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. 2000 Aug;79(2):629–637. doi: 10.1016/S0006-3495(00)76321-1

Influence of temporal correlation of synaptic input on the rate and variability of firing in neurons.

G Svirskis 1, J Rinzel 1
PMCID: PMC1300963  PMID: 10919997

Abstract

The spike trains that transmit information between neurons are stochastic. We used the theory of random point processes and simulation methods to investigate the influence of temporal correlation of synaptic input current on firing statistics. The theory accounts for two sources for temporal correlation: synchrony between spikes in presynaptic input trains and the unitary synaptic current time course. Simulations show that slow temporal correlation of synaptic input leads to high variability in firing. In a leaky integrate-and-fire neuron model with spike afterhyperpolarization the theory accurately predicts the firing rate when the spike threshold is higher than two standard deviations of the membrane potential fluctuations. For lower thresholds the spike afterhyperpolarization reduces the firing rate below the theory's predicted level when the synaptic correlation decays rapidly. If the synaptic correlation decays slower than the spike afterhyperpolarization, spike bursts can occur during single broad peaks of input fluctuations, increasing the firing rate over the prediction. Spike bursts lead to a coefficient of variation for the interspike intervals that can exceed one, suggesting an explanation of high coefficient of variation for interspike intervals observed in vivo.

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Selected References

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  1. Abeles M., Prut Y. Spatio-temporal firing patterns in the frontal cortex of behaving monkeys. J Physiol Paris. 1996;90(3-4):249–250. doi: 10.1016/s0928-4257(97)81433-7. [DOI] [PubMed] [Google Scholar]
  2. Aertsen A. M., Gerstein G. L., Habib M. K., Palm G. Dynamics of neuronal firing correlation: modulation of "effective connectivity". J Neurophysiol. 1989 May;61(5):900–917. doi: 10.1152/jn.1989.61.5.900. [DOI] [PubMed] [Google Scholar]
  3. Allen C., Stevens C. F. An evaluation of causes for unreliability of synaptic transmission. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10380–10383. doi: 10.1073/pnas.91.22.10380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Azouz R., Gray C. M. Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci. 1999 Mar 15;19(6):2209–2223. doi: 10.1523/JNEUROSCI.19-06-02209.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bair W., Koch C. Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput. 1996 Aug 15;8(6):1185–1202. doi: 10.1162/neco.1996.8.6.1185. [DOI] [PubMed] [Google Scholar]
  6. Binder M. D., Robinson F. R., Powers R. K. Distribution of effective synaptic currents in cat triceps surae motoneurons. VI. Contralateral pyramidal tract. J Neurophysiol. 1998 Jul;80(1):241–248. doi: 10.1152/jn.1998.80.1.241. [DOI] [PubMed] [Google Scholar]
  7. Brivanlou I. H., Warland D. K., Meister M. Mechanisms of concerted firing among retinal ganglion cells. Neuron. 1998 Mar;20(3):527–539. doi: 10.1016/s0896-6273(00)80992-7. [DOI] [PubMed] [Google Scholar]
  8. Burkitt A. N., Clark G. M. Analysis of integrate-and-fire neurons: synchronization of synaptic input and spike output. Neural Comput. 1999 May 15;11(4):871–901. doi: 10.1162/089976699300016485. [DOI] [PubMed] [Google Scholar]
  9. Calvin W. H., Stevens C. F. Synaptic noise and other sources of randomness in motoneuron interspike intervals. J Neurophysiol. 1968 Jul;31(4):574–587. doi: 10.1152/jn.1968.31.4.574. [DOI] [PubMed] [Google Scholar]
  10. Destexhe A., Paré D. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol. 1999 Apr;81(4):1531–1547. doi: 10.1152/jn.1999.81.4.1531. [DOI] [PubMed] [Google Scholar]
  11. Ferster D. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J Neurosci. 1986 May;6(5):1284–1301. doi: 10.1523/JNEUROSCI.06-05-01284.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. GERSTEIN G. L., MANDELBROT B. RANDOM WALK MODELS FOR THE SPIKE ACTIVITY OF A SINGLE NEURON. Biophys J. 1964 Jan;4:41–68. doi: 10.1016/s0006-3495(64)86768-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gibson J. R., Beierlein M., Connors B. W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature. 1999 Nov 4;402(6757):75–79. doi: 10.1038/47035. [DOI] [PubMed] [Google Scholar]
  14. Gluss B. A model for neuron firing with exponential decay of potential resulting in diffusion equations for probability density. Bull Math Biophys. 1967 Jun;29(2):233–243. doi: 10.1007/BF02476897. [DOI] [PubMed] [Google Scholar]
  15. Gray C. M., König P., Engel A. K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature. 1989 Mar 23;338(6213):334–337. doi: 10.1038/338334a0. [DOI] [PubMed] [Google Scholar]
  16. Hardingham N. R., Larkman A. U. Rapid report: the reliability of excitatory synaptic transmission in slices of rat visual cortex in vitro is temperature dependent. J Physiol. 1998 Feb 15;507(Pt 1):249–256. doi: 10.1111/j.1469-7793.1998.249bu.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lampl I., Reichova I., Ferster D. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron. 1999 Feb;22(2):361–374. doi: 10.1016/s0896-6273(00)81096-x. [DOI] [PubMed] [Google Scholar]
  18. Lester R. A., Clements J. D., Westbrook G. L., Jahr C. E. Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature. 1990 Aug 9;346(6284):565–567. doi: 10.1038/346565a0. [DOI] [PubMed] [Google Scholar]
  19. Mann-Metzer P., Yarom Y. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J Neurosci. 1999 May 1;19(9):3298–3306. doi: 10.1523/JNEUROSCI.19-09-03298.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Matsui K., Hosoi N., Tachibana M. Excitatory synaptic transmission in the inner retina: paired recordings of bipolar cells and neurons of the ganglion cell layer. J Neurosci. 1998 Jun 15;18(12):4500–4510. doi: 10.1523/JNEUROSCI.18-12-04500.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Paré D., Shink E., Gaudreau H., Destexhe A., Lang E. J. Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons In vivo. J Neurophysiol. 1998 Mar;79(3):1450–1460. doi: 10.1152/jn.1998.79.3.1450. [DOI] [PubMed] [Google Scholar]
  22. Raman I. M., Trussell L. O. The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron. 1992 Jul;9(1):173–186. doi: 10.1016/0896-6273(92)90232-3. [DOI] [PubMed] [Google Scholar]
  23. Reich D. S., Victor J. D., Knight B. W. The power ratio and the interval map: spiking models and extracellular recordings. J Neurosci. 1998 Dec 1;18(23):10090–10104. doi: 10.1523/JNEUROSCI.18-23-10090.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Riehle A., Grün S., Diesmann M., Aertsen A. Spike synchronization and rate modulation differentially involved in motor cortical function. Science. 1997 Dec 12;278(5345):1950–1953. doi: 10.1126/science.278.5345.1950. [DOI] [PubMed] [Google Scholar]
  25. Roelfsema P. R., Engel A. K., König P., Singer W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature. 1997 Jan 9;385(6612):157–161. doi: 10.1038/385157a0. [DOI] [PubMed] [Google Scholar]
  26. STEIN R. B. A THEORETICAL ANALYSIS OF NEURONAL VARIABILITY. Biophys J. 1965 Mar;5:173–194. doi: 10.1016/s0006-3495(65)86709-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shadlen M. N., Newsome W. T. Noise, neural codes and cortical organization. Curr Opin Neurobiol. 1994 Aug;4(4):569–579. doi: 10.1016/0959-4388(94)90059-0. [DOI] [PubMed] [Google Scholar]
  28. Shadlen M. N., Newsome W. T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci. 1998 May 15;18(10):3870–3896. doi: 10.1523/JNEUROSCI.18-10-03870.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Silver R. A., Traynelis S. F., Cull-Candy S. G. Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ. Nature. 1992 Jan 9;355(6356):163–166. doi: 10.1038/355163a0. [DOI] [PubMed] [Google Scholar]
  30. Softky W. R., Koch C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci. 1993 Jan;13(1):334–350. doi: 10.1523/JNEUROSCI.13-01-00334.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Steinmetz P. N., Roy A., Fitzgerald P. J., Hsiao S. S., Johnson K. O., Niebur E. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature. 2000 Mar 9;404(6774):187–190. doi: 10.1038/35004588. [DOI] [PubMed] [Google Scholar]
  32. Stern E. A., Kincaid A. E., Wilson C. J. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol. 1997 Apr;77(4):1697–1715. doi: 10.1152/jn.1997.77.4.1697. [DOI] [PubMed] [Google Scholar]
  33. Treves A., Panzeri S., Rolls E. T., Booth M., Wakeman E. A. Firing rate distributions and efficiency of information transmission of inferior temporal cortex neurons to natural visual stimuli. Neural Comput. 1999 Apr 1;11(3):601–632. doi: 10.1162/089976699300016593. [DOI] [PubMed] [Google Scholar]
  34. Vaadia E., Haalman I., Abeles M., Bergman H., Prut Y., Slovin H., Aertsen A. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature. 1995 Feb 9;373(6514):515–518. doi: 10.1038/373515a0. [DOI] [PubMed] [Google Scholar]
  35. Victor J. D., Purpura K. P. Spatial phase and the temporal structure of the response to gratings in V1. J Neurophysiol. 1998 Aug;80(2):554–571. doi: 10.1152/jn.1998.80.2.554. [DOI] [PubMed] [Google Scholar]
  36. Wahl L. M., Jack J. J., Larkman A. U., Stratford K. J. The effects of synaptic noise on measurements of evoked excitatory postsynaptic response amplitudes. Biophys J. 1997 Jul;73(1):205–219. doi: 10.1016/S0006-3495(97)78061-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weliky M., Katz L. C. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science. 1999 Jul 23;285(5427):599–604. doi: 10.1126/science.285.5427.599. [DOI] [PubMed] [Google Scholar]
  38. Wilbur W. J., Rinzel J. A theoretical basis for large coefficient of variation and bimodality in neuronal interspike interval distributions. J Theor Biol. 1983 Nov 21;105(2):345–368. doi: 10.1016/s0022-5193(83)80013-7. [DOI] [PubMed] [Google Scholar]

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