Abstract
Time course of formation of the inhibitory receptor network (GABA-Aα1 and GABA-B1) in the respiratory subnuclei (ventral and lateral) of the solitary tract (NTS) during the early postnatal period was studied on laboratory Wistar rats under normal conditions and prenatal serotonin deficiency. It was found that in normal rats the maturation of the inhibitory receptor networks in both NTS subnuclei occurs within the first three postnatal weeks. Some features of their formation were noticed. The dynamics of changes in intensity of GABA-Аα1 expression in the ventral and lateral subnuclei proceeds in a similar way. During the first postnatal week, GABA-Aα1 expression is low. In the neuropil, the network of GABA-Aα1-containing presynaptic terminals and synapses is poorly developed. Within the second week, the number of GABA-Aα1-expressing neurons increases in both subnuclei with a simultaneous rise in the density of the network of terminals and synaptic structures. By the end of the third week, the number of GABA-Aα1-expressing neurons decreases, but the network density continues to increase. GABA-B1 expression in the ventral and lateral subnuclei occurs also simultaneously, although with some distinctions. During the first postnatal week, intensity of GABA-B1 expression is weak. In the neuropil, few GABA-B1-containing terminals form a loose network with sporadic synaptic structures. During the second week, expression of the receptor increases, being particularly considerable in the ventral subnuclei. Simultaneously, the density of the presynaptic terminals increases. By the end of the third week, the number of GABA-B1-expressing neurons in the ventral subnuclei decreases, while in the lateral subnuclei remains almost intact and the network density increases. The data obtained show that prenatal serotonin deficiency leads to malformation and impaired maturation of the GABAergic inhibitory neuronal network in the ventrolateral part of NTS.
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Austgen, J.R, Fong, A.Y., Foley, C.M., Mueller, P.J., Kline, D.D., Heesch, C.M., and Hasser, E.M., Expresion of group I metabotropic glutamate receptors on phenotypically different cells within the nucleus of the solitary tract in the rat, Neurosci., 2009, vol. 159, no. 2, pp. 701–716.
Bailey, T.W., Appleyard, S.M., Jin, Y.H., and Andresen, M.C., Organization and properties of GABAergic neurons in solitary tract nucleus (NTS), J. Neurophysiol., 2008, vol. 99, no. 4, pp. 1712–1722.
Chan, R.K. and Sawchenko, P.E., Organization and transmitter specificity or medullary neurons activated by sustained hypertension implications for understanding barorecepter reflex circuity, J. Neurosci., 1998, vol. 18, no. 1, pp. 371–387.
Wang, L. and Bradley, R.M., Influence of GABA on neurons of the gustatory zone of the rat nucleus of the solitary tract, Brain Res., 1993, vol. 616, pp. 144–153.
Kuwana, S., Okada, Y., Sugawara, Y., Tsunekawa, N., and Obata, K., Neurosci., 2003, vol. 120, no. 3, pp. 861–870.
McDougall, S.J., Bailey, T.W., Mendelowitz, D., and Andresen, M.C., Propofol enhances both tonic and phasic inhibitory currents in second-order neurons of the solitary tract nucleus (NTS), Neuropharmacol., 2008, vol. 54, no. 3, pp. 552–563.
Thomas, P., Mortensen, M., Hosie, A.M., and Smart, T.G., Dynamic mobility of functional GABA-A receptors at inhibitory synapses, Nat. Neurosci., 2005, vol. 8, no. 7, pp. 889–897.
Belan, P.V. and Kostyuk, P.G., Glutamate-receptor- induced modulation of GABAtrgic synaptic transmission in the hippocampus, Pflügers Arch., 2002, vol. 444, nos. 1–2, pp. 26–37.
Jones, K.A., Borowsky, B., Tamm, J.A., Craig, D.A., Durkin, M.M., Dai, M., et al., GABA (B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2, Nature, 1998, vol. 396, no. 6712, pp. 674–679.
Mohler, H. and Fritschy, J.M., GABA-B receptors make into the top-as dimmers, Trends Pharmacol. Sci., 1999, vol. 20, no. 3, pp. 87–89.
Schuler, V., Luscher, C., Blanchet, C., Kix, N., Sansing, G., and Kiebs, K., et al., Epilepsy, hyperalgesia, impaired memory and loss of pre- and postsynaptic GABA (B) responses in mice lacking GABA (B1), Neuron, 2001, vol. 31, no. 1, pp. 47–58.
Margeta-Mitrovic, M., Jan, Y.N., and Jan, L.Y., Ligand-induced signal transduction within heterodimeric GABA (B) receptor, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, no. 25, pp. 4643–4648.
Isgeld, U., Bijak, M., and Jarolimek, W., A physiological role for GABA-B receptors and the effects of baclofen in the mammalian central nervous system, Prog. Neurobiol., 1995, vol. 46, no. 4, pp. 423–462.
Liu, Q. and Wong-Riley, M.T., Postnatal changes in the expression of serotonin 2A receptors in various brain stem nuclei of the rat, J. Appl. Physiol., 2008, vol. 104, no. 6, pp. 1801–1808.
Liu, Q. and Wong-Riley, M.T., Postnatal changes in tryptophan hydroxylase and serotonin transporter immunoreactivity in multiple braiNTSem nuclei of the rat: implications for a sensitive period, J. Comp. Neurol., 2010, vol. 518, no. 7, pp. 1082–1097.
Liu, Q. and Wong-Riley, M.T., Postnatal changes in the expressions of serotonin 1A, 1B, and 2A receptors in ten brain stem nuclei of the rat: implication for a sensitive period, Neurosci., 2000, vol. 165, pp. 61–78.
Paxinos, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates, 5th ed., Academic Press, 2004.
Guthmann, A., Fritschy, J.M., Ottersen, O.P., Torp, R., and Herbert, H., GABA, GABA transporters, GABA (A) receptor subunits and GAD mRNAs in the rat parabrachial and Kölliker–Fuse nuclei, J. Comp. Neurol., 1998, vol. 400, no. 2, pp. 229–243.
Heck, W.L., Basaraba, A.M., Slusarczyk, A., and Schweitzer, L., Early GABA-A receptor clustering during the development of the rostral nucleus of the solitary tract, J. Anat., 2003, vol. 202, no. 4, pp. 387–396.
Kannenberg, K., Sieghart, W., and Reuter, H., Clusters of GABAA receptors on cultured hippocampal cells correlate only partially with functional synapses, Eur. J. Neurosci., 1999, vol. 11, pp. 1256–1264.
Grabauskas, G. and Bradley, R.M., Potentiation of GABAergic synaptic transmission in the rostral nucleus of the solitary tract, Neurosci., 1999, vol. 94, pp. 1173–1182.
Brown, M., Renehan, W.E., and Schweitzer, L., Changes in GABA-immunoreactivity during development of the rostral subdivision of the nucleus of the solitary tract (rNTS), Neurosci., 2000, vol. 100, pp. 849–859.
Nakagawa, T., Wakamori, M., Shirasaki, T., Nakaye, T., and Akaike, N., Gamma-aminobutyric acid-induced response in acutely isolated nucleus solitarii neurons of the rat, Am. J. Physiol., 1991, vol. 260, pp. 745–749.
Bradley, R.M., King, M.S., Wang, L., and Shu, X., Neurotransmitter and neuromodulator activity in the gustatory zone of the nucleus tractus solitarius, Chem. Senses, 1996, vol. 21, pp. 377–385.
Serrats, J., Mengod, G., and Cortes, R., Expression of serotonin 5-HT2C receptors in GABAergic cells of the anterior raphe nuclei, J. Chem. Neuroanat., 2005, vol. 29, pp. 83–91.
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Original Russian Text © L.I. Khozhai, 2016, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2016, Vol. 52, No. 6, pp. 444—450.
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Khozhai, L.I. Formation of GABA-Aα1 and GABA-B1 receptor-mediated inhibitory network in the ventrolateral part of the solitary tract nucleus during the early postnatal period under normal conditions and prenatal serotonin deficiency. J Evol Biochem Phys 52, 499–506 (2016). https://doi.org/10.1134/S1234567816060094
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DOI: https://doi.org/10.1134/S1234567816060094