 1, pp. 315--360. DOI: https://doi.org/10.1152/physrev.2000.80.1.315

[19] Willard A.L. Effects of serotonin on the generation of the motor program for swimming by the medicinal leech. J. Neurosci., 1981, vol. 1, no. 9, pp. 936--944. DOI: https://doi.org/10.1523/JNEUROSCI.01-09-00936.1981