Annals of Biomedical Engineering

, Volume 35, Issue 5, pp 847–857 | Cite as

Nonlinear Dynamic Model of CA1 Short-Term Plasticity using Random Impulse Train Stimulation

  • Ghassan GholmiehEmail author
  • Spiros Courellis
  • Vasilis Marmarelis
  • Theodore Berger


A comprehensive, quantitative description of the nonlinear dynamic characteristics of the short-term plasticity (STP) in the CA1 hippocampal region is presented. It is based on the Volterra–Poisson modeling approach using random impulse train (RIT) stimuli. In vitro hippocampal slice preparations were used from adult rats. RIT stimuli were applied at the Schaffer collaterals and population spike responses were recorded at the CA1 cell body layer. The computed STP descriptors that capture the nonlinear dynamics of the underlying STP mechanisms were the Volterra–Poisson kernels. The kernels quantified the presence of facilitatory and inhibitory STP behavior in magnitude and duration. A third order Volterra–Poisson STP model was introduced that accurately predicted in-sample and out-of-sample system responses. The proposed model could also accurately predict impulse pair and short impulse train system responses.


CA1 Multielectrode array Nonlinear analysis Paired pulse Random impulse train Short-term plasticity Kernels 



This work was supported by Grant No. RR-01861 from the Division of Research Resources of the National Institutes of Health and by Grants 0646 and 0259 from DARPA Controlled Biological Systems Program and the Office of Naval Research.


  1. 1.
    Abbott L. F., J. A. Varela, K. Sen, S. B. Nelson (1997) Synaptic depression and cortical gain control. Science 275:220–224PubMedCrossRefGoogle Scholar
  2. 2.
    Berger T. W., J. L. Eriksson, D. A. Ciarolla, R. J Sclabassi (1988) Nonlinear systems analysis of the hippocampal Perforant Path-Dentate projection. II Effects of random train stimulation. J. Neurophysiol. 60:1077–1094Google Scholar
  3. 3.
    Berger T. W., J. L. Eriksson, D. A. Ciarolla, R. J. Sclabassi (1988) Nonlinear systems analysis of the hippocampal Perforant Path-Dentate projection. III Comparison of random train and paired impulse stimulation. J. Neurophysiol. 60:1095–1109PubMedGoogle Scholar
  4. 4.
    Buonomano D. V. (1999) Distinct functional types of associative Long-Term Potentiation in the neocortical and hippocampal pyramidal neurons. J. Neurosci. 19(16):6748–6754PubMedGoogle Scholar
  5. 5.
    Buonomano D. V. (2000) Decoding temporal information: A model based on short-term synaptic plasticity. J. Neurosci. 20(3):1129–1141PubMedGoogle Scholar
  6. 6.
    Castellucci V. F., E. R. Kandel (1974) A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc. Natl. Acad. Sci. USA 71(12):5004–5008PubMedCrossRefGoogle Scholar
  7. 7.
    Castro-Alamancos M. A., B. W. Connors (1997) Distinct forms of short-term plasticity at excitatory synapses of hippocampus and neocortex. Proc. Natl. Acad. Sci. USA 94:4161–4166PubMedCrossRefGoogle Scholar
  8. 8.
    Creager R., T. Dunwiddie, G. Lynch (1980) Paired-pulse and frequency facilitation in the CA1 region of the in vitro rat hippocampus. J. Neurophysiol. 299:409–424Google Scholar
  9. 9.
    Courellis, S. H., V. Z. Marmarelis, and T. W. Berger. Modeling event-driven nonlinear dynamics in neuronal systems with multiple inputs. Annual Conference Biomedical Engineering Society, Seattle, WA, 2000Google Scholar
  10. 10.
    Dobrunz L. E., C. F. Stevens (1999) Response of hippocampal synapses to natural stimulation patterns. Neuron 22(1):157–166PubMedCrossRefGoogle Scholar
  11. 11.
    Ferster D., N. Spruston (1995) Cracking the neuronal code. Science 270:756–757PubMedCrossRefGoogle Scholar
  12. 12.
    Fortune E. S., G. R. Rose (2000) Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information .J. Neurosci. 20(18):7122–7130PubMedGoogle Scholar
  13. 13.
    Fuhrmann G., I. Segev, H. Markram, M. Tsodyks (2002) Coding of temporal information by activity-dependent synapses. J. Neurophys. 87:140–148Google Scholar
  14. 14.
    Gerstner W., A. Kreiter, H. Markram, A. Herz (1997) Neural codes: Firing rate and beyond. Proc. Natl. Acad. Sci. USA 94:12740–12741PubMedCrossRefGoogle Scholar
  15. 15.
    Gholmieh G., S. H. Courellis, V. Z. Marmarelis, T. W. Berger (2002) An efficient method for modelling short term plasticity using random impulse stimuli. J. Neurosci. Methods 21(2):111–127CrossRefGoogle Scholar
  16. 16.
    Gholmieh G., S. H. Courellis, V. Z. Marmarelis, T. W. Berger, M. Baudry (2001) A biosensor for detecting changes in cognitive processing based on nonlinear systems analysis. Bios. Bioelec. 16(7–8):491–501CrossRefGoogle Scholar
  17. 17.
    Gross G. W., B. K. Rhoadas, D. L. Reust, F. U. Schwalm (1993) Stimulation of monolayer networks in culture through thin film indium-tin oxide recording electrodes. J. Neurosci. Methods 50:131–143PubMedCrossRefGoogle Scholar
  18. 18.
    Konig P., A. K. Engel, W. Singer (1996) Integrator or coincidence detector? the role of the cortical neuron revisited. Trends Neurosci 19:130–137PubMedCrossRefGoogle Scholar
  19. 19.
    Leung L. S., X. W. Fu (1994) Factors affecting paired-pulse facilitation in the hippocampal CA1 neurons in vitro. Brain Res. 650:75–84PubMedCrossRefGoogle Scholar
  20. 20.
    Markram H., M. Tsodyks (1996) Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382:807–810PubMedCrossRefGoogle Scholar
  21. 21.
    Marmarelis V. Z. (2004) Nonlinear Dynamic Modeling of Physiological Systems. Wiley, New York, NYGoogle Scholar
  22. 22.
    Marmarelis V. Z., T. W. Berger (2005) General methodology for nonlinear modeling of neural systems with Poisson point-process inputs. Math. Biosci. 196:1–13PubMedCrossRefGoogle Scholar
  23. 23.
    Michelson H. B., Kapur J., E. W. Lothman (1989) Reduction of paired pulse inhibition in the CA1 region of the hippocampus by pilocarpine in naive and in amygdala-kindled rats. Exp. Neurol. 104(3):264–271PubMedCrossRefGoogle Scholar
  24. 24.
    O’Donovan M. J., J. Rinzel (1997) Synaptic depression: A dynamic regulator of synaptic communication with varied functional roles. Trends Neurosci. 20:431–432PubMedCrossRefGoogle Scholar
  25. 25.
    Pananceau M, H. Chen, B. Gustafsson (1998) Short-term facilitation evoked during brief afferent tetani is not altered by long-term potentiation in the guinea-pig hippocampal CA1 region. J. Physiol. 508(2):503–514PubMedCrossRefGoogle Scholar
  26. 26.
    Papatheodoropoulos C., G. Kostopoulos (2000) Dorsal-ventral differentiation of short-term synaptic plasticity in rat CA1 hippocampal region. Neurosci. Lett. 286(1):57–60PubMedCrossRefGoogle Scholar
  27. 27.
    Richmond B. J., L. M. Optican (1990) Temporal encoding of two-dimensional patterns by single units in primate visual cortex. II. Information transmission. J. Neurophysiol. 64:370–380PubMedGoogle Scholar
  28. 28.
    Rieke, F., D. Waarland, R. R. De Ruyter Van Steveninck, and W. Bialek. Spikes: Exploring the Neural Code. MIT Press, Cambridge, MA, 1997Google Scholar
  29. 29.
    Senn W., I. Segev, M. Tsodyks (1998) Reading neuronal synchrony with depressing synapses. Neural Comput. 10:815–819PubMedCrossRefGoogle Scholar
  30. 30.
    Sclabassi R. J., J. L. Eriksson, R. Port, G. Robinson, T. W. Berger (1988) Nonlinear systems analysis of the hippocampal Perforant Path-Dentate Projection I. Theoretical and interpretational considerations. J. Neurophysiol. 60:1066–1076PubMedGoogle Scholar
  31. 31.
    Stringer J. L., E. W. Lothman (1988) In vitro effects of extracellular calcium concentrations on hippocampal pyramidal cell responses. Exp. Neurol. 101(1):132–146PubMedCrossRefGoogle Scholar
  32. 32.
    Tsodyks M. V., H. Markram (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl. Acad. Sci. USA 94:719–723PubMedCrossRefGoogle Scholar
  33. 33.
    Valentin A., J. J. Garcia-Seoane, A. Colino (1997) Lithium enhances synaptic transmission in neonatal rat hippocampus. Neuroscience 78(2):385–391PubMedCrossRefGoogle Scholar
  34. 34.
    Varela J. A., K. Sen., J. Gibson, J. Fost, L. F. Abbot, S. B. Nelson (1997) A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of the visual cortex. J. Neurosci. 17:7926–7940PubMedGoogle Scholar
  35. 35.
    Westwick D. T., B. Suki, K. R. Lutchen (1998) Sensitivity analysisof kernel estimates: Implications in nonlinear physiological systemidentification. Ann. Biomed. Eng. 26(3):488–501PubMedCrossRefGoogle Scholar
  36. 36.
    Zucker R. S. (1998) Short-term synaptic plasticity. Ann. Rev. Neurosci. 12:13–31CrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2007

Authors and Affiliations

  • Ghassan Gholmieh
    • 1
    Email author
  • Spiros Courellis
    • 2
  • Vasilis Marmarelis
    • 2
  • Theodore Berger
    • 2
    • 3
  1. 1.Division of NeurologyChildrens Hospital Los AngelesLos AngelesUSA
  2. 2.Department of Biomedical EngineeringUSCLos AngelesUSA
  3. 3.Neuroscience ProgramUSCLos AngelesUSA

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