Abstract
Functional cortical columns and nuclei of the ventral thalamus play a key role in processing of sensory information; therefore, detailed studies on formation of neuron-to-neuron gap junctions in these areas are of great theoretical and practical importance. In the present study, we applied electron-microscopy methods to examine the structure and specific distribution of interneuronal gap junctions in the cortical layer IV and thalamic nuclei, including VPM, RTN, Pom, and VPL. In the cortex, we found more interneuronal gap junctions than in thalamic nuclei. In all structures studied we revealed and described axo-dendritic, dendrodendritic, and “mixed” synapses. We report on the axo-dendritic gap junctions for the first time. It is suggested that this type of contacts plays some functional role in local synchronization of neuronal activity within one ensemble on the presynaptic level.
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Blanc, E.M., Bruce-Keller, A.J., and Mattson, M.P., Astrocytic gap junctional communication decreases neuronal vulnerability to oxidative stress-induced disruption of Ca2+ homeostasis and cell death, J. Neurochem., 1998, vol. 70, pp. 958–970.
Connors, B.W. and Long, M.A., Electrical synapses in the mammalian brain, Annu. Rev. Neurosci., 2004, vol. 27, pp. 393–418.
Deans, M., Gibson, J., Sellitto, C., Connors, B., and Paul, D., Synchronization activity of inhibitory networks in neocortex requires electrical synapses containing connexin 36, Neuron, 2001, vol. 31, pp. 477–485.
Fukuda, T. and Kosaka, T., Ultrastructural study of gap junctions between dendrites of parvalbumin-containing GABAergic neurons in various neocortical areas of the adult rat, Neuroscience, 2003, vol. 120, pp. 5–20.
Fukuda, T., Kosaka, T., Singer, W., and Galuske, R.A.W., Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network, J. Neurosci., 2006, vol. 26, pp. 3434–3443.
Galarreta, M. and Hestrin, S., Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, pp. 12438–12443.
Giaume, C., Tabernero, A., and Medina, J.M., Metabolic trafficking through astrocytic gap junctions, Glia, 1997, vol. 21, pp. 114–123.
Gibson, J.R., Beierlein, M., and Connors, B.W., Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4, J. Neurophysiol., 2005, vol. 93, pp. 467–480.
Hamzei-Sichani, F., Davidson, K.G.V., Yasumura, T., Janssen, W.G.M., Wearne, S.L., Hof, P.R., Traub, R.D., Gutiérrez, R., Ottersen, O.P., and Rash, J.E., Mixed electrical–chemical synapses in adult rat hippocampus are primarily glutamatergic and coupled by connexin-36, Front. Neuroanat., 2012, vol. 6, p. 13. doi 10.3389/fnana.2012.00013
Kirichenko, E.Y., Churyumova, G.A., and Logvinov, A.K., Ultrastructural study of glial gap junctions in the thalamic nuclei of rat, Biochemistry (Moscow) Suppl. Ser. A: Membr. Cell Biol., 2016, vol. 10, no. 3, pp. 207–217.
Kirichenko, E.Yu., Povilaitite, P.E., and Sukhov, A.G., Gap junctions role in local rhythmogenesis in cortical columns, Morfologiya, 2008, vol. 133, no. 1, pp. 31–34.
Kivrak, B. and Erzurumlu, R., Development of the principal nucleus trigeminal lemniscal projections in the mouse, J. Comp. Neurol., 2013, vol. 521, pp. 299–311.
Kosaka, T., Deans, M.R., Paul, D.L., and Kosaka, K., Neuronal gap junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice, Neuroscience, 2005, vol. 134, pp. 757–769.
Landisman, C., Long, M., Beierlein, M., Deans, M., Paul, D., and Connors, B., Electrical synapses in the thalamic reticular nucleus, J. Neurosci., 2002, vol. 22, pp. 1002–1009.
Logvinov, A.K., Kirichenko, E.Yu., and Povilaitite, P.E., Laminar distribution of gap-junctions in rat somatic cortical columns, J. Integr. Neurosci., 2009, vol. 8, pp. 425–431.
Logvinov, A.K., Kirichenko, E.Yu., Povilaitite, P.E., and Sukhov, A.G., Structural organization of rat barrel cortex (immunohistochemical study), Morfologiya, 2010, vol. 137, no. 1, pp. 10–13.
Lübke, J. and Feldmeyer, D., Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex, Brain Struct. Funct., 2007, vol. 212, pp. 3–17.
Nagy, J.I. and Rash, J.E., Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS, Brain Res. Brain Res. Rev., 2000, vol. 32, pp. 29–44.
Paxinos, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates, New York: Academic Press, 1998.
Pereda, A.E., Electrical synapses and their functional interactions with chemical synapses, Nat. Rev. Neurosci., 2014, vol. 15, no. 4, pp. 250–263.
Ransom, B.R. and Orkand, R.K., Glial–neuronal interactions in non-synaptic areas of the brain: studies in the optic nerve, Trends Neurosci., 1996, vol. 19, pp. 352–358.
Scemes, E. and Spray, D.C., Increased intercellular communication in mouse astrocytes exposed to hyposmotic shocks, Glia, 1998, vol. 24, pp. 74–84.
Serkov, F.N. and Kazakov, V.N., Neirofiziologiya talamusa (Neurophysiology of Thalamus), Kiev: Naukova dumka, 1980.
Sloper, J.J., Gap junctions between dendrites in the primate neocortex, Brain Res., 1972, vol. 44, pp. 641–646.
Sukhov, A.G., Neironnaya organizatsiya taktil’nogo analizatora krysy (Neuronal Organization of Rat Tactile Analyzer), Rostov-on-Don: Izd. RGU, 1992.
Traub, R.D., Duncan, R., Russell, A.J.C., Baldeweg, T., Tu, Y., Cunningham, M.O., and Whittington, M.A., Spatiotemporal patterns of electrocorticographic very fast oscillations (>80 Hz) consistent with a network model based on electrical coupling between principal neurons, Epilepsia, 2010, vol. 51, pp. 1587–1597.
Yamamoto, T., Ochalski, A., Hertzberg, E.L., and Nagy, J.I., On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin-43 expression, J. Comp. Neurol., 1990, vol. 302, pp. 853–883.
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Kirichenko, E.Y., Logvinov, A.K. & Filippova, S.Y. Neuronal Gap Junctions in Cortical Columns and Nuclei of the Ventral Thalamus of Rats. Cell Tiss. Biol. 12, 74–79 (2018). https://doi.org/10.1134/S1990519X18010091
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DOI: https://doi.org/10.1134/S1990519X18010091