Cannabinoid-mediated short-term plasticity in hippocampus

Abstract

Endocannabinoids (eCBs) modulate both excitatory and inhibitory neurotransmission in hippocampus via activation of pre-synaptic cannabinoid receptors. Here, we present a model for cannabinoid mediated short-term depression of excitation (DSE) based on our recently developed model for the equivalent phenomenon of suppressing inhibition (DSI). Furthermore, we derive a simplified formulation of the calcium-mediated endocannabinoid synthesis that underlies short-term modulation of neurotransmission in hippocampus. The simplified model describes cannabinoid-mediated short-term modulation of both hippocampal inhibition and excitation and is ideally suited for large network studies. Moreover, the implementation of the simplified DSI/DSE model provides predictions on how both phenomena are modulated by the magnitude of the pre-synaptic cell’s activity. In addition we demonstrate the role of DSE in shaping the post-synaptic cell’s firing behaviour qualitatively and quantitatively in dependence on eCB availability and the pre-synaptic cell’s activity. Finally, we explore under which conditions the combination of DSI and DSE can temporarily shift the fine balance between excitation and inhibition. This highlights a mechanism by which eCBs might act in a neuro-protective manner during high neural activity.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Alger, B.E. (2002). Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Progress in Neurobiology, 68(4), 247–286.

    CAS  PubMed  Article  Google Scholar 

  2. Blair, R.E. (2006). Activation of the cannabinoid type-1 receptor mediates the anticonvulsant properties of cannabinoids in the hippocampal neuronal culture models of acquired epilepsy and status epilepticus. Journal of Pharmacology and Experimental Therapeutics, 317(3), 1072–1078.

    CAS  PubMed  Article  Google Scholar 

  3. Chen, K., Neu, A., Howard, A.L., Foldy, C., Echegoyen, J., Hilgenberg, L., Smith, M., Mackie, K., Soltesz, I. (2007). Prevention of plasticity of endocannabinoid signaling inhibits persistent limbic hyperexcitability caused by developmental seizures. Journal of Neuroscience, 27(1), 46–58.

    PubMed  Article  Google Scholar 

  4. Diana, M.A., & Marty, A. (2004). Endocannabinoid-mediated short-term synaptic plasticity: depolarization-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). British Journal of Pharmacology, 142(1), 9–19.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  5. Földy, C., Neu, A., Jones, M.V., Soltesz, I. (2006). Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release. Journal of Neuroscience, 26(5), 1465–1469.

    PubMed  Article  Google Scholar 

  6. Gao, Y., Vasilyev, D.V., Goncalves, M.B., Howell, F.V., Hobbs, C., Reisenberg, M., Shen, R., Zhang, M.Y., Strassle, B.W., Lu, P., et al (2010). Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. Journal of Neuroscience, 30(6), 2017–2024.

    CAS  PubMed  Article  Google Scholar 

  7. Glickfeld, L.L., & Scanziani, M. (2006). Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nature Neuroscience, 9(6), 807–815.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  8. Goodman, D.F.M. (2009). The brian simulator. Frontiers in Neuroscience, 3(2), 192–197.

    PubMed Central  PubMed  Article  Google Scholar 

  9. Guo, J., & Ikeda, S.R. (2004). Endocannabinoids modulate N-type calcium channels and G-protein-coupled inwardly rectifying potassium channels via CB1 cannabinoid receptors heterologously expressed in mammalian neurons. Molecular Pharmacology, 65(3), 665–674.

    CAS  PubMed  Article  Google Scholar 

  10. Hajos, N., & Freund, T.F. (2002). Distinct cannabinoid sensitive receptors regulate hippocampal excitation and inhibition. Chemistry and Physics of Lipids, 121(1–2), 73–82.

    CAS  PubMed  Article  Google Scholar 

  11. Hashimotodani, Y., Ohno-Shosaku, T., Watanabe, M., Kano, M. (2007). Roles of phospholipase cbeta and NMDA receptor in activity-dependent endocannabinoid release. Journal of Physiology, 584, 373–380.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  12. Hemond, P., Epstein, D., Boley, A., Migliore, M., Ascoli, G.A., Jaffe, D.B. (2008). Distinct classes of pyramidal cells exhibit mutually exclusive firing patterns in hippocampal area CA3b. Hippocampus, 18(4), 411–424.

    PubMed  Article  Google Scholar 

  13. Hines, M.L., Morse, T., Migliore, M., Carnevale, N.T., Shepherd, G.M. (2004). Modeldb: A database to support computational neuroscience. Journal of Computational Neuroscience, 17(1), 7–11.

    PubMed Central  PubMed  Article  Google Scholar 

  14. Huguenard, J., & Mccormick, D.A. (1994). Electrophysiology of the neuron: an interactive tutorial. New York: Oxford University Press.

  15. Iremonger, K.J., Wamsteeker Cusulin, J.I., Bains, J.S. (2013). Changing the tune: plasticity and adaptation of retrograde signals. Trends in Neurosciences, 36(8), 471–479.

    CAS  PubMed  Article  Google Scholar 

  16. Kano, M., Ohno-Shosaku, T., Hashimotodani, Y., Uchigashima, M., Watanabe, M. (2009). Endocannabinoid-mediated control of synaptic transmission. Physiological Reviews, 89(1), 309–380.

    CAS  PubMed  Article  Google Scholar 

  17. Kim, J., & Alger, B.E. (2004). Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nature Neuroscience, 7(7), 697–698.

    CAS  PubMed  Article  Google Scholar 

  18. Lenz, R.A., & Alger, B.E. (1999). Calcium dependence of depolarization-induced suppression of inhibition in rat hippocampal CA1 pyramidal neurons. Journal of Physiology, 521, 147–157.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Marsicano, G. (2003). Cb1 cannabinoid receptors and on-demand defense against excitotoxicity. Science, 302(5642), 84–88.

    CAS  PubMed  Article  Google Scholar 

  20. MATLAB (2010). version 7.10.0 (R2010a). The MathWorks Inc., Natick, Massachusetts.

  21. Monory, K., & Lutz, B. (2008). The endocannabinoid system as a therapeutic target in epilepsy. Cannabinoids and the Brain, 407–422.

  22. Monory, K., Massa, F., Egertová, M., Eder, M., Blaudzun, H., Westenbroek, R., Kelsch, W., Jacob, W., Marsch, R., Ekker, M., et al (2006). The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron, 51(4), 455–466.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  23. Morishita, W., & Alger, B.E. (1999). Evidence for endogenous excitatory amino acids as mediators in DSI of GABA(A)ergic transmission in hippocampal CA1. Journal of Neurophysiology, 82, 2556–2564.

    CAS  PubMed  Google Scholar 

  24. Nowacki, J. (2011). Xppy. URL http://seis.bris.ac.uk/enxjn/xppy/.

  25. Ohno-Shosaku, T., Maejima, T., Kano, M. (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron, 29(3), 729–738.

    CAS  PubMed  Article  Google Scholar 

  26. Ohno-Shosaku, T., Shosaku, J., Tsubokawa, H., Kano, M. (2002a). Cooperative endocannabinoid production by neuronal depolarization and group i metabotropic glutamate receptor activation. European Journal of Neuroscience, 15(6), 953–961.

    Article  Google Scholar 

  27. Ohno-Shosaku, T., Tsubokawa, H., Mizushima, I., Yoneda, N., Zimmer, A., Kano, M. (2002b). Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. Journal of Neuroscience, 22(10), 3864–3872.

    CAS  Google Scholar 

  28. Pan, B., Wang, W., Zhong, P., Blankman, J.L., Cravatt, B.F., Liu, Q. (2011). Alterations of endocannabinoid signaling, synaptic plasticity, learning, and memory in monoacylglycerol lipase knock-out mice. Journal of Neuroscience, 31(38), 13, 420–13, 430.

    CAS  Article  Google Scholar 

  29. Peterfi, Z., Urban, G.M., Papp, O.I., Nemeth, B., Monyer, H., Szabo, G., Erdelyi, F., Mackie, K., Freund, T.F., Hajos, N., et al (2012). Endocannabinoid-mediated long-term depression of afferent excitatory synapses in hippocampal pyramidal cells and gabaergic interneurons. Journal of Neuroscience, 32(41), 14, 448–14, 463.

    CAS  Article  Google Scholar 

  30. Piomelli, D., Giuffrida, A., Calignano, A., Rodriguez de Fonseca, F. (2000). The endocannabinoid system as a target for therapeutic drugs. Trends in Pharmacological Sciences, 21(6), 218–224.

    CAS  PubMed  Article  Google Scholar 

  31. De Schutter, E., & Smolen, P. (1998). Methods in neuronal modeling: from ions to networks, The MIT Press, chapter Calcium dynamics in large neuronal models.

  32. Shinomoto, S., & Sakai, Y. (1999). Inter-spike interval statistics of cortical neurons. Lecture Notes in Computer Science, 171–179.

  33. Straiker, A., Wager-Miller, J., Hu, S.S., Blankman, J.L., Cravatt, B.F., Mackie, K. (2011). COX-2 and fatty acid amide hydrolase can regulate the time course of depolarization-induced suppression of excitation. British Journal of Pharmacology, 164(6), 1672–1683.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  34. Tanimura, A., Yamazaki, M., Hashimotodani, Y., Uchigashima, M., Kawata, S., Abe, M., Kita, Y., Hashimoto, K., Shimizu, T., Watanabe, M., Sakimura, K., Kano, M. (2010). The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron, 65, 320–327.

    CAS  PubMed  Article  Google Scholar 

  35. Traub, R.D., & Miles, R. (1991). Neuronal Networks of the Hippocampus. New York: Cambridge University Press.

  36. Wang, J., & Zucker, R.S. (2001). Photolysis-induced suppression of inhibition in rat hippocampal CA1 pyramidal neurons. Journal of Physiology, 533 (Pt 3), 757–763.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  37. Wang, X.J., & Buzsaki, G. (1996). Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network. Journal of Neuroscience, 16, 6402–6413.

    CAS  PubMed  Google Scholar 

  38. Wilson, R.I., & Nicoll, R.A. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature, 410(6828), 1–4.

    Article  Google Scholar 

  39. Zachariou, M., Alexander, S.P., Coombes, S., Christodoulou, C. (2013). A biophysical model of endocannabinoid-mediated short term depression in hippocampal inhibition. PloS ONE, 8(3), e58,926.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Chris Christodoulou and Stephen Coombes for useful comments and discussions. The authors also wish to acknowledge the anonymous reviewers for their helpful comments to the manuscript. This work was co-funded by the European Regional Development Fund and the Republic of Cyprus through the Research Promotion Foundation (DIDAKTOR/0609/12) and by a Young Researchers grant from the University of Cyprus.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Margarita Zachariou.

Additional information

Conflict of interest

The authors declare that they have no conflict of interest.

Action Editor: Claudia Clopath

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zachariou, M., Thul, R. Cannabinoid-mediated short-term plasticity in hippocampus. J Comput Neurosci 37, 533–547 (2014). https://doi.org/10.1007/s10827-014-0518-4

Download citation

Keywords

  • Calcium
  • DSI
  • DSE
  • Endocannabinoids
  • Hippocampus
  • Short-term plasticity