Advertisement

Journal of Computational Neuroscience

, Volume 33, Issue 3, pp 573–585 | Cite as

Neuromodulatory changes in short-term synaptic dynamics may be mediated by two distinct mechanisms of presynaptic calcium entry

  • Myongkeun Oh
  • Shunbing Zhao
  • Victor Matveev
  • Farzan NadimEmail author
Article

Abstract

Although synaptic output is known to be modulated by changes in presynaptic calcium channels, additional pathways for calcium entry into the presynaptic terminal, such as non-selective channels, could contribute to modulation of short term synaptic dynamics. We address this issue using computational modeling. The neuropeptide proctolin modulates the inhibitory synapse from the lateral pyloric (LP) to the pyloric dilator (PD) neuron, two slow-wave bursting neurons in the pyloric network of the crab Cancer borealis. Proctolin enhances the strength of this synapse and also changes its dynamics. Whereas in control saline the synapse shows depression independent of the amplitude of the presynaptic LP signal, in proctolin, with high-amplitude presynaptic LP stimulation the synapse remains depressing while low-amplitude stimulation causes facilitation. We use simple calcium-dependent release models to explore two alternative mechanisms underlying these modulatory effects. In the first model, proctolin directly targets calcium channels by changing their activation kinetics which results in gradual accumulation of calcium with low-amplitude presynaptic stimulation, leading to facilitation. The second model uses the fact that proctolin is known to activate a non-specific cation current I MI . In this model, we assume that the MI channels have some permeability to calcium, modeled to be a result of slow conformation change after binding calcium. This generates a gradual increase in calcium influx into the presynaptic terminals through the modulatory channel similar to that described in the first model. Each of these models can explain the modulation of the synapse by proctolin but with different consequences for network activity.

Keywords

Neuromodulation Proctolin Short-term synaptic dynamics Pyloric network 

Notes

Acknowledgements

This work was supported by the National Science Foundation grant DMS-0817703 (VM) and the National Institute of Mental Health grant MH060605 (FN).

References

  1. Abbott, L. F., Varela, J. A., Sen, K., & Nelson, S. B. (1997). Synaptic depression and cortical gain control. Science, 275(5297), 220–224.PubMedCrossRefGoogle Scholar
  2. Ayali, A., Johnson, B. R., & Harris-Warrick, R. M. (1998). Dopamine modulates graded and spike-evoked synaptic inhibition independently at single synapses in pyloric network of lobster. Journal of Neurophysiology, 79(4), 2063–2069.PubMedGoogle Scholar
  3. Babich, O., Matveev, V., Harris, A. L., & Shirokov, R. (2007). Ca2+-dependent inactivation of CaV1.2 channels prevents Gd3+ block: does Ca2+ block the pore of inactivated channels? Journal of General Physiology, 129(6), 477–483.PubMedCrossRefGoogle Scholar
  4. Bardoni, R., Torsney, C., Tong, C. K., Prandini, M., & MacDermott, A. B. (2004). Presynaptic NMDA receptors modulate glutamate release from primary sensory neurons in rat spinal cord dorsal horn. Journal of Neuroscience, 24(11), 2774–2781.PubMedCrossRefGoogle Scholar
  5. Barriere, G., Tartas, M., Cazalets, J. R., & Bertrand, S. S. (2008). Interplay between neuromodulator-induced switching of short-term plasticity at sensorimotor synapses in the neonatal rat spinal cord. The Journal of Physiology, 586(7), 1903–1920.PubMedCrossRefGoogle Scholar
  6. Berretta, N., & Jones, R. S. (1996). Tonic facilitation of glutamate release by presynaptic N-methyl-D-aspartate autoreceptors in the entorhinal cortex. Neuroscience, 75(2), 339–344.PubMedCrossRefGoogle Scholar
  7. Bertram, R., Sherman, A., & Stanley, E. F. (1996). Single-domain/bound calcium hypothesis of transmitter release and facilitation. Journal of Neurophysiology, 75(5), 1919–1931.PubMedGoogle Scholar
  8. Bertram, R., Swanson, J., Yousef, M., Feng, Z. P., & Zamponi, G. W. (2003). A minimal model for G protein-mediated synaptic facilitation and depression. Journal of Neurophysiology, 90(3), 1643–1653.PubMedCrossRefGoogle Scholar
  9. Bieda, M. C., & Copenhagen, D. R. (2004). N-type and L-type calcium channels mediate glycinergic synaptic inputs to retinal ganglion cells of tiger salamanders. Visual Neuroscience, 21(4), 545–550.PubMedCrossRefGoogle Scholar
  10. Borst, J. G., & Sakmann, B. (1998). Facilitation of presynaptic calcium currents in the rat brainstem. The Journal of Physiology, 513(Pt 1), 149–155.PubMedCrossRefGoogle Scholar
  11. Buchholtz, F., Golowasch, J., Epstein, I. R., & Marder, E. (1992). Mathematical model of an identified stomatogastric ganglion neuron. Journal of Neurophysiology, 67(2), 332–340.PubMedGoogle Scholar
  12. Chance, F. S., Nelson, S. B., & Abbott, L. F. (1998). Synaptic depression and the temporal response characteristics of V1 cells. Journal of Neuroscience, 18(12), 4785–4799.PubMedGoogle Scholar
  13. Cuttle, M. F., Tsujimoto, T., Forsythe, I. D., & Takahashi, T. (1998). Facilitation of the presynaptic calcium current at an auditory synapse in rat brainstem. The Journal of Physiology, 512(Pt 3), 723–729.PubMedCrossRefGoogle Scholar
  14. Dittman, J. S., Kreitzer, A. C., & Regehr, W. G. (2000). Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. Journal of Neuroscience, 20(4), 1374–1385.PubMedGoogle Scholar
  15. Fossier, P., Tauc, L., & Baux, G. (1999). Calcium transients and neurotransmitter release at an identified synapse. Trends in Neurosciences, 22(4), 161–166.PubMedCrossRefGoogle Scholar
  16. Galarreta, M., & Hestrin, S. (1998). Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nature Neuroscience, 1(7), 587–594.PubMedCrossRefGoogle Scholar
  17. Golowasch, J., & Marder, E. (1992). Proctolin activates an inward current whose voltage dependence is modified by extracellular Ca2+. Journal of Neuroscience, 12(3), 810–817.PubMedGoogle Scholar
  18. Gray, M. L., & Golowasch, J. (2011) Intracellular signaling of peptidergic neuromodulatory input to the pyloric network in the stomatogastric ganglion of Cancer borealis. In Soc Neurosci Abst, 2011 (Vol. 37, Vol. 707.04)Google Scholar
  19. Gundlfinger, A., Leibold, C., Gebert, K., Moisel, M., Schmitz, D., & Kempter, R. (2007). Differential modulation of short-term synaptic dynamics by long-term potentiation at mouse hippocampal mossy fibre synapses. The Journal of Physiology, 585(Pt 3), 853–865.PubMedCrossRefGoogle Scholar
  20. Hermann, J., Grothe, B., & Klug, A. (2009). Modeling short-term synaptic plasticity at the calyx of held using in vivo-like stimulation patterns. Journal of Neurophysiology, 101(1), 20–30.PubMedCrossRefGoogle Scholar
  21. Hige, T., Fujiyoshi, Y., & Takahashi, T. (2006). Neurosteroid pregnenolone sulfate enhances glutamatergic synaptic transmission by facilitating presynaptic calcium currents at the calyx of Held of immature rats. European Journal of Neuroscience, 24(7), 1955–1966.PubMedCrossRefGoogle Scholar
  22. Inchauspe, C. G., Martini, F. J., Forsythe, I. D., & Uchitel, O. D. (2004). Functional compensation of P/Q by N-type channels blocks short-term plasticity at the calyx of held presynaptic terminal. Journal of Neuroscience, 24(46), 10379–10383.PubMedCrossRefGoogle Scholar
  23. Ishikawa, T., Kaneko, M., Shin, H. S., & Takahashi, T. (2005). Presynaptic N-type and P/Q-type Ca2+ channels mediating synaptic transmission at the calyx of Held of mice. The Journal of Physiology, 568(Pt 1), 199–209.PubMedCrossRefGoogle Scholar
  24. Johnson, B. R., Brown, J. M., Kvarta, M. D., Lu, J. Y., Schneider, L. R., Nadim, F., et al. (2011). Differential modulation of synaptic strength and timing regulate synaptic efficacy in a motor network. Journal of Neurophysiology, 105(1), 293–304.PubMedCrossRefGoogle Scholar
  25. Johnson, B. R., Kloppenburg, P., & Harris-Warrick, R. M. (2003). Dopamine modulation of calcium currents in pyloric neurons of the lobster stomatogastric ganglion. Journal of Neurophysiology, 90(2), 631–643.PubMedCrossRefGoogle Scholar
  26. Johnson, B. R., Schneider, L. R., Nadim, F., & Harris-Warrick, R. M. (2005). Dopamine modulation of phasing of activity in a rhythmic motor network: contribution of synaptic and intrinsic modulatory actions. Journal of Neurophysiology, 94(5), 3101–3111.PubMedCrossRefGoogle Scholar
  27. Kreitzer, A. C., & Regehr, W. G. (2000). Modulation of transmission during trains at a cerebellar synapse. Journal of Neuroscience, 20(4), 1348–1357.PubMedGoogle Scholar
  28. Lagarias, J. C., Reeds, J. A., Wright, M. H., & Wright, P. E. (1998). Convergence properties of the Nelder-Mead simplex method in low dimensions. SIAM Journal on Optimization, 9(1), 112–147.CrossRefGoogle Scholar
  29. MacLeod, K. M., Horiuchi, T. K., & Carr, C. E. (2007). A role for short-term synaptic facilitation and depression in the processing of intensity information in the auditory brain stem. Journal of Neurophysiology, 97(4), 2863–2874.PubMedCrossRefGoogle Scholar
  30. Mamiya, A., Manor, Y., & Nadim, F. (2003). Short-term dynamics of a mixed chemical and electrical synapse in a rhythmic network. Journal of Neuroscience, 23(29), 9557–9564.PubMedGoogle Scholar
  31. Mamiya, A., & Nadim, F. (2005). Target-specific short-term dynamics are important for the function of synapses in an oscillatory neural network. Journal of Neurophysiology, 94(4), 2590–2602.PubMedCrossRefGoogle Scholar
  32. Manor, Y., Bose, A., Booth, V., & Nadim, F. (2003). Contribution of synaptic depression to phase maintenance in a model rhythmic network. Journal of Neurophysiology, 90(5), 3513–3528.PubMedCrossRefGoogle Scholar
  33. Manor, Y., Nadim, F., Abbott, L. F., & Marder, E. (1997). Temporal dynamics of graded synaptic transmission in the lobster stomatogastric ganglion. Journal of Neuroscience, 17(14), 5610–5621.PubMedGoogle Scholar
  34. Marder, E., & Bucher, D. (2007). Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annual Review of Physiology, 69, 291–316.PubMedCrossRefGoogle Scholar
  35. Markram, H., & Tsodyks, M. (1996). Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature, 382(6594), 807–810.PubMedCrossRefGoogle Scholar
  36. Matveev, V., Bertram, R., & Sherman, A. (2006). Residual bound Ca2+ can account for the effects of Ca2+ buffers on synaptic facilitation. Journal of Neurophysiology, 96, 3389–3397.PubMedCrossRefGoogle Scholar
  37. Nadim, F., Booth, V., Bose, A., & Manor, Y. (2003). Short-term synaptic dynamics promote phase maintenance in multi-phasic rhythms. Neurocomputing, 52–4, 79–87.CrossRefGoogle Scholar
  38. Olcese, R. (2007). And yet it moves: conformational States of the Ca2+ channel pore. Journal of General Physiology, 129(6), 457–459.PubMedCrossRefGoogle Scholar
  39. Pan, B., & Zucker, R. S. (2009). A general model of synaptic transmission and short-term plasticity. Neuron, 62(4), 539–554.PubMedCrossRefGoogle Scholar
  40. Reyes, A., Lujan, R., Rozov, A., Burnashev, N., Somogyi, P., & Sakmann, B. (1998). Target-cell-specific facilitation and depression in neocortical circuits. Nature Neuroscience, 1(4), 279–285.PubMedCrossRefGoogle Scholar
  41. Rose, G., & Fortune, E. (1999). Frequency-dependent PSP depression contributes to low-pass temporal filtering in Eigenmannia. Journal of Neuroscience, 19(17), 7629–7639.PubMedGoogle Scholar
  42. Schneggenburger, R., & Neher, E. (2005). Presynaptic calcium and control of vesicle fusion. Current Opinion in Neurobiology, 15(3), 266–274.PubMedCrossRefGoogle Scholar
  43. Stout, A. K., Li-Smerin, Y., Johnson, J. W., & Reynolds, I. J. (1996). Mechanisms of glutamate-stimulated Mg2+ influx and subsequent Mg2+ efflux in rat forebrain neurones in culture. The Journal of Physiology, 492(Pt 3), 641–657.PubMedGoogle Scholar
  44. Swensen, A. M., & Marder, E. (2000). Multiple peptides converge to activate the same voltage-dependent current in a central pattern-generating circuit. Journal of Neuroscience, 20(18), 6752–6759.PubMedGoogle Scholar
  45. Swensen, A. M., & Marder, E. (2001). Modulators with convergent cellular actions elicit distinct circuit outputs. Journal of Neuroscience, 21(11), 4050–4058.PubMedGoogle Scholar
  46. Thies, R. E. (1965). Neuromuscular depression and the apparent depletion of transmitter in mammalian muscle. Journal of Neurophysiology, 28, 428–442.PubMedGoogle Scholar
  47. Thirumalai, V., Prinz, A. A., Johnson, C. D., & Marder, E. (2006). Red pigment concentrating hormone strongly enhances the strength of the feedback to the pyloric rhythm oscillator but has little effect on pyloric rhythm period. Journal of Neurophysiology, 95(3), 1762–1770.PubMedCrossRefGoogle Scholar
  48. Tsodyks, M., Pawelzik, K., & Markram, H. (1998). Neural networks with dynamic synapses. Neural Computation, 10(4), 821–835.PubMedCrossRefGoogle Scholar
  49. Tsodyks, M. V., & Markram, H. (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proceedings of the National Academy of Sciences of the United States of America, 94(2), 719–723.PubMedCrossRefGoogle Scholar
  50. Tsujimoto, T., Jeromin, A., Saitoh, N., Roder, J. C., & Takahashi, T. (2002). Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science, 295(5563), 2276–2279.PubMedCrossRefGoogle Scholar
  51. Verhoog, M. B., & Mansvelder, H. D. (2011). Presynaptic ionotropic receptors controlling and modulating the rules for spike timing-dependent plasticity. Neural Plasticity, 2011, 870763.PubMedCrossRefGoogle Scholar
  52. von Gersdorff, H., Schneggenburger, R., Weis, S., & Neher, E. (1997). Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors. Journal of Neuroscience, 17(21), 8137–8146.Google Scholar
  53. Wang, S. J., Wang, K. Y., Wang, W. C., & Sihra, T. S. (2006). Unexpected inhibitory regulation of glutamate release from rat cerebrocortical nerve terminals by presynaptic 5-hydroxytryptamine-2A receptors. Journal of Neuroscience Research, 84(7), 1528–1542.PubMedCrossRefGoogle Scholar
  54. Wu, L. G., & Betz, W. J. (1998). Kinetics of synaptic depression and vesicle recycling after tetanic stimulation of frog motor nerve terminals. Biophysical Journal, 74(6), 3003–3009.PubMedCrossRefGoogle Scholar
  55. Wu, L. G., & Saggau, P. (1997). Presynaptic inhibition of elicited neurotransmitter release. Trends in Neurosciences, 20(5), 204–212.PubMedCrossRefGoogle Scholar
  56. Xu, J., He, L., & Wu, L. G. (2007). Role of Ca(2+) channels in short-term synaptic plasticity. Current Opinion in Neurobiology, 17(3), 352–359.PubMedCrossRefGoogle Scholar
  57. Xu, J., & Wu, L. G. (2005). The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron, 46(4), 633–645.PubMedCrossRefGoogle Scholar
  58. Yue, D. T., Backx, P. H., & Imredy, J. P. (1990). Calcium-sensitive inactivation in the gating of single calcium channels. Science, 250(4988), 1735–1738.PubMedCrossRefGoogle Scholar
  59. Zhao, S., Sheibanie, A. F., Oh, M., Rabbah, P., & Nadim, F. (2011). Peptide neuromodulation of synaptic dynamics in an oscillatory network. Journal of Neuroscience, 31(39), 13991–14004.PubMedCrossRefGoogle Scholar
  60. Zhou, L., Zhao, S., & Nadim, F. (2007). Neuromodulation of short-term synaptic dynamics examined in a mechanistic model based on kinetics of calcium currents. Neurocomputing, 70(10–12), 2050–2054.PubMedCrossRefGoogle Scholar
  61. Zucker, R. S., & Regehr, W. G. (2002). Short-term synaptic plasticity. Annual Review of Physiology, 64, 355–405.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Myongkeun Oh
    • 1
  • Shunbing Zhao
    • 2
  • Victor Matveev
    • 1
  • Farzan Nadim
    • 1
    • 2
    Email author
  1. 1.Department of Mathematical SciencesNew Jersey Institute of TechnologyNewarkUSA
  2. 2.Department of Biological SciencesRutgers UniversityNewarkUSA

Personalised recommendations