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Possible Mechanisms of the Influence of the Supramillary Nucleus on the Functioning of the Dentate Gyrus and the CA2 Field of the Hippocamsus (Role of Disinhibition)

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Abstract—We analyzed possible mechanisms of the influence of the supramammillary nucleus of the hypothalamus (SMN) on the activity of granule cells of the dentate gyrus and pyramidal neurons of the CA2 field of the hippocampus. We used known data on the functional organization of excitatory and inhibitory interactions in the neural network, which includes the SMN, hippocampus, septum, and entorhinal cortex. We propose that the induction of long-term potentiation in the perforant path inputs to granule cells and pyramidal neurons of the CA2 field during simultaneous stimulation of the SMN and the entorhinal cortex is promoted by disinhibition, which involves interconnected inhibitory neurons located in different fields of the hippocampus, the septum, and the SMN. In the waking state, the glutamatergic input from the SMN to the CA2 field promotes the potentiation of inputs from the entorhinal cortex and from the CA3 field to the pyramidal neurons of the CA2 field, which facilitates the propagation of signals through the trisynaptic hippocampal pathway. Taking into account the known data on the increased activity of the SMN during paradoxical sleep, data on the participation of the SMN in an increase in the activity of granule cells and pyramidal neurons of the CA2 field, and data on the high efficiency of input from the CA2 field into the CA1 field, we hypothesized that during paradoxical sleep, when the transmission of information through the classical trisynaptic pathway is suppressed, it is transferred to the CA1 field through the dentate gyrus and CA2 field. Our analysis suggests that the SMN-induced facilitation of signal transmission through different hippocampal fields as well as an increase in the activity of SMN and granule cells during paradoxical sleep, which promotes neurogenesis, may underlie the participation of SMN in memory processes.

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REFERENCES

  1. Pan, W.X. and McNaughton, N., Prog. Neurobiol., 2004, vol. 74, no. 3, pp. 127–166.

    Article  PubMed  Google Scholar 

  2. Vertes, R.P. and McKenna, J.T., Synapse, 2000, vol. 38, no. 3, pp. 281–293.

    Article  CAS  PubMed  Google Scholar 

  3. Nitsch, R. and Leranth, C., J. Comp. Neurol., 1996, vol. 364, no. 3, pp. 425–438.

    Article  CAS  PubMed  Google Scholar 

  4. Leranth, C. and Hajszan T., Prog. Brain Res., 2007, vol. 163, pp. 63–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Shahidi, S., Motamedi, F., and Naghdi, N., Brain Res., 2004, vol. 1026, pp. 267–274.

    Article  CAS  PubMed  Google Scholar 

  6. Vann, S.D. and Nelson, A.J., Prog Brain Res., 2015, vol. 219, pp. 163–185.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Luppi, P.H., Billwiller, F., and Fort, P., Curr. Opin. Neurobiol., 2017, vol. 44, pp. 59–64.

    Article  CAS  PubMed  Google Scholar 

  8. Renouard, L., Billwiller, F., Ogawa, K., Clément, O., Camargo, N., Abdelkarim, M., Gay, N., Scoté-Blachon, C., Touré, R., Libourel, P.A., Ravassard, P., Salvert, D., Peyron, C., Claustrat, B., Léger, L., Salin, P., Malleret, G., Fort, P., and Luppi, P.H., Sci. Adv., 2015, vol. 1, no. 3, e1400177.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Nakanishi, K., Saito, H., and Abe, K., Eur. J. Neurosci., 2001, vol. 13, no. 4, pp. 793–800.

    Article  CAS  PubMed  Google Scholar 

  10. Hashimotodani, Y., Karube, F., Yanagawa, Y., Fujiyama, F., and Kano, M., Cell. Rep., 2018, vol. 25, no. 10, pp. 2704–2715.

    Article  CAS  PubMed  Google Scholar 

  11. Boyce, R., Williams, S., and Adamantidis, A., Curr. Opin. Neurobiol., 2017, vol. 44, pp. 167–177.

    Article  CAS  PubMed  Google Scholar 

  12. Ohara, S., Sato, S., Tsutsui, K., Witter, M.P., and Iijima, T., PLoS One, 2013, vol. 8, no. 11, e78928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Alhourani, A., Fish, K.N., Wozny, T.A, Sudhakar, V., Hamilton, R.L., and Richardson, R.M., J. Neurophysiol., 2020, vol. 123, no. 4, pp. 392–406.

    Article  CAS  PubMed  Google Scholar 

  14. Han, Z.S., Buhl, E.H., Lörinczi, Z., and Somogyi, P., Eur. J. Neurosci., 1993, vol. 5, no. 5, pp. 395–410.

    Article  CAS  PubMed  Google Scholar 

  15. Houser, C.R., Prog. Brain Res., 2007, vol. 163, pp. 217–232.

    Article  CAS  PubMed  Google Scholar 

  16. Sik, A., Penttonen, M., and Buzsáki, G., Eur. J. Neurosci., 1997, vol. 9, no. 3, pp. 573–588.

    Article  CAS  PubMed  Google Scholar 

  17. Halasy, K. and Somogyi, P., Eur. J. Neurosci., 1993, vol. 5, no. 5, pp. 411–429.

    Article  CAS  PubMed  Google Scholar 

  18. Tóth, K. and Maglóczky, Z., Front. Neuroanat., 2014, vol. 8, Article 100.

    PubMed  PubMed Central  Google Scholar 

  19. Blasco-Ibáñez, J.M., Martínez-Guijarro, F.J., and Freund, T.F., Neuroreport, 2000, vol. 11, no. 14, pp. 3219–3225.

    Article  PubMed  Google Scholar 

  20. Ribak, C.E., Seress, L., and Leranth, C., J. Comp. Neurol., 1993, vol. 327, no. 2, pp. 298–321.

    Article  CAS  PubMed  Google Scholar 

  21. Han, Z.S., Neurosci. Res., 1994, vol. 19, no. 1, pp. 101–110.

    Article  CAS  PubMed  Google Scholar 

  22. Elgueta, C. and Bartos M., Nat. Commun., 2019, vol. 10, no. 1, pp. 5561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Scharfman, H.E., Prog. Brain Res., 2007, vol. 163, pp. 627–637.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Scharfman, H.E., Neuroscience, 1996, vol. 72, no. 3, pp. 655–668.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Frotscher, M., Soriano, E., and Leranth, C., Epilepsy Res. Suppl., 1992, vol. 7, pp. 65–78.

    CAS  PubMed  Google Scholar 

  26. Ruan, M., Young, C.K., and McNaughton, N., Front. Neural Circuits, 2017, vol. 11, Article 62.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Soussi, R., Zhang, N., Tahtakran, S., Houser, C.R., and Esclapez, M., Eur. J. Neurosci., 2010, vol. 32, no. 5, pp. 771–785.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Root, D.H., Zhang, S., Barker, D.J., Miranda-Barrientos, J., Liu, B., Wang, H.L., and Morales, M., Cell Rep., 2018, vol. 23, no. 12, pp. 3465–3479.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Pedersen, N.P., Ferrari, L., Venner, A., Wang, J.L., Abbott, S.B.G., Vujovic, N., Arrigoni, E., Saper, C.B., and Fuller, P.M., Nat. Commun., 2017, vol. 8, no. 1, pp. 1405.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Hansen M.G., Ledri L.N., Kirik D., Kokaia M., Ledri M., Front. Cell Neurosci., 2018, vol. 11, Article 433.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Patton, P.E. and McNaughton, B., Hippocampus, 1995. 5, no. 4, pp. 245–286.

    Article  CAS  PubMed  Google Scholar 

  32. Frotscher, M., Jonas, P., and Sloviter, R.S., Cell Tissue Res., 2006, vol. 326, no. 2, pp. 361–367.

    Article  PubMed  Google Scholar 

  33. Botterill, J.J., Lu Y.L., LaFrancois, J.J., Bernstein, H.L., Alcantara-Gonzalez, D., Jain, S., Leary, P., and Scharfman, H.E., Cell Rep., 2019, vol. 29, no. 9, pp. 2875–2889.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Benoy, A., Dasgupta, A., and Sajikumar, S., Exp. Brain Res., 2018, vol. 236, no. 4, pp. 919–931.

    Article  CAS  PubMed  Google Scholar 

  35. Cui, Z., Gerfen, C.R., and Young, W.S. 3rd., J. Comp. Neurol., 2013, vol. 521, no. 8, pp. 1844–1866.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kohara K., Pignatelli M., Rivest A.J., Jung H.Y., Kitamura T., Suh J., Frank D., Kajikawa K., Mise N., Obata Y., Wickersham I.R., and Tonegawa S., Nat. Neurosci., 2014, vol. 17, no. 2, pp. 269–79.

    Article  CAS  PubMed  Google Scholar 

  37. Llorens-Martín, M., Jurado-Arjona, J., Avila, J., and Hernández, F., Exp. Neurol., 2015, vol. 263, pp. 285–292.

    Article  PubMed  Google Scholar 

  38. Chevaleyre, V. and Siegelbaum, S.A., Neuron, 2010, vol. 66, no. 4, pp. 560–572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Nasrallah, K., Piskorowski, R.A., and Chevaleyre, V., Neurobiol. Learn. Mem., 2017, vol. 138, pp. 173–181.

    Article  PubMed  Google Scholar 

  40. Mercer, A., Trigg, H.L, and Thomson, A.M., J. Neurosci., 2007, vol. 27, no. 27, pp. 7329–7338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hayani, H., Song, I., and Dityatev, A., Front. Cell Neurosci., 2018, vol. 12. Article 149.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Mercer, A., Eastlake, K., Trigg, H.L., and Thomson, A.M., Hippocampus, 2012, vol. 22, no. 1, pp. 43–56.

    Article  PubMed  Google Scholar 

  43. Caruana, D.A., Alexander, G.M., and Dudek, S.M., Learn. Mem., 2012, vol. 19, no. 9, pp. 391–400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Nasrallah, K., Piskorowski, R.A., and Chevaleyre, V., eNeuro, 2015, vol. 2, no. 4, pii: ENEURO.0049-15.

  45. Leroy, F., Brann, D.H., Meira, T., and Siegelbaum, S.A., Neuron, 2017, vol. 95, no. 5, pp. 1089–1102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Berger, B., Esclapez, M., Alvarez, C., Meyer, G., and Catala, M., J. Comp. Neurol., 2001, vol. 429, no. 4, pp. 515–529.

    Article  CAS  PubMed  Google Scholar 

  47. Dasgupta, A., Baby, N., Krishna, K., Hakim, M., Wong, Y.P., Behnisch, T., Soong, T.W., and Sajikumar, S., Proc. Natl. Acad. Sci. USA, 2017, vol. 114, no. 41, pp. E8741–E8749.

    Article  CAS  PubMed  Google Scholar 

  48. Bartesaghi, R., Migliore, M., and Gessi, T., Neuroscience, 2006, vol. 142, no. 1, pp. 247–265.

    Article  CAS  PubMed  Google Scholar 

  49. Leranth, C., Carpi, D., Buzsaki, G., and Kiss, J., Neuroscience, 1999, vol. 88, no. 3, pp. 701–718.

    Article  CAS  PubMed  Google Scholar 

  50. Borhegyi, Z. and Freund, T.F., Brain Res. Bull., 1998, vol. 46, no. 5, pp. 453–459.

    Article  CAS  PubMed  Google Scholar 

  51. Christiansen, K., Dillingham, C.M., Wright, N.F., Saunders, R.C., Vann, S.D., and Aggleton, J.P., Eur. J. Neurosci., 2016, vol. 43, no. 8, pp. 1044–1061.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Risold, P.Y. and Swanson, L.W., Science, 1996, vol. 272, pp. 1484–1486.

    Article  CAS  PubMed  Google Scholar 

  53. Austin, K.B., Bronzino, J.D., and Morgane, P.J., Exp. Brain Res., 1989, vol. 77, no. 3, pp. 594–604.

    Article  CAS  PubMed  Google Scholar 

  54. Van Dort, C.J., Zachs, D.P, Kenny, J.D., Zheng, S., Goldblum, R.R., Gelwan, N.A., Ramos, D.M., Nolan, M.A., Wang, K., Weng, F-Ju., Lin, Y., Wilson, M.A., and Brown, E.N., Proc. Natl. Acad. Sci. USA, 2015, vol. 112, no. 2, pp. 584–589.

    Article  CAS  PubMed  Google Scholar 

  55. Kroeger, D., Ferrari, L.L., Petit, G., Mahoney, C.E., Fuller, P.M., Arrigoni, E., and Scammell, T.E., J. Neurosci., 2017, vol. 37, no. 5, pp. 1352–1366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hallanger, A.E. and Wainer, B.H., J. Comp. Neurol., 1988, vol. 274, no. 4, pp. 483–515.

    Article  CAS  PubMed  Google Scholar 

  57. Satoh, K. and Fibiger, H.C., J. Comp. Neurol., 1986, vol. 253, no. 3, pp. 277–302.

    Article  CAS  PubMed  Google Scholar 

  58. Ariffin, M.Z., Jiang, F., Low, C-M., and Khanna, S., Hippocampus, 2010, vol. 20, no. 7, pp. 852–865.

    CAS  PubMed  Google Scholar 

  59. Ariffin, M.Z., Low, C-M., and Khanna, S., Front. Neuroanat., 2017, vol. 11, Article 79.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Bramham, C.R. and Srebro, B., Brain Res., 1989, vol. 493, no. 1, pp. 74–86.

    Article  CAS  PubMed  Google Scholar 

  61. Luo, J., Phan, T.X., Yang, Y., Garelick, M.G., and Storm, D.R., J. Neurosci., 2013, vol. 33, pp. 6460–6468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Billwiller, F., Renouard, L., Clement, O., Fort, P., and Luppi, P.H., Brain Struct. Funct., 2017, vol. 222, no. 3, pp. 1495–1507.

    Article  PubMed  Google Scholar 

  63. Nasrallah, K., Therreau, L., Robert, V., Huang, A.J.Y., McHugh, T.J., Piskorowski, R.A., and Chevaleyre, V., Cell Rep., 2019, vol. 27, no. 1, pp. 86–98.

    Article  CAS  PubMed  Google Scholar 

  64. Sil’kis, I.G., Zhurn. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2008, vol. 58, no. 3, pp. 261–275.

    Google Scholar 

  65. Sil’kis, I.G., Zhurn. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2010, vol. 60, no. 6, pp. 645–663.

    Google Scholar 

  66. Guzman-Marin, R., Suntsova, N., Bashir, T., Nienhuis, R., Szymusiak, R., and McGinty, D., Sleep, 2008, vol. 31, no. 2, pp. 167–175.

    Article  PubMed  PubMed Central  Google Scholar 

  67. López-Virgen, V., Zárate-López, D., Adirsch, F.L., Collas-Aguilar, J., and González-Pérez, Ó., Gac. Med. Mex., 2015, vol. 151, no. 1, pp. 99–104.

    PubMed  Google Scholar 

  68. Mueller, A.D., Meerlo, P., McGinty, D., and Mistlberger, R.E., Curr. Top Behav. Neurosci., 2015, vol. 25, pp. 151–181.

    Article  PubMed  Google Scholar 

  69. Parent, J.M., Yu, T.W., Leibowitz, R.T., Geschwind, D.H., Sloviter, R.S., and Lowenstein, D.H., J. Neurosci., 1997, vol. 17, no. 10, pp. 3727–3738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kempermann, G., Song, H., and Gage, F.H., Cold Spring Harb. Perspect. Biol., 2015, vol. 7, no. 9, p. a018812.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Aranda, L., Santín, L.J., Begega, A., Aguirre, J.A., and Arias, J.L., Behav. Brain Res., 2006, vol. 167, no. 1, pp. 156–164.

    Article  PubMed  Google Scholar 

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This work was supported by the Russian Foundation for Basic Research, project no. 19-515-52001/MNT p.

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Correspondence to I. G. Silkis.

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Abbreviations: GC, granule cell of the dentate gyrus; LTP, long-term potentiation of the excitatory synaptic input; DG, dentate gyrus; MC, hilus mossy cell; BC, GABAergic basket cell; CC, GABAergic chandelier cell; MS, medial septum; PV, parvalbumin; PS, paradoxical sleep; PP, perforant path; SMN, supramamillary nucleus of the hypothalamus; EC, entorhinal cortex

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Silkis, I.G., Markevich, V.A. Possible Mechanisms of the Influence of the Supramillary Nucleus on the Functioning of the Dentate Gyrus and the CA2 Field of the Hippocamsus (Role of Disinhibition). Neurochem. J. 14, 375–383 (2020). https://doi.org/10.1134/S181971242004011X

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