Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro

Abstract

The precise role of synchronous neuronal firing in signal encoding remains unclear. To examine what kinds of signals can be carried by synchrony, I reproduced a multilayer feedforward network of neurons in an in vitro slice preparation of rat cortex using an iterative procedure. When constant and time-varying frequency signals were delivered to the network, the firing of neurons in successive layers became progressively more synchronous. Notably, synchrony in the in vitro network developed even with uncorrelated input, persisted under a wide range of physiological conditions and was crucial for the stable propagation of rate signals. The firing rate was represented by a classical rate code in the initial layers, but switched to a synchrony-based code in the deeper layers.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Constructing feedforward networks in vitro.
Figure 2: Development of synchrony.
Figure 3: Synchrony with Poisson input.
Figure 4: Synchrony in networks with excitatory and inhibitory neurons.
Figure 5: Synchrony in heterogeneous networks.
Figure 6: Representation and propagation of frequency signals.
Figure 7: Synchrony with sinusoidally modulated inputs.

Similar content being viewed by others

References

  1. Abeles, M. Corticonics 208–258 (Cambridge Univ. Press, Cambridge, 1991).

    Google Scholar 

  2. Shadlen, M.N. & Newsome, W.T. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4, 569–579 (1994).

    Article  CAS  PubMed  Google Scholar 

  3. Ferster, D. & Spruston, N. Cracking the neuronal code. Science 270, 756–757 (1995).

    Article  CAS  PubMed  Google Scholar 

  4. Shadlen, M.N. & Newsome, W.T. The variable discharge of cortical neurons: implications for connectivity, computation and information coding. J. Neurosci. 18, 3870–3896 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Shadlen, M.N. & Movshon, J.A. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24, 67–77 (1999).

    Article  CAS  PubMed  Google Scholar 

  6. Meister, M. & Berry, M.J. The neural code of the retina. Neuron 22, 435–450 (1999).

    Article  CAS  PubMed  Google Scholar 

  7. Borst, A. & Theunissen, F.E. Information theory and neural coding. Nat. Neurosci. 2, 947–957 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. deCharms, R.C. & Zador, A. Neural representation and the cortical code. Annu. Rev. Neurosci. 23, 613–647 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Van Rullen, R. & Thorpe, S.J. Rate coding versus temporal order coding: what the retinal ganglion cells tell the visual cortex. Neural Comp. 13, 1255–1283 (2001).

    Article  CAS  Google Scholar 

  10. Riehle, A., Grun, S., Diesmann, M. & Aertsen, A. Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278, 1950–1953 (1997).

    Article  CAS  PubMed  Google Scholar 

  11. Prut, Y. et al. Spatiotemporal structure of cortical activity: properties and behavioral relevance. J. Neurophysiol. 79, 2857–2874 (1998).

    Article  CAS  PubMed  Google Scholar 

  12. Hatsopoulos, N.G., Ojakangas, C.L., Paninksi, L. & Donoghue, J.P. Information about movement direction obtained from synchronous activity of motor cortical neurons. Proc. Natl. Acad. Sci. USA 95, 15706–15711 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Murthy, V.N. & Fetz, E.E. Coherent 25–35 Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc. Natl. Acad. Sci. USA 89, 5670–5674 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Baker, S.N., Kilner, J.M., Pinches, E.M. & Lemon, R.N. The role of synchrony and oscillations in the motor output. Exp. Brain Res. 128, 109–117 (1999).

    Article  CAS  PubMed  Google Scholar 

  15. Conway, B.A. et al., Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J. Physiol. 489, 917–924 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Baker, S.N., Spinks, R., Jackson A. & Lemon, R.N. Synchronization in monkey motor cortex during a precision grip task. I. Task–dependent modulation in single–unit synchrony. J. Neurophysiol. 85, 869–885 (2001).

    Article  CAS  PubMed  Google Scholar 

  17. Feige, B., Aertsen, A. & Kristeva–Feige, R. Dynamic synchronization between multiple cortical motor areas and muscle activity in phasic voluntary movements. J. Neurophysiol. 84, 2622–2629 (2000).

    Article  CAS  PubMed  Google Scholar 

  18. Panzeri, S., Petersen, R.S., Schultz, S.R. & Lebedev, M. The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron, 29, 769–777 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. Abeles, M., Bergman, E., Margalit, H. & Vaadia, E. Spatiotemporal firing patterns in the frontal cortex of behaving monkeys. J. Neurophysiol. 70, 1629–1638 (1993).

    Article  CAS  PubMed  Google Scholar 

  20. Diesmann, M., Gewaltig, M.O. & Aertsen, A. Stable propagation of synchronous spiking in cortical neural networks. Nature 402, 529–533 (1999).

    Article  CAS  PubMed  Google Scholar 

  21. Cateau, H. & Fukai, T. Fokker–Planck approach to the pulse packet propagation in synfire chain. Neural Net. 14, 675–685 (2001).

    Article  CAS  Google Scholar 

  22. Diesmann, M., Gewaltig, M., Rotter, S. & Aertsen, A., State space analysis of synchronous spiking in cortical neural networks. Neurocomputing 565, 38–40 (2001).

    Google Scholar 

  23. Gewaltig M., Diesmann, M. & Aertsen A. Propagation of cortical synfire activity: survival probability in single trials and stability in the mean. Neural Net. 14, 657–673 (2001).

    Article  CAS  Google Scholar 

  24. Barlow, H.B. Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1, 371–394 (1972).

    Article  CAS  PubMed  Google Scholar 

  25. van Rossum, M.C., Turrigiano, G.G. & Nelson, S.B. Fast propagation of firing rates through layered networks of noisy neurons. J. Neurosci. 22, 1956–1966 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Mazurek, M.E. & Shadlen, M.N. Limits to the temporal fidelity of cortical spike rate signals. Nat. Neurosci. 5, 463–471 (2002).

    Article  CAS  PubMed  Google Scholar 

  27. Litvak, V., Sompolinsky, H., Segev, I. & Abeles, M. On the transmission of rate code in long feed-forward networks with excitatory–inhibitory balance. J. Neurosci. 23, 3006–3015 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Oviedo, H. & Reyes, A.D. Boosting of neuronal firing evoked with asynchronous and synchronous inputs to the dendrite. Nat. Neurosci. 5, 261–266 (2002).

    Article  CAS  PubMed  Google Scholar 

  29. Markram, H., Lubke, J., Frotscher, M., Roth, A. & Sakmann, B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurons in the developing rat neocortex. J. Physiol. 500, 409–440 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Reyes, A.D. et al. Target-cell–specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1, 279–285 (1998).

    Article  CAS  PubMed  Google Scholar 

  31. Reyes, A.D. & Sakmann, B. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J. Neurosci. 19, 3827–3835 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Perkel, D.H., Gerstein, G.L. & Moore, G.P. Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys. J. 7, 419–440 (1967).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Fetz, E., Toyama, K. & Smith, W. Synaptic interactions between cortical neurons. Cereb. Cortex 9, 1 (1991).

    Article  Google Scholar 

  34. Pinsky, P.F. & Rinzel, J. Synchrony measures for biological neural networks. Biol. Cybern. 73, 129–37 (1995).

    Article  CAS  PubMed  Google Scholar 

  35. Sharp, A., O'Neil, M.B., Abbott, L.F. & Marder, E. The dynamic clamp: artificial conductances in biological neurons. TINS 16, 389–394 (1993).

    CAS  PubMed  Google Scholar 

  36. Reyes, A.D., Rubel, E.W. & Spain, W.J. In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J. Neurosci. 16, 993–1007 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Chance, F., Abbott, L.F. & Reyes, A.D. Gain modulation from background synaptic input. Neuron 35, 773–782 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. Mainen, Z.F. & Sejnowski, T.J. Reliability of spike timing in neocortical neurons. Science 268, 1503–1506 (1995).

    Article  CAS  PubMed  Google Scholar 

  39. Stevens, C.F. & Zador, A. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1, 210–217 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Connors, B.W. & Gutnick, M.J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13, 99–104 (1990).

    CAS  PubMed  Google Scholar 

  41. Schwindt, P.C., O'Brien, J.A. & Crill, W.E. Quantitative analysis of firing properties of pyramidal neurons from layer 5 of rat sensorimotor cortex. J. Neurophysiol. 77, 2484–2498 (1997).

    Article  CAS  PubMed  Google Scholar 

  42. Softky, W. & Koch, C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci. 13, 334–350 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Holt, G.R., Softky, W.R., Koch, C. & Douglas, R.J. Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J. Neurophysiol. 75, 1806–1814 (1996).

    Article  CAS  PubMed  Google Scholar 

  44. Markram, H., Wang, Y. & Tsodyks, M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc. Natl. Acad. Sci. USA 9, 5323–5328 (1998).

    Article  Google Scholar 

  45. Reyes, A.D. & Fetz, E.E. Effects of transient depolarizing potentials on the firing rate of cat neocortical neurons. J. Neurophysiol. 69, 1673–1682 (1993).

    Article  CAS  PubMed  Google Scholar 

  46. Reyes, A.D. & Fetz, E.E. Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. J. Neurophysiol. 69, 1661–1672 (1993).

    Article  CAS  PubMed  Google Scholar 

  47. Baker, S.N. Quantification of the relative efficacies of asynchronous and oscillating inputs to a motoneuron pool using a computer model. J. Physiol. 504, 116 (1997).

    Google Scholar 

  48. Azouz, R. & Gray, C.M. Cellular mechanisms contributing to response variability of cortical neurons in vivo. J. Neurosci. 19, 2209–2223 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Azouz, R. & Gray, C.M. Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37, 513–523 (2003).

    Article  CAS  PubMed  Google Scholar 

  50. Matsumura, M. et al. Synaptic interactions between primate precentral cortex neurons revealed by spike–triggered averaging of intracellular membrane potentials in vivo. J. Neurosci. 16, 7757–7767 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The author wishes to thank H. Cateau, F. Chance, T. Lewis and R. Shapley for providing helpful comments. This work was supported by National Science Foundation grant IBN–0079619 and by the Edith J. Low-Beer foundation.

Author information

Authors and Affiliations

Authors

Ethics declarations

Competing interests

The author declares no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reyes, A. Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro. Nat Neurosci 6, 593–599 (2003). https://doi.org/10.1038/nn1056

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1056

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing