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The contribution of dopamine to the functioning of the hippocampus during spatial learning (a hypothetical mechanism)

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Abstract

A hypothetical mechanism for the influence of dopamine on the formation of neuronal representations of “object–place” associations in the hippocampus is proposed for spatial learning. According to this mechanism, dopamine that is released in a new situation or during expectation of reinforcement improves conditions for the development of homosynaptic long-term potentiation (LTP) of the input to the dentate gyrus granule cells from the medial entorhinal cortex, which transmits information about spatial location of objects and characteristics of objects. The effect occurs due to the activation of D1/D5 receptors on granule cells and D2 receptors on inhibitory interneurons. Heterosynaptic depression is simultaneously developed in inputs that were not activated. As a result, a contrasting representation of the learned “object–place” association is formed on neurons of the dentate gyrus. From these neurons, information about the association via the CA3 field is transmitted to the radial layer of the CA1 field by Schaffer collaterals, whereas the stratum lacunosum-moleculare receives signals directly from the entorhinal cortex and thalamic nucleus reuniens, which connects the hippocampus with the prefrontal cortex. The sign of the modulatory influence of dopamine on the efficacy of excitatory inputs to pyramid neurons of the CA1 field depends on the relationship between excitation and inhibition of these neurons, as well as the dopamine concentration. By acting on D1/D5 receptors on the pyramidal neurons of the CA1 field, dopamine can promote LTP induction in Schaffer collaterals simultaneously with LTP induction in the relatively strong perforant input, whereas relatively weak perforant input, as well as the input from the nucleus reuniens, become depressed. This depression is promoted by the activation of D1/D5 receptors on the inhibitory interneurons of the CA1 field, induction of LTP in these neurons, and the following enhancement of afferent inhibition of pyramidal cells. As a consequence, neuronal representation of the learned “object–place” association in the CA1 field is distorted more weakly by non-relevant information that comes from the entorhinal cortex and thalamus. As a result, the error probability during the performance of spatial task decreases. Because activation of D1/D5 receptors on pyramidal neurons of the prefrontal cortex promotes LTP induction in the input from the CA1 field, dopamine must improve the goal-directed performance of spatial tasks. The proposed mechanism explains the results of some experimental studies that seemed to be contradictory or incomprehensible.

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Abbreviations

VTA:

ventral tegmental area

HFS:

high frequency stimulation

LTD:

long-term depression

LTP:

long-term potentiation

DG:

dentate gyrus

LP:

latent period

mPFC:

medial prefrontal cortex

LFS:

low frequency stimulation

PP:

perforant pathway

PPl and PPm:

lateral and medial perforant pathways

PFC:

prefrontal cortex

NR:

thalamic nucleus reuniens

EC:

entorhinal cortex

ECl and ECm:

lateral and medial parts of the entorhinal cortex

References

  1. Gilbert, P.E. and Kesner, R.P., Behav. Neurosci., 2002, vol. 116, no. 1, pp. 63–71.

    Article  PubMed  Google Scholar 

  2. Gilbert, P.E. and Kesner, R.P., Neurobiol. Learn. Mem., 2004, vol. 81, no. 1, pp. 39–45.

    Article  PubMed  Google Scholar 

  3. Gasbarri, A., Verney, C., Innocenzi, R., Campana, E., and Pacitti, C., Brain Res., 1994, vol. 668, nos. 1–2, pp. 71–79.

    Article  PubMed  Google Scholar 

  4. Bethus, I., Tse, D., and Morris, R.G., J. Neurosci., 2010, vol. 30, no. 5, pp. 1610–1618.

    Article  CAS  PubMed  Google Scholar 

  5. Rossato, J.I., Bevilaqua, L.R., Izquierdo, I., Medina, J.H., and Cammarota, M., Science, 2009, vol. 325, no. 5943, pp. 1017–1020.

    Article  CAS  PubMed  Google Scholar 

  6. Huang, Y.Y. and Kandel, E.R., Proc. Natl. Acad. Sci. USA, 1995, vol. 92, no. 7, pp. 2446–2450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Li, S., Cullen, W.K., Anwyl, R., and Rowan, M.J., Nat. Neurosci., 2003, vol. 6, no. 5, pp. 526–531.

    CAS  PubMed  Google Scholar 

  8. Nai, Q., Li, S., Wang, S.H., Liu, J., Lee, F.J., Frankland, P.W., and Liu, F., Biol. Psychiatry, 2010, vol. 67, no. 3, pp. 246–254.

    Article  CAS  PubMed  Google Scholar 

  9. Gasbarri, A., Sulli, A., Innocenzi, R., Pacitti, C., and Brioni, J.D., Neurosci., 1996, vol. 74, no. 4, pp. 1037–1044.

    Article  CAS  Google Scholar 

  10. Packard, M.G. and White, N.M., Behav. Neurosci., 1991, vol. 105, no. 2, pp. 295–306.

    Article  CAS  PubMed  Google Scholar 

  11. O’Carroll, C.M., Martin, S.J., Sandin, J., Frenguelli, B., and Morris, R.G., Learn. Mem., 2006, vol. 13, no. 6, pp. 760–769.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Tran, A.H., Uwano, T., Kimura, T., Hori, E., Katsuki, M., Nishijo, H., and Ono, T., J. Neurosci., 2008, vol. 28, no. 50, pp. 13390–13400.

    Article  CAS  PubMed  Google Scholar 

  13. da Silva, W.C., Köhler, C.C., Radiske, A., and Cammarota, M., Neurobiol. Learn. Mem., 2012, vol. 97, no. 2, pp. 271–275.

    Article  PubMed  CAS  Google Scholar 

  14. Clausen, B., Schachtman, T.R., Mark, L.T., Reinholdt, M., and Christoffersen, G.R., Behav. Brain Res., 2011, vol. 223, no. 2, pp. 241–254.

    Article  CAS  PubMed  Google Scholar 

  15. Mizumori, S.J.Y., N. Y. Oxford Univers. Press, 2008.

  16. Kentros, C.G., Agnihotri, N.T., Streater, S., Hawkins, R.D., and Kandel, E.R., Neuron, 2004, vol. 42, no. 2, pp. 283–295.

    Article  CAS  PubMed  Google Scholar 

  17. Martig, A.K. and Mizumori, S.J., Hippocampus, 2011, vol. 21, no. 2, p. 172.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Gill, K.M. and Mizumori, S.J., Behav. Neurosci., 2006, vol. 120, no. 2, pp. 377–392.

    Article  CAS  PubMed  Google Scholar 

  19. Martig, A.K. and Mizumori, S.J., Learn. Mem., 2011, vol. 18, no. 4, pp. 260–271.

    Article  PubMed  Google Scholar 

  20. Da Cunha, C., Silva, M.H., Wietzikoski, S., Wietzikoski, E.C., Ferro, M.M., Kouzmine, I., and Canteras, N.S., Behav. Neurosci., 2006, vol. 120, no. 6, pp. 1279–1284.

    Article  PubMed  Google Scholar 

  21. Pan, W.X., Schmidt, R., Wickens, J.R., and Hyland, B.I., J. Neurosci., 2005, vol. 25, no. 26, pp. 6235–6242.

    Article  CAS  PubMed  Google Scholar 

  22. Puryear, C.B., Kim, M.J., and Mizumori, S.J., Behav. Neurosci., 2010, no. 2, pp. 234–247.

    Article  Google Scholar 

  23. Kest, K., Cruz, I., Chen, D.H., Galaj, E., and Ranaldi, R., Behav. Brain Res., 2012, vol. 235, no. 2, pp. 150–157.

    Article  CAS  PubMed  Google Scholar 

  24. Ranaldi, R., Rev. Neurosci., 2014, vol. 25, no. 5, pp. 621–630.

    CAS  PubMed  Google Scholar 

  25. Sil’kis, I.G., Ross. Fiziol. Zhurn. im. I.M. Sechenova, 2007, vol. 93, no. 3, pp. 225–235.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  28. Petersen, R.P., Moradpour, F., Eadie, B.D., Shin, J.D., Kannangara, T.S., Delaney, K.R., and Christie B.R., Neurosci., 2013, vol. 252, pp. 154–168.

    Article  CAS  Google Scholar 

  29. van Groen, T., Miettinen, P., and Kadish, I., Hippocampus, 2003, vol. 13, no. 1, pp. 133–149.

    Article  PubMed  Google Scholar 

  30. Kosub, K.A., Do, V.H., and Derrick, B.E., Neurosci. Lett., 2005, vol. 374, no. 1, pp. 29–34.

    Article  CAS  PubMed  Google Scholar 

  31. Witter, M.P. and Amaral, D.G., J. Comp. Neurol., 1991, vol. 307, no. 3, pp. 437–459.

    Article  CAS  PubMed  Google Scholar 

  32. Craig, S. and Commins, S., Brain Res., 2007, vol. 1147, pp. 124–139.

    Article  CAS  PubMed  Google Scholar 

  33. Bartesaghi, R. and Gessi, T., Hippocampus, 2004, vol. 14, no. 8, pp. 948–963.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  35. Sil’kis, I.G., Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2002, vol. 52, no. 4, pp. 392–405.

    Google Scholar 

  36. Buckmaster, P.S. and Schwartzkroin, P.A., J. Neurosci., 1995, vol. 15, no. 1. (Pt. 2), pp. 774–789.

    CAS  PubMed  Google Scholar 

  37. Hayashi, H. and Nonaka, Y., Neural. Netw., 2011, vol. 24, no. 3, pp. 233–246.

    Article  PubMed  Google Scholar 

  38. Mott, D.D., Li, Q., Okazaki, M.M., Turner, D.A., and Lewis, D.V., J. Neurophysiol., 1999, vol. 82, no. 3, pp. 1438–1450.

    CAS  PubMed  Google Scholar 

  39. Brucato, F.H., Levin, E.D., Mott, D.D., Lewis, D.V., Wilson, W.A., and Swartzwelder, H.S., Neurosci., 1996, vol. 74, no. 2, pp. 331–339.

    Article  CAS  Google Scholar 

  40. Empson, R.M. and Heinemann, U., J. Physiol., 1995, vol. 484 (Pt. 3), pp. 707–720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Otmakhova, N.A. and Lisman, J.E., J. Neurosci., 1999, vol. 19, no. 4, pp. 1437–1445.

    CAS  PubMed  Google Scholar 

  42. McBain, C.J., Di Chiara, T.J., and Kauer, J.A., J. Neurosci., 1994, vol. 14, no. 7, pp. 4433–4445.

    CAS  PubMed  Google Scholar 

  43. Oliva, A.A., Jiang, M., Lam, T., Smith, K.L., and Swann, J.W., J. Neurosci., 2000, vol. 20, no. 9, pp. 3354–3368.

    CAS  PubMed  Google Scholar 

  44. Canning, K.J., Wu, K., Peloquin, P., Kloosterman, F., and Leung, L.S., Ann. NY Acad. Sci., 2000, vol. 911, pp. 55–72.

    Article  CAS  PubMed  Google Scholar 

  45. Yeckel, M.F. and Berger, T.W., Proc. Natl. Acad. Sci. USA, 1990, vol. 87, no. 15, pp. 5832–5836.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Gonzalez, J., Morales, I.S., Villarreal, D.M., and Derrick, B.E., J. Neurophysiol., 2014, vol. 111, no. 6, pp. 1259–1273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Pöschel, B. and Stanton, P.K., Prog. Brain Res., 2007, vol. 163, pp. 473–500.

    Article  PubMed  CAS  Google Scholar 

  48. Sil’kis, I.G., Zhurn. Vyssh. Nerv. Deyat., 1995, vol. 45, no. 6, pp. 1151–1166.

    Google Scholar 

  49. Lin, Y.W., Yang, H.W., Wang, H.J., Gong, C.L., Chiu, T.H., and Min, M.Y., Eur. J. Neurosci., 2006, vol. 23, no. 9, pp. 2362–2374.

    Article  PubMed  Google Scholar 

  50. Colbert, C.M. and Levy, W.B., J. Neurophysiol., 1992, vol. 68, no. 1, pp. 1–8.

    CAS  PubMed  Google Scholar 

  51. Levy, W.B., Desmond, N.L., and Zhang, D.X., Learn. Mem., 1998, vol. 4, no. 6, pp. 510–518.

    Article  CAS  PubMed  Google Scholar 

  52. Wang, J.H. and Stelzer, A., J. Neurophysiol., 1996, vol. 75, no. 4, pp. 1687–1702.

    CAS  PubMed  Google Scholar 

  53. Dvorak-Carbone, H. and Schuman, E.M., J. Neurophysiol., 1999, vol. 81, no. 3, pp. 1036–1044.

    CAS  PubMed  Google Scholar 

  54. Colbert, C.M. and Levy, W.B., Brain Res., 1993, vol. 606, no. 1, pp. 87–91.

    Article  CAS  PubMed  Google Scholar 

  55. Wöhrl, R., von Haebler, D., and Heinemann, U., Eur. J. Neurosci., 2007, vol. 25, no. 1, pp. 251–258.

    Article  PubMed  Google Scholar 

  56. Mott, D.D. and Lewis, D.V., Int. Rev. Neurobiol., 1994, vol. 36, pp. 97–223.

    Article  CAS  PubMed  Google Scholar 

  57. Remondes, M. and Schuman, E.M., Nature, 2002, vol. 416, no. 6882, pp. 736–740.

    Article  CAS  PubMed  Google Scholar 

  58. Gangarossa, G., Longueville, S., De Bundel, D., Perroy, J., Herve, D., Girault, J.A., and Valjent, E., Hippocampus, 2012, vol. 22, no. 12, pp. 2199–2207.

    Article  CAS  PubMed  Google Scholar 

  59. Goldsmith, S.K. and Joyce, J.N., Hippocampus, 1994, vol. 4, no. 3, pp. 354–373.

    Article  CAS  PubMed  Google Scholar 

  60. Khan, Z.U., Gutíerrez, A., Martín, R., Penafiel, A., Rivera, A., and De La Calle, A., J. Comp. Neurol., 1998, vol. 402, no. 3, pp. 353–371.

    Article  CAS  PubMed  Google Scholar 

  61. Mrzljak, L., Bergson, C., Pappy, M., Huff, R., Levenson, R., and Goldman-Rakic, P.S., Nature, 1996, vol. 381, no. 6579, pp. 245–248.

    Article  CAS  PubMed  Google Scholar 

  62. Romo-Parra, H., Aceves, J., and Gutierrez, R., Hippocampus, 2005, vol. 15, no. 2, pp. 254–259.

    Article  CAS  PubMed  Google Scholar 

  63. Mockett, B.G., Brooks, W.M., Tate, W.P., and Abraham, W.C., Brain Res., 2004, vol. 1021, no. 1, pp. 92–100.

    Article  CAS  PubMed  Google Scholar 

  64. Silkis, I.G., Biosystems, 1998, vol. 48, nos. 1–3, pp. 205–213.

    Article  CAS  PubMed  Google Scholar 

  65. Jenson, D., Yang, K., Acevedo-Rodriguez, A., Levine, A., Broussard, J.I., Tang, J., and Dani, J.A., Neuropharmacology, 2015, vol. 90, pp. 23–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Yang, K. and Dani, J.A., J. Neurosci., 2014, vol. 34, no. 48, pp. 15888–15897.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Kulla, A. and Manahan-Vaughan, D., Cereb. Cortex, 2000, vol. 10, no. 6, pp. 614–620.

    Article  CAS  PubMed  Google Scholar 

  68. Davis, C.D., Jones, F.L., and Derrick, B.E., J. Neurosci., 2004, vol. 24, no. 29, pp. 6497–6506.

    Article  CAS  PubMed  Google Scholar 

  69. Zeineh, M.M., Engel, S.A., Thompson, P.M., and Bookheimer, S.Y., Science, 2003, vol. 299, no. 5606, pp. 577–580.

    Article  CAS  PubMed  Google Scholar 

  70. Schultz, W., J. Neurophysiol., 1998, vol. 80, no. 1, pp. 1–27.

    CAS  PubMed  Google Scholar 

  71. Wiescholleck, V. and Manahan-Vaughan, D., Hippocampus, 2014, vol. 24, no. 12, pp. 1615–1622.

    Article  CAS  PubMed  Google Scholar 

  72. Saab, B.J., Georgiou, J., Nath, A., Lee, F.J., Wang, M., Michalon, A., Liu, F., Mansuy, I.M., and Roder, J.C., Neuron, 2009, vol. 63, no. 5, pp. 643–656.

    Article  CAS  PubMed  Google Scholar 

  73. Xu, T.X. and Yao, W.D., Proc. Natl. Acad. Sci. USA, 2010, vol. 107, no. 37, pp. 16366–16371.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Xu, T.X., Ma, Q., Spealman, R.D., and Yao, W.D., J. Neurochem., 2010, vol. 115, no. 6, pp. 1643–1654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Navakkode, S., Sajikumar, S., Korte, M., and Soong, T.W., Learn. Mem., 2012, vol. 19, no. 7, pp. 294–299.

    Article  CAS  PubMed  Google Scholar 

  76. Ito, H.T. and Schuman, E.M., Front. Neural. Circuits, 2007, p. 1.1doi 10.3389/neuro.04.001.2007

    Google Scholar 

  77. Hansen, N. and Manahan-Vaughan, D., Cereb. Cortex, 2014, vol. 24, no. 4, pp. 845–858.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Otmakhova, N.A. and Lisman, J.E., J. Neurosci., 1996, vol. 16, no. 23, pp. 7478–7486.

    CAS  PubMed  Google Scholar 

  79. Rozas, C., Carvallo, C., Contreras, D., Carreño, M., Ugarte, G., Delgado, R., Zeise, M.L., and Morales, B., Neuropharmacology, 2015, vol. 99, pp. 15–27.

    Article  CAS  PubMed  Google Scholar 

  80. Suárez, L.M., Bustamante, J., and Orensanz, L.M., Martín del Río, R., Solís, J.M., Neuropharmacology, 2014, vol. 79, pp. 101–111.

    Article  PubMed  CAS  Google Scholar 

  81. Navakkode, S., Sajikumar, S., and Frey, J.U., Neuropharmacology, 2007, vol. 52, no. 7, pp. 1547–1554.

    Article  CAS  PubMed  Google Scholar 

  82. Roggenhofer, E., Fidzinski, P., Shor, O., and Behr, J., PLoS One, 2013, vol. 8, no. 4.

    Google Scholar 

  83. Varela, J.A., Hirsch, S.J., Chapman, D., Leverich, L.S., and Greene, R.W., J. Neurosci., 2009, vol. 29, no. 10, pp. 3109–3119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ito, H.T., Smith, S.E., Hsiao, E., and Patterson, P.H., Brain Behav. Immun., 2010, vol. 24, no. 7, pp. 930–941.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Manahan-Vaughan, D. and Braunewell, K.H., Proc. Natl. Acad. Sci. USA, 1999, vol. 96, no. 15, pp. 8739–8744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Lemon, N. and Manahan-Vaughan, D., J. Neurosci., 2006, vol. 26, no. 29, pp. 7723–7729.

    Article  CAS  PubMed  Google Scholar 

  87. Wei, C.L., Liu, Y.H., Yang, M.H., Liu, Z.Q., and Ren, W., Neurosignals, 2013, vol. 21, nos. 3–4, pp. 150–159.

    Article  CAS  PubMed  Google Scholar 

  88. Liu, N., Xue, B., Xing, H., Xu, L., and Jiang, S.X., Sheng Li Xue Bao, 2009, vol. 61, no. 6, pp. 511–516.

    CAS  PubMed  Google Scholar 

  89. Swant, J., Chirwa, S., Stanwood, G., and Khoshbouei, H., PLoS One, 2010, vol. 5, no. 6.

    Google Scholar 

  90. Chen, Z., Ito, K., Fujii, S., Miura, M., Furuse, H., Sasaki, H., Kaneko, K., Kato, H., and Miyakawa, H., Receptors Channels, 1996, vol. 4, no. 1, pp. 1–8.

    CAS  PubMed  Google Scholar 

  91. Bartsch, J.C., Fidzinski, P., Huck, J.H., Hörtnagl, H., Kovács, R., Liotta, A., Priller, J., Wozny, C., and Behr, J., Neuropsychopharmacology, 2015, vol. 40, no. 4, pp. 987–995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Herwerth, M., Jensen, V., Novak, M., Konopka, W., Hvalby, O., and Köhr, G., Cereb. Cortex, 2012, vol. 22, no. 8, pp. 1786–1798.

    Article  PubMed  Google Scholar 

  93. Sil’kis, I.G., Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2014, vol. 64, no. 1, pp. 82–100.

    Google Scholar 

  94. Thierry, A.M., Gioanni, Y., égénétais, E., and Glowinski, J., DHippocampus, 2000, vol. 10, no. 4, pp. 411–419.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  96. Cassel, J.C., Pereira de Vasconcelos, A., Loureiro, M., Cholvin, T., Dalrymple-Alford, J.C., and Vertes, R.P., Prog. Neurobiol., 2013, vol. 111, pp. 34–52.

    Article  PubMed  Google Scholar 

  97. Bokor, H., Csáki, A., Kocsis, K., and Kiss, J., Eur. J. Neurosci., 2002, vol. 16, no. 7, pp. 1227–1239.

    Article  PubMed  Google Scholar 

  98. Dolleman van der Weel, M.J. and Witter, M.P., Neurosci. Let., 2000, vol. 278, no. 3, pp. 145–148.

    Article  CAS  Google Scholar 

  99. Vertes, R.P., Hoover, W.B., Do Valle, A.C., Sherman, A., and Rodriguez, J.J., J. Comp. Neurol., 2006, vol. 499, no. 5, pp. 768–796.

    Article  PubMed  Google Scholar 

  100. Bertram, E.H. and Zhang, D.X., Neurosci., 1999, vol. 92, no. 1, pp. 15–26.

    Article  CAS  Google Scholar 

  101. Ito, H.T., Zhang, S.J., Witter, M.P., Moser, E.I., and Moser, M.B., Nature, 2015, vol. 522, no. 7554, pp. 50–55.

    Article  CAS  PubMed  Google Scholar 

  102. Vertes, R.P., Prog. Brain Res., 2015, vol. 219, pp. 121–144.

    Article  PubMed  Google Scholar 

  103. Oda, S., Funato, H., Adachi-Akahane, S., Ito, M., Okada, A., Igarashi, H., Yokofujita, J., and Kuroda, M., Brain Res., 2010, vol. 1329, pp. 89–102.

    Article  CAS  PubMed  Google Scholar 

  104. Jay, T.M., Rocher, C., Hotte, M., Naudon, L., and Gurden, H., Spedding M., Neurotox Res., 2004, vol. 6, no. 3. pp. 233–244.

    Article  PubMed  Google Scholar 

  105. Ishikawa, A., Kadota, T., Kadota, K., Matsumura, H., and Nakamura, S., Eur. J. Neurosci., 2005, vol. 22, no. 7, pp. 1713–1719.

    Article  PubMed  Google Scholar 

  106. Dommett, E., Coizet, V., Blaha, C.D., Martindale, J., Lefebvre, V., Walton, N., Mayhew, J.E., Overton, P.G., and Redgrave, P., Science, 2005, vol. 307, no. 5714, pp. 1476–1479.

    Article  CAS  PubMed  Google Scholar 

  107. Kemp, A. and Manahan-Vaughan, D., Proc. Natl. Acad. Sci. USA, 2004, vol. 101, no. 21, pp. 8192–8197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Knight, R.T., Nature, 1996, vol. 383, no. 10, pp. 256–259.

    Article  CAS  PubMed  Google Scholar 

  109. Goh, J.J. and Manahan-Vaughan, D., Front. Integr. Neurosci., 2013, vol. 7, p. 1. doi 10.3389/fnint.2013.00001

    Article  PubMed  PubMed Central  Google Scholar 

  110. Lisman, J.E. and Otmakhova, N.A., Hippocampus, 2001, vol. 11, no. 5, pp. 551–568.

    Article  CAS  PubMed  Google Scholar 

  111. Dolleman van der Weel, M.J., Lopes da Silva, F.H., and Witter, M.P., J. Neurosci., 1997, vol. 17, no. 14, pp. 5640–5650.

    CAS  PubMed  Google Scholar 

  112. Cohen, B.M., Wan, W., Froimowitz, M.P., Ennulat, D.J., Cherkerzian, S., and Konieczna, H., Psychopharmacology (Berl.), 1998, vol. 135, no. 1, pp. 37–43.

    Article  CAS  Google Scholar 

  113. Knierim, J.J., Lee, I., and Hargreaves, E.L., Hippocampus, 2006, vol. 16, no. 9, pp. 755–764.

    Article  PubMed  Google Scholar 

  114. Kirkby, D.L. and Higgins, G.A., Eur. J. Neurosci., 1998, vol. 10, no. 3, pp. 823–838.

    Article  CAS  PubMed  Google Scholar 

  115. Wilson, D.I., Langston, R.F., Schlesiger, M.I., Wagner, M., Watanabe, S., and Ainge, J.A., Hippocampus, 2013, vol. 3, no. 5, pp. 352–366.

    Article  Google Scholar 

  116. Duan, T.T., Tan, J.W., Yuan, Q., Cao, J., Zhou, Q.X., and Xu, L., Psychopharmacology (Berl.), 2013, vol. 228, no. 3, pp. 451–461.

    Article  CAS  Google Scholar 

  117. Sariñana, J., Kitamura, T., Künzler P., Sultzman, L., and Tonegawa, S., Proc. Natl. Acad. Sci. USA, 2014, vol. 111, no. 22, pp. 8245–8250.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Furini, C.R., Myskiw, J.C., Schmidt, B.E., Marcondes, L.A., and Izquierdo, I., Behav. Brain Res., 2014, vol. 271, pp. 212–217.

    Article  CAS  PubMed  Google Scholar 

  119. Esmaeili, M.H., Kermani, M., Parvishan, A., and Haghparast, A., Behav. Brain Res., 2012, vol. 231, no. 19, pp. 111–115.

    Article  CAS  PubMed  Google Scholar 

  120. Subramaniyan, S., Hajali, V., Scherf, T., Sase, S.J., Sialana, F.J., Gröger, M., Bennett, K.L., Pollak, A., Li, L., Korz, V., and Lubec, G., Behav. Brain Res., 2015, vol. 283, pp. 162–174.

    Article  CAS  PubMed  Google Scholar 

  121. Liao, Y., Shi, Y.W., Liu, Q.L., and Zhao, H., Brain Res., 2013, vol. 1524, pp. 26–33.

    Article  CAS  PubMed  Google Scholar 

  122. Ortiz, O., Delgado-García, J.M., Espadas, I., Bahí, A., Trullas, R., Dreyer, J.L., Gruart, A., and Moratalla, R., J. Neurosci., 2010, vol. 30, no. 37, pp. 12288–12300.

    Article  CAS  PubMed  Google Scholar 

  123. Sariñana, J. and Tonegawa, S., Hippocampus, 2015. doi 10.1002/hipo.22492 [Epub. ahead of print].

    Google Scholar 

  124. Wan, P., Wang, S., Zhang, Y., Lv, J., and Jin, Q.H., Pharmazie, 2014, vol. 69, no. 9, pp. 709–710.

    CAS  PubMed  Google Scholar 

  125. Morgan R., Gibbs, J.T., Melief, E.J., Postupna, N.O., Sherfield, E.E., Wilson, A., Dirk, KeeneC., Montine, T.J., Palmiter, R.D., and Darvas, M., Exp. Neurol., 2015, vol. 271, pp. 205–214.

    Article  CAS  Google Scholar 

  126. Hallock, H.L., Wang, A., Shaw, C.L., and Griffin, A.L., Behav. Neurosci., 2013, vol. 127, no. 6, pp. 860–866.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Loureiro, M., Cholvin, T., Lopez, J., Merienne, N., Latreche, A., Cosquer, B., Geiger, K., Kelche, C., Cassel, J.C., and Pereira de Vasconcelos, A., J. Neurosci., 2012, vol. 32, no. 29, pp. 9947–9959.

    Article  CAS  PubMed  Google Scholar 

  128. Hembrook, J.R., Onos, K.D., and Mair, R.G., Hippocampus, 2012, vol. 22, no. 4, pp. 853–860.

    Article  CAS  PubMed  Google Scholar 

  129. Cassel, J.C., Pereira de Vasconcelos, A., Loureiro, M., Cholvin, T., Dalrymple-Alford, J.C., and Vertes, R.P., Prog. Neurobiol., 2013, vol. 111, pp. 34–52.

    Article  PubMed  Google Scholar 

  130. Wang, G.W. and Cai, J.X., Behav. Brain Res., 2006, vol. 175, no. 2, pp. 329–336.

    Article  PubMed  Google Scholar 

  131. Griffin, A.L., Front. Syst. Neurosci., 2015, vol. 9, p. 29. doi 10.3389/fnsys.2015.00029

    Article  PubMed  PubMed Central  Google Scholar 

  132. Werlen, E. and Jones, M.W., Prog. Brain Res., 2015, vol. 219, pp. 187–216.

    Article  PubMed  Google Scholar 

  133. Seamans, J.K., Floresco, S.B., and Phillips, A.G., J. Neurosci., 1998, vol. 18, no. 4, pp. 1613–1621.

    CAS  PubMed  Google Scholar 

  134. Floresco, S.B. and Phillips, A.G., Behav. Neurosci., 2001, vol. 115, no. 4, pp. 934–939.

    Article  CAS  PubMed  Google Scholar 

  135. Savalli, G., Bashir, Z.I., and Warburton, E.C., Learn. Mem., 2015, vol. 22, no. 2, pp. 69–73.

    Article  PubMed  PubMed Central  Google Scholar 

  136. Rusu, G., Popa, G., Ochiuz, L., Nechifor, M., and Tartau, L., Rev. Med. Chir. Soc. Med. Nat. Iasi, 2014, vol. 118, no. 1, pp. 116–124.

    PubMed  Google Scholar 

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  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

    I. G. Silkis

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Original Russian Text © I.G. Silkis, 2016, published in Neirokhimiya, 2016, Vol. 33, No. 1, pp. 42–55.

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Silkis, I.G. The contribution of dopamine to the functioning of the hippocampus during spatial learning (a hypothetical mechanism). Neurochem. J. 10, 34–46 (2016). https://doi.org/10.1134/S181971241601013X

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