Skip to main content
SpringerLink
Log in

The Role of Hypothalamus in the Formation of Neural Representations of Object–Place Associations in the Hippocampus during Wakefulness and Paradoxical Sleep

  • THEORETICAL ARTICLES
  • Published:
Neurochemical Journal Aims and scope Submit manuscript

Abstract—We compared the formation of neural representations of object–place associations between the waking state and paradoxical sleep in the hippocampus. The activity of hippocampal neurons is affected by the supramammillary, paraventricular, and supraoptic nuclei of the hypothalamus. Sequentially complexifying representations of object–place associations are formed during signal transduction from the dentate gyrus through the CA3 to CA1 fields on the neurons of these areas in the waking state. Inputs from the supramammillary nucleus to the dentate gyrus and CA2 field, as well as inputs to the CA2 field from the paraventricular and supraoptic hypothalamic nuclei, containing vasopressin and oxytocin-secreting neurons, facilitate signal transmission into the CA1 field by promoting long-term potentiation (LTP) of the efficacy of CA3–CA2 and CA2–CA1 connections and the summation of excitation from the CA3 and CA2 fields to the neurons of CA1 field connected with the prefrontal cortex. Information about odors from the olfactory bulb entering the CA2 field through the paraventricular and supraoptic nuclei is incorporated into the representations of object–place associations. In paradoxical sleep, when the transmission of signals along the dentate gyrus–CA3–CA1 pathway is limited, the inputs from the hypothalamic nuclei facilitate LTP at each step of the dentate gyrus-CA2–CA1 pathway. As a result, during paradoxical sleep the conditions are improved in order to form new representations of object–place associations on CA2 pyramidal neurons and their target cells in the CA1 field connected with the amygdala. It follows from the analysis performed that neural representations of object–place associations formed on the hippocampal neurons during paradoxical sleep are different from those formed in the waking state.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Karabulut, S., Korkmaz Bayramov, K., Bayramov, R., Ozdemir, F., Topaloglu, T., Ergen, E., Vazgan, K., Taskiran, A.S., and Golgeli, A., Behav. Brain Res., 2019, vol. 361, pp. 7–13.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Ruskin, D.N., Liu, C., Dunn, K.E., Bazan, N.G., and LaHoste, G.J., Eur. J. Neurosci., 2004, vol. 19, no. 11, pp. 3121–3124.

    Article  PubMed  Google Scholar 

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

  5. Sil’kis, I.G., Zhurn. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2008b, vol. 58, no. 5, pp. 521–539.

    Google Scholar 

  6. Gottesmann, C., Psychiatry. Clin. Neurosci., 2002, vol. 56, no. 4, pp. 345–354.

    Article  CAS  PubMed  Google Scholar 

  7. Hobson, J.A., Stickgold, R., and Pace-Schott, E.F., Neuroreport, 1998, vol. 9, no. 3.

  8. Sil’kis, I.G., Usp. Fiziol. Nauk, 2002, vol. 33, no. 1, pp. 40–56.

    PubMed  Google Scholar 

  9. Sil’kis, I.G., Zhurn. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2009, vol. 59, no. 6, pp. 645–661.

    Google Scholar 

  10. Sil’kis, I.G., Zhurn. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2011, vol. 61, no. 1, pp. 645–663.

    Google Scholar 

  11. Raam, T., McAvoy, K.M., Besnard, A., Veenema, A.H., and Sahay, A., Nat. Commun., 2017, vol. 8, no. 1, p. 2001.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Masurkar, A.V., Tian, C., Warren, R., Reyes, I., Lowes, D.C., Brann, D.H., and Siegelbaum, S.A., J. Neurophysiol., 2020, vol. 123, no. 3, pp. 980–992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Pang, C.C., Kiecker, C., O’Brien, J.T., Noble, W., and Chang, R.C., Neuroscientist, 2019, vol. 25, no. 2, pp. 167–180.

    Article  CAS  PubMed  Google Scholar 

  14. Young, W.S., Li, J., Wersinger, S.R., and Palkovits, M., Neuroscience, 2006, vol. 143, no. 4, pp. 1031–1039.

    Article  CAS  PubMed  Google Scholar 

  15. Sil’kis, I.G., Zhurn. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2021, vol. 71, no. 2, pp. 147–163.

  16. Maejima, Y., Takahashi, S., Takasu, K., Takenoshita, S., Ueta, Y., and Shimomura, K., Neuroreport, 2017, vol. 28, no. 6, pp. 360–366.

    Article  CAS  PubMed  Google Scholar 

  17. Piepenbrock, N., Valatx, J.L., Malquarti, V., and Jouvet, M., Neurosci. Lett., 1985, vol. 62, no. 2, pp. 151–156.

    Article  CAS  PubMed  Google Scholar 

  18. Coculescu, M., Serbanescu, A., and Temeli, E., Waking Sleeping, 1979, vol. 3, no. 3, pp. 273–277.

    CAS  PubMed  Google Scholar 

  19. 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 

  20. 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, p. 1405.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. 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 

  22. Hoover, W.B. and Vertes, R.P., Brain Struct. Funct., 2012, vol. 217, no. 2, pp. 191–209.

    Article  PubMed  Google Scholar 

  23. Laroche, S., Davis, S., and Jay, T.M., Hippocampus, 2000, vol. 10, no. 4, pp. 438–446.

    Article  CAS  PubMed  Google Scholar 

  24. Dolleman-van der Weel, M.J., Griffin, A.L., Ito, H.T., Shapiro, M.L., Witter, M.P., Vertes, R.P., and Allen, T.A., Learn. Mem., 2019, vol. 26, no. 7, pp. 191–205.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Cassel, J.-C., Pereira de Vasconcelos, A., Neurosci. Biobehav. Rev., 2015, vol. 54, pp. 175–196.

    Article  PubMed  Google Scholar 

  26. Aranda, L., Santin, 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 

  27. Cilz, N.I., Cymerblit-Sabba, A., and Young, W.S., Genes Brain Behav., 2019, vol. 18, no. 1, e12535.

  28. Piskorowski, R.A. and Chevaleyre, V., Curr. Opin. Neurobiol., 2018, vol. 52, pp. 54–59.

    Article  CAS  PubMed  Google Scholar 

  29. Lin, Y.T., Hsieh, T.Y., Tsai, T.C., Chen, C.C., Huang, C.C., and Hsu, K.S., J. Neurosci., 2018, vol. 38, no. 5, pp. 1218–1231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Pagani, J.H., Zhao, M., Cui, Z., Avram, S.K., Caruana, D.A., Dudek, S.M., and Young, W.S., Mol. Psychiatry, 2015, vol. 20, no. 4, pp. 490–499.

    Article  CAS  PubMed  Google Scholar 

  31. Stevenson, E.L. and Caldwell, H.K., Horm. Behav., 2012, vol. 61, no. 3, pp. 277–282.

    Article  CAS  PubMed  Google Scholar 

  32. 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 

  33. Dudek, S.M., Alexander, G.M., and Farris, S., Nat. Rev. Neurosci., 2016, vol. 17, no. 2, pp. 89–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 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. 269–279.

    Article  CAS  PubMed  Google Scholar 

  35. Shinohara, Y., Hosoya, A., Yahagi, K., Ferecsko, A.S., Yaguchi, K., Sik, A., Itakura, M., Takahashi, M., and Hirase, H., Eur. J. Neurosci., 2012, vol. 35, pp. 702–710.

    Article  PubMed  Google Scholar 

  36. Lee, S.H., Marchionni, I., Bezaire, M., Varga, C., Danielson, N., Lovett-Barron, M., Losonczy, A., and Soltesz, I., Neuron, 2014, vol. 82, no. 5, pp. 1129–1144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Okuyama, T., Kitamura, T., Roy, D.S., Itohara, S., and Tonegawa, S., Science, 2016, vol. 353, no. 6307, pp. 1536–1541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Alexander, G.M., Farris, S., Pirone, J.R., Zheng, C., Colgin, L.L., and Dudek, S.M., Nat. Commun., 2016, vol. 7, p. 10300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Berretta, S. and Benes, F.M., Nat. Protoc., 2006, vol. 1, no. 2, pp. 833–839.

    Article  CAS  PubMed  Google Scholar 

  40. Smith, D.A. and Flynn, J.P., Brain Res., 1980, vol. 194, no. 1, pp. 41–51.

    Article  CAS  PubMed  Google Scholar 

  41. Kafetzopoulos, V., Kokras, N., Sotiropoulos, I., Oliveira, J.F., Leite-Almeida, H., Vasalou, A., Sardinha, V.M., Papadopoulou-Daifoti, Z., Almeida, O.F.X., Antoniou, K., Sousa, N., and Dalla, C., Mol. Psychiatry, 2018, vol. 23, no. 3, pp. 579–586.

    Article  CAS  PubMed  Google Scholar 

  42. Hallock, H.L., Wang, A., and Griffin, A.L., J. Neurosci., 2016, vol. 36, no. 32, pp. 8372–8389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Vu, T., Gugustea, R., and Leung, L.S., Brain Struct. Funct, 2020, vol. 225, no. 6, pp. 1817–1838.

    Article  CAS  PubMed  Google Scholar 

  44. Klein, M.M., Cholvin, T., Cosquer, B., Salvadori, A., Le Mero, J., Kourouma, L., Boutillier, A.L., Pereira de Vasconcelos, A., and Cassel, J.C., Brain Struct. Funct., 2019, vol. 224, no. 4, pp. 1659–1676.

    Article  PubMed  Google Scholar 

  45. Barker, G.R. and Warburton, E.C., J. Neurosci., 2018, vol. 38, no. 13, pp. 3208–3217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Barker, G.R. and Warburton, E.C., Cereb. Cortex, 2015, vol. 25, no. 2, pp. 472–481.

    Article  PubMed  Google Scholar 

  47. Cholvin, T., Hok, V., Giorgi, L., Chaillan, F.A., and Poucet, B., J. Neurosci., 2018, vol. 38, no. 1, pp. 158–172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ito, H.T., Moser, E.I., and Moser, M.B., Neuron, 2018, vol. 99, no. 3, pp. 576–587.

    Article  CAS  PubMed  Google Scholar 

  49. Luppi, P.H. and Fort, P., Handb. Clin. Neurol., 2019, vol. 160, pp. 359–370.

    Article  PubMed  Google Scholar 

  50. Steininger, T.L., Alam, M.N., Gong, H., Szymusiak, R., and McGinty, D., Brain Res., 1999, vol. 840, nos. 1–2, pp. 138–147.

    Article  CAS  PubMed  Google Scholar 

  51. Vertes, R.P., Crane, A.M., Colom, L.V., and Bland, B.H., J. Comp. Neurol., 1995, vol. 359, no. 1, pp. 90–116.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  53. Ravassard, P., Hamieh, A.M., Malleret, G., and Salin, P.A., Neurobiol. Learn. Mem., 2015, vol. 122, pp. 4–10.

    Article  PubMed  Google Scholar 

  54. Born, J. and Fehm, H.L., Exp. Clin. Endocrinol. Diabetes, 1998, vol. 106, no. 3, pp. 153–163.

    Article  CAS  PubMed  Google Scholar 

  55. 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 

  56. 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, p. 1405.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Renouard, L., Billwiller, F., Ogawa, K., Clement, 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.

  58. 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 

  59. Silkis, I.G. and Markevich, V.A., Neurochem. J., 2020, vol. 14, pp. 375–383.

    Article  CAS  Google Scholar 

  60. Born, J., Kellner, C., Uthgenannt, D., Kern, W., and Fehm, H.L., Am. J. Physiol., 1992, vol. 262, no. 3, Pt. 1, pp. E295–Е300.

  61. Perras, B., Pannenborg, H., Marshall, L., Pietrowsky, R., Born, J., and Lorenz Fehm, H., J. Clin. Psychopharmacol., 1999, vol. 19, no. 1, pp. 28–36.

    Article  CAS  PubMed  Google Scholar 

  62. Brown, M.H. and Nunez, A.A., Physiol. Behav., 1989, vol. 46, no. 4, pp. 759–762.

    Article  CAS  PubMed  Google Scholar 

  63. Schwartz, M.D. and Kilduff, T.S., Psychiatr. Clin. North Am., 2015, vol. 38, no. 4, pp. 615–644.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Bertrand, E., Lechowicz, W., Lewandowska, E., Szpak, G.M., Dymecki, J., Kosno-Kruszewska, E., and Wierzba-Bobrowicz, T., Folia Neuropathol., 2003, vol. 41, no. 4, pp. 197–207.

    PubMed  Google Scholar 

  65. Sopp, M.R. Michael, T., Weeβ, H.G., and Mecklinger, A., Cogn. Affect. Behav. Neurosci., 2017, vol. 17, no. 6, pp. 1186–1209.

    Article  PubMed  Google Scholar 

  66. Wiesner, C.D., Pulst, J., Krause, F., Elsner, M., Baving, L., Pedersen, A., Prehn-Kristensen, A., and Goder, R., Neurobiol. Learn. Mem., 2015, vol. 122, pp. 131–141.

    Article  PubMed  Google Scholar 

  67. Nishida, M., Pearsall, J., Buckner, R.L., and Walker, M.P., Cereb. Cortex, 2009, vol. 19, no. 5, pp. 1158–1166.

    Article  PubMed  Google Scholar 

  68. Cantero, J.L., Atienza, M., Stickgold, R., Kahana, M.J., Madsen, J.R., and Kocsis, B., J. Neurosci., 2003, vol. 23, no. 34, pp. 10897–10903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Boyce, R., Glasgow, S.D., Williams, S., and Adamantidis, A., Science, 2016, vol. 352, no. 6287, pp. 812–816.

    Article  CAS  PubMed  Google Scholar 

  70. Guise, K.G. and Shapiro, M.L., Neuron, 2017, vol. 94, no. 1, pp. 183–192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Kim, S.Y., Kark, S.M., Daley, R.T., Alger, S.E., Reboucas, D., Kensinger, E.A., and Payne, J.D., Hippocampus, 2020, vol. 30, no. 8, pp. 829–841.

    Article  CAS  PubMed  Google Scholar 

  72. Mizuseki, K., Diba, K., Pastalkova, E., and Buzsaki, G., Nat. Neurosci., 2011, vol. 14, no. 9, pp. 1174–1181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Valero, M., Cid, E., Averkin, R.G., Aguilar, J., Sanchez-Aguilera, A., Viney, T.J., Gomez-Dominguez, D., Bellistri, E., and la Prida de L.M, Nat. Neurosci., 2015, vol. 18, no. 9, pp. 1281–1290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Varela, C., Front. Neural Circuits, 2014, vol. 8, Article 69.

  75. Scarpelli, S., D’Atri, A., Gorgoni, M., Ferrara, M., and De Gennaro, L., Front. Psychol., 2015, vol. 6, Article 605.

  76. Kubota, Y., Takasu, N.N., Horita, S., Kondo, M., Shimizu, M., Okada, T., Wakamura, T., and Toichi, M., Brain Res., 2011, vol. 1389, pp. 83–92.

    Article  CAS  PubMed  Google Scholar 

  77. McKenna, J.T. and Vertes, R.P., J. Comp. Neurol., 2004, vol. 480, no. 2, pp. 115–142.

    Article  PubMed  Google Scholar 

  78. 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 

  79. Goswamee, P. and McQuiston, A.R., Front. Cell Neurosci., 2019, vol. 13, Article 267.

  80. Varela, C., Kumar, S., Yang, J.Y., and Wilson, M.A., Brain Struct. Funct., 2014, vol. 219, no. 3, pp. 911–929.

    Article  CAS  PubMed  Google Scholar 

  81. Lee, S.H., Simons, S.B., Heldt, S.A., Zhao, M., Schroeder, J.P., Vellano, C.P., Cowan, D.P., Ramineni, S., Yates, C.K., Feng, Y., Smith, Y., Sweatt, J.D., Weinshenker, D., Ressler, K.J., Dudek, S.M., and Hepler, J.R., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 39, pp. 16994–16998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Lin, Y.T., Hsieh, T.Y., Tsai, T.C., Chen, C.C., Huang, C.C., and Hsu, K.S., J. Neurosci., 2018, vol. 38, no. 5, pp. 1218–1231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Karni, A., Tanne, D., Rubenstein, B.S., Askenasy, J.J., and Sagi, D., Science, 1994, vol. 265, no. 5172, pp. 679–682.

    Article  CAS  PubMed  Google Scholar 

  84. Plihal, W. and Born, J., J. Cogn. Neurosci., 1997, vol. 9, no. 4, pp. 534–547.

    Article  CAS  PubMed  Google Scholar 

  85. Louie, K. and Wilson, M.A., Neuron, 2001, vol. 29, no. 1, pp. 145–156.

    Article  CAS  PubMed  Google Scholar 

  86. Kudrimoti, H.S., Barnes, C.A., and McNaughton, B.L., J. Neurosci., 1999, vol. 19, no. 10, pp. 4090–4101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Abel, T., Havekes, R., Saletin, J.M., and Walker, M.P., Curr. Biol., 2013, vol. 23, no. 17, pp. R774–R788.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Senzai, Y. and Buzsáki, G., Neuron, 2017, vol. 93, no. 3, pp. 691–704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

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

    PubMed  Google Scholar 

  91. 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 

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

  93. 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 

  94. Sawangjit, A., Kelemen, E., Born, J., and Inostroza, M., Front. Behav. Neurosci., 2017, vol. 11, Article 28.

  95. Braak, H., Braak, E., Yilmazer, D., de Vos, R.A., Jansen, E.N., and Bohl, J., J. Neural Transm. (Vienna), 1996, vol. 103, no. 4, pp. 455–490.

    Article  CAS  Google Scholar 

  96. Tang, X., Qin, Y., Wu, J., Zhang, M., Zhu, W., and Miller, M.I., Magn. Reson. Imaging, 2016, vol. 34, no. 8, pp. 1087–1099.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Adamowicz, D.H., Roy, S., Salmon, D.P., Galasko, D.R., Hansen, L.A., Masliah, E., and Gage, F.H., J. Neurosci., 2017, vol. 37, no. 7, pp. 1675–1684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

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

Author information

Authors and Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, ul. Butlerova 5a, 117865, Moscow, Russia

    I. G. Silkis

Authors
  1. I. G. Silkis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. G. Silkis.

Ethics declarations

Conflict of Interest. The author declares that she has no conflict of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silkis, I.G. The Role of Hypothalamus in the Formation of Neural Representations of Object–Place Associations in the Hippocampus during Wakefulness and Paradoxical Sleep. Neurochem. J. 15, 139–147 (2021). https://doi.org/10.1134/S1819712421020148

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1819712421020148

Keywords:

Abbreviations:

Search

Navigation