Reliability and Precision Are Optimal for Non-Uniform Distributions of Presynaptic Release Probability

Abstract

Most conceptual and computational models assume that synaptic transmission is reliable, a simplification rarely substantiated by data. The functional consequences of the recruitment of high and low initial release probability synapses on the reliability and precision of their postsynaptic targets are studied in a multi-compartmental model of a hippocampal CA1 pyramidal cell. We show that changes in the firing rate of CA3 afferent inputs (rate remapping) are not reflected in the firing rate of the CA1 cell but in the reliability and precise timing of some of its action potentials, suggesting that a signature of remapping may be found in the precise spike timing of CA1. Our results suggest that about half of the action potentials produced by a CA1 cell can potentially carry reliable information in their precise timing with about 25 ms precision, a time scale on the order of the gamma cycle. We show further that reliable events were primarily elicited by CA3 synapses in a state of low probability of release. Overall, our results suggest that the non-uniform distribution of initial release probabilities observed experimentally achieves an optimum yielding simultaneously high precision and high reliability, and allows large populations of CA3 synapses to contribute to the production of reliable CA1 spiking events.

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Fellous, J. and Corral-Frías, N. (2015) Reliability and Precision Are Optimal for Non-Uniform Distributions of Presynaptic Release Probability. Journal of Biomedical Science and Engineering, 8, 170-183. doi: 10.4236/jbise.2015.83017.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Bi, G.Q. and Poo, M.M. (1998) Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type. Journal of Neuroscience, 18, 10464-10472.
[2] Campanac, E. and Debanne, D. (2008) Spike Timing-Dependent Plasticity: A Learning Rule for Dendritic Integration in Rat CA1 Pyramidal Neurons. The Journal of Physiology, 586, 779-793.
http://dx.doi.org/10.1113/jphysiol.2007.147017
[3] Mainen, Z.F. and Sejnowski, T.J. (1995) Reliability of Spike Timing in Neocortical Neurons. Science, 268, 1503-1506.
http://dx.doi.org/10.1126/science.7770778
[4] Fellous, J.M., Houweling, A.R., Modi, R.H., Rao, R.P., Tiesinga, P.H., et al. (2001) Frequency Dependence of Spike Timing Reliability in Cortical Pyramidal Cells and Interneurons. Journal of Neurophysiology, 85, 1782-1787.
[5] Maurer, A.P. and McNaughton, B.L. (2007) Network and Intrinsic Cellular Mechanisms Underlying Theta Phase Precession of Hippocampal Neurons. Trends in Neurosciences, 30, 325-333.
http://dx.doi.org/10.1016/j.tins.2007.05.002
[6] Sutherland, G.R. and McNaughton, B. (2000) Memory Trace Reactivation in Hippocampal and Neocortical Neuronal Ensembles. Current Opinion in Neurobiology, 10, 180-186.
http://dx.doi.org/10.1016/S0959-4388(00)00079-9
[7] Lee, A.K. and Wilson, M.A. (2002) Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep. Neuron, 36, 1183-1194.
http://dx.doi.org/10.1016/S0896-6273(02)01096-6
[8] Wilson, M.A. and McNaughton, B.L. (1994) Reactivation of Hippocampal Ensemble Memories during Sleep. Science, 265, 676-679.
http://dx.doi.org/10.1126/science.8036517
[9] Wang, H.P., Spencer, D., Fellous, J.M. and Sejnowski, T.J. (2010) Synchrony of Thalamocortical Inputs Maximizes Cortical Reliability. Science, 328, 106-109.
http://dx.doi.org/10.1126/science.1183108
[10] Tiesinga, P., Fellous, J.M. and Sejnowski, T.J. (2008) Regulation of Spike Timing in Visual Cortical Circuits. Nature Reviews Neuroscience, 9, 97-107.
http://dx.doi.org/10.1038/nrn2315
[11] Rotman, Z. and Klyachko, V.A. (2013) Role of Synaptic Dynamics and Het-erogeneity in Neuronal Learning of Temporal Code. Journal of Neurophysiology, 110, 2275-2286.
http://dx.doi.org/10.1152/jn.00454.2013
[12] Kandaswamy, U., Deng, P.Y., Stevens, C.F. and Klyachko, V.A. (2010) The Role of Presynaptic Dynamics in Processing of Natural Spike Trains in Hippocampal Synapses. Journal of Neuroscience, 30, 15904-15914.
http://dx.doi.org/10.1523/JNEUROSCI.4050-10.2010
[13] Dobrunz, L.E. and Stevens, C.F. (1997) Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses. Neuron, 18, 995-1008.
http://dx.doi.org/10.1016/S0896-6273(00)80338-4
[14] Allen, C. and Stevens, C.F. (1994) An Evaluation of Causes for Unreliability of Synaptic Transmission. Proceedings of the National Academy of Sciences of the USA, 91, 10380-10383.
http://dx.doi.org/10.1073/pnas.91.22.10380
[15] Dobrunz, L.E., Huang, E.P. and Stevens, C.F. (1997) Very Short-Term Plasticity in Hippocampal Synapses. Proceedings of the National Academy of Sciences of the USA, 94, 14843-14847.
http://dx.doi.org/10.1073/pnas.94.26.14843
[16] Alabi, A.A. and Tsien, R.W. (2012) Synaptic Vesicle Pools and Dynamics. Cold Spring Harbor Perspectives in Biology, 4, Article ID: a013680.
http://dx.doi.org/10.1101/cshperspect.a013680
[17] Hines, M.L. and Carnevale, N.T. (1997) The NEURON Simulation Environment. Neural Computation, 9, 1179-1209.
http://dx.doi.org/10.1162/neco.1997.9.6.1179
[18] Major, G., Larkman, A.U., Jonas, P., Sakmann, B. and Jack, J.J. (1994) Detailed Passive Cable Models of Whole-Cell Recorded CA3 Pyramidal Neurons in Rat Hippocampal Slices. Journal of Neuroscience, 14, 4613-4638.
[19] Stuart, G., Spruston, N. and Hausser, M. (1999) Dendrites. Oxford University Press, Oxford, 376 p.
[20] Cash, S. and Yuste, R. (1999) Linear Summation of Excitatory Inputs by CA1 Pyramidal Neurons. Neuron, 22, 383-394.
http://dx.doi.org/10.1016/S0896-6273(00)81098-3
[21] Volman, V., Levine, H., Ben-Jacob, E. and Sejnowski, T.J. (2009) Locally Balanced Dendritic Integration by Short-Term Synaptic Plasticity and Active Dendritic Conductances. Journal of Neurophysiology, 102, 3234-3250.
http://dx.doi.org/10.1152/jn.00260.2009
[22] Huang, E.P. and Stevens, C.F. (1997) Estimating the Distribution of Synaptic Reliabilities. Journal of Neurophysiology, 78, 2870-2880.
[23] Zucker, R.S. and Regehr, W.G. (2002) Short-Term Synaptic Plasticity. Annual Review of Physiology, 64, 355-405.
http://dx.doi.org/10.1146/annurev.physiol.64.092501.114547
[24] Maass, W. and Zador, A.M. (1999) Dynamic Stochastic Synapses as Computational Units. Neural Computation, 11, 903-917.
http://dx.doi.org/10.1162/089976699300016494
[25] Matveev, V. and Wang, X.J. (2000) Differential Short-Term Synaptic Plasticity and Transmission of Complex Spike Trains: To Depress or to Facilitate? Cerebral Cortex, 10, 1143-1153.
http://dx.doi.org/10.1093/cercor/10.11.1143
[26] Hanse, E. and Gustafsson, B. (2001) Quantal Variability at Glutamatergic Synapses in Area CA1 of the Rat Neonatal Hippocampus. Journal of Physiology, 531, 467-480.
http://dx.doi.org/10.1111/j.1469-7793.2001.0467i.x
[27] Chen, G., Harata, N.C. and Tsien, R.W. (2004) Paired-Pulse Depression of Unitary Quantal Amplitude at Single Hippocampal Synapses. Proceedings of the National Academy of Sciences of the USA, 101, 1063-1068.
http://dx.doi.org/10.1073/pnas.0307149101
[28] Hanse, E. and Gustafsson, B. (2001) Factors Explaining Heterogeneity in Short-Term Synaptic Dynamics of Hippocampal Glutamatergic Synapses in the Neonatal Rat. Journal of Physiology, 537, 141-149.
http://dx.doi.org/10.1111/j.1469-7793.2001.0141k.x
[29] Dittman, J.S., Kreitzer, A.C. and Regehr, W.G. (2000) Interplay between Facilitation, Depression, and Residual Calcium at Three Presynaptic Terminals. Journal of Neuroscience, 20, 1374-1385.
[30] Sun, H.Y., Lyons, S.A. and Dobrunz, L.E. (2005) Mechanisms of Target-Cell Specific Short-Term Plasticity at Schaffer Collateral Synapses onto Interneurones versus Pyramidal Cells in Juvenile Rats. Journal of Physiology, 568, 815-840.
http://dx.doi.org/10.1113/jphysiol.2005.093948
[31] Matveev, V. and Wang, X.J. (2000) Implications of All-or-None Synaptic Transmission and Short-Term Depression beyond Vesicle Depletion: A Computational Study. Journal of Neuroscience, 20, 1575-1588.
[32] Dobrunz, L.E. and Stevens, C.F. (1999) Response of Hippocampal Synapses to Natural Stimulation Patterns. Neuron, 22, 157-166.
http://dx.doi.org/10.1016/S0896-6273(00)80687-X
[33] Klyachko, V.A. and Stevens, C.F. (2006) Temperature-Dependent Shift of Balance among the Components of Short-Term Plasticity in Hippocampal Synapses. Journal of Neuroscience, 26, 6945-6957.
http://dx.doi.org/10.1523/JNEUROSCI.1382-06.2006
[34] Markram, H., Wang, Y. and Tsodyks, M. (1998) Differential Signaling via the Same Axon of Neocortical Pyramidal Neurons. Proceedings of the National Academy of Sciences of the USA, 95, 5323-5328.
http://dx.doi.org/10.1073/pnas.95.9.5323
[35] Gandhi, S.P. and Stevens, C.F. (2003) Three Modes of Synaptic Vesicular Recycling Revealed by Single-Vesicle Imaging. Nature, 423, 607-613.
http://dx.doi.org/10.1038/nature01677
[36] Murthy, V.N., Sejnowski, T.J. and Stevens, C.F. (1997) Heterogeneous Release Properties of Visualized Individual Hippocampal Synapses. Neuron, 18, 599-612.
http://dx.doi.org/10.1016/S0896-6273(00)80301-3
[37] Destexhe, A., Mainen, Z.F. and Sejnowski, T.J. (1996) Kinetic Models of Synaptic Transmission. In: Koch, C., Segev, I., Eds., Methods in Neuronal Modeling, MIT Press, Cambridge.
[38] Wilson, M.A. and McNaughton, B.L. (1993) Dynamics of the Hippocampal Ensemble Code for Space. Science, 261, 1055-1058.
http://dx.doi.org/10.1126/science.8351520
[39] Destexhe, A., Rudolph, M., Fellous, J.M. and Sejnowski, T.J. (2001) Fluctuating Synaptic Conductances Recreate in Vivo-Like Activity in Neocortical Neurons. Neuroscience, 107, 13-24.
http://dx.doi.org/10.1016/S0306-4522(01)00344-X
[40] Fellous, J.M., Rudolph, M., Destexhe, A. and Sejnowski, T.J. (2003) Synaptic Background Noise Controls the Input/Output Characteristics of Single Cells in an in Vitro Model of in Vivo Activity. Neuroscience, 122, 811-829.
http://dx.doi.org/10.1016/j.neuroscience.2003.08.027
[41] Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.B. and Moser. E.I. (2004) Distinct Ensemble Codes in Hippocampal Areas CA3 and CA1. Science, 305, 1295-1298.
http://dx.doi.org/10.1126/science.1100265
[42] Colgin, L.L., Moser, E.I. and Moser, M.B. (2008) Understanding Memory through Hippocampal Remapping. Trends in Neurosciences, 31, 469-477.
http://dx.doi.org/10.1016/j.tins.2008.06.008
[43] Leutgeb, S., Leutgeb, J.K., Moser, E.I. and Moser, M.B. (2006) Fast Rate Coding in Hippocampal CA3 Cell Ensembles. Hippocampus, 16, 765-774.
http://dx.doi.org/10.1002/hipo.20201
[44] Fenton, A.A. and Muller, R.U. (1998) Place Cell Discharge Is Extremely Variable during Individual Passes of the Rat through the Firing Field. Proceedings of the National Academy of Sciences of the USA, 95, 3182-3187.
http://dx.doi.org/10.1073/pnas.95.6.3182
[45] Thomson, A.M. (2000) Molecular Frequency Filters at Central Synapses. Progress in Neurobiology, 62, 159-196.
http://dx.doi.org/10.1016/S0301-0082(00)00008-3
[46] Abbott, L.F., Varela, J.A., Sen, K. and Nelson, S.B. (1997) Synaptic Depression and Cortical Gain Control. Science, 275, 220-224.
http://dx.doi.org/10.1126/science.275.5297.221
[47] Rothman, J.S., Cathala, L., Steuber, V. and Silver, R.A. (2009) Synaptic Depression Enables Neuronal Gain Control. Nature, 457, 1015-1018.
http://dx.doi.org/10.1038/nature07604
[48] Manor, Y. and Nadim, F. (2001) Synaptic Depression Mediates Bistability in Neuronal Networks with Recurrent Inhibitory Connectivity. Journal of Neuroscience, 21, 9460-9470.
[49] Markram, H., Pikus, D., Gupta, A. and Tsodyks, M. (1998) Potential for Multiple Mechanisms, Phenomena and Algorithms for Synaptic Plasticity at Single Synapses. Neuropharmacology, 37, 489-500.
http://dx.doi.org/10.1016/S0028-3908(98)00049-5
[50] Goldman, M.S. (2004) Enhancement of Information Transmission Efficiency by Synaptic Failures. Neural Computation, 16, 1137-1162.
http://dx.doi.org/10.1162/089976604773717568
[51] Goldman, M.S., Maldonado, P. and Abbott, L.F. (2002) Redundancy Reduction and Sustained Firing with Stochastic Depressing Synapses. Journal of Neuroscience, 22, 584-591.

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