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.

  • Letter
  • Published:

Correlation between neural spike trains increases with firing rate

Abstract

Populations of neurons in the retina1,2,3, olfactory system4, visual5 and somatosensory6 thalamus, and several cortical regions7,8,9,10 show temporal correlation between the discharge times of their action potentials (spike trains). Correlated firing has been linked to stimulus encoding9, attention11, stimulus discrimination4, and motor behaviour12. Nevertheless, the mechanisms underlying correlated spiking are poorly understood2,3,13,14,15,16,17,18,19,20, and its coding implications are still debated13,16,21,22. It is not clear, for instance, whether correlations between the discharges of two neurons are determined solely by the correlation between their afferent currents, or whether they also depend on the mean and variance of the input. We addressed this question by computing the spike train correlation coefficient of unconnected pairs of in vitro cortical neurons receiving correlated inputs. Notably, even when the input correlation remained fixed, the spike train output correlation increased with the firing rate, but was largely independent of spike train variability. With a combination of analytical techniques and numerical simulations using ‘integrate-and-fire’ neuron models we show that this relationship between output correlation and firing rate is robust to input heterogeneities. Finally, this overlooked relationship is replicated by a standard threshold-linear model, demonstrating the universality of the result. This connection between the rate and correlation of spiking activity links two fundamental features of the neural code.

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

Access options

Buy this article

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

Figure 1: Relationship between output spike correlation and rate in in vitro cells.
Figure 2: The correlation–rate relationship in an integrate-and-fire neuron model.
Figure 3: Correlation–rate relationship in a simple network.
Figure 4: Nonlinearities shape the correlation–rate relationship in a phenomenological neural model.

Similar content being viewed by others

References

  1. Mastronarde, D. N. Correlated firing of cat retinal ganglion cells. I. spontaneously active inputs to x-and y-cells. J. Neurophysiol. 49, 303–324 (1983)

    Article  CAS  Google Scholar 

  2. Schneidman, E., Berry, M. J., Segev, R. & Bialek, W. Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440, 1007–1012 (2006)

    Article  ADS  CAS  Google Scholar 

  3. Shlens, J. et al. The structure of multi-neuron firing patterns in primate retina. J. Neurosci. 26, 8254–8266 (2006)

    Article  CAS  Google Scholar 

  4. Stopfer, M., Bhagavan, S., Smith, B. H. & Laurent, G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70–74 (1997)

    Article  ADS  CAS  Google Scholar 

  5. Alonso, J. M., Usrey, W. M. & Reid, W. M. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815–819 (1996)

    Article  ADS  CAS  Google Scholar 

  6. Bruno, R. M. & Sakmann, B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312, 1622–1627 (2006)

    Article  ADS  CAS  Google Scholar 

  7. Zohary, E., Shadlen, M. N. & Newsome, W. T. Correlated neuronal discharge rate and its implication for psychophysical performance. Nature 370, 140–143 (1994)

    Article  ADS  CAS  Google Scholar 

  8. Kohn, A. & Smith, M. A. Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J. Neurosci. 25, 3661–3673 (2005)

    Article  CAS  Google Scholar 

  9. deCharms, R. C. & Merzenich, M. M. Primary cortical representation of sounds by the coordination of action potentials. Nature 381, 610–613 (1996)

    Article  ADS  CAS  Google Scholar 

  10. Bair, W., Zohary, E. & Newsome, W. T. Correlated firing in macaque visual area MT: Time scales and relationship to behavior. J. Neurosci. 21, 1676–1697 (2001)

    Article  CAS  Google Scholar 

  11. Steinmetz, P. N. et al. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404, 187–190 (2000)

    Article  ADS  CAS  Google Scholar 

  12. Vaadia, E. et al. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373, 515–518 (1995)

    Article  ADS  CAS  Google Scholar 

  13. Abeles, M. Corticonics: Neural circuits of the cerebral cortex (Cambridge Univ. Press, New York, 1991)

    Book  Google Scholar 

  14. Svirskis, G. & Hounsgaard, J. Influence of membrane properties on spike synchronization in neurons: theory and experiments. Network Comput. Neural Syst. 14, 747–763 (2003)

    Article  ADS  Google Scholar 

  15. Galán, R. F., Fourcaud-Trocme, N., Ermentrout, G. B. & Urban, N. N. Correlation-induced synchronization of oscillations in olfactory bulb neurons. J. Neurosci. 26, 3646–3655 (2006)

    Article  Google Scholar 

  16. 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  Google Scholar 

  17. Binder, M. D. & Powers, R. K. Relationship between simulated common synaptic input and discharge synchrony in cat spinal motoneurons. J. Neurophysiol. 86, 2266–2275 (2001)

    Article  CAS  Google Scholar 

  18. Dorn, J. D. & Ringach, D. L. Estimating membrane voltage correlations from extracellular spike trains. J. Neurophysiol. 89, 2271–2278 (2003)

    Article  Google Scholar 

  19. Reyes, A. D. Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro. Nature Neurosci. 6, 593–599 (2003)

    Article  ADS  CAS  Google Scholar 

  20. Doiron, B., Rinzel, J. & Reyes, A. Stochastic synchronization in finite size spiking networks. Phys. Rev. E 74, 030903 (2006)

    Article  ADS  MathSciNet  Google Scholar 

  21. Averbeck, B. B., Latham, P. E. & Pouget, A. Neural correlations, population coding and computation. Nature Rev. Neurosci. 7, 358–366 (2006)

    Article  CAS  Google Scholar 

  22. Salinas, E. & Sejnowski, T. J. Correlated neuronal activity and the flow of neural information. Nature Rev. Neurosci. 2, 539–550 (2001)

    Article  CAS  Google Scholar 

  23. Destexhe, A., Rudolph, M. & Paré, D. The high-conductance state of neocortical neurons in vivo. Nature Rev. Neurosci. 4, 739–751 (2003)

    Article  CAS  Google Scholar 

  24. Lampl, I., Reichova, I. & Ferster, D. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22, 361–374 (1999)

    Article  CAS  Google Scholar 

  25. Ricciardi, L. M. Diffusion Processes and Related Topics in Biology (Springer, Berlin, 1977)

    Book  Google Scholar 

  26. Lindner, B., Doiron, B. & Longtin, A. Theory of oscillatory firing induced by spatially correlated noise and delayed inhibitory feedback. Phys. Rev. E 72, 061919 (2005)

    Article  ADS  MathSciNet  Google Scholar 

  27. Lau, D. et al. Impaired fast-spiking, suppressed cortical inhibition, and increased susceptibility to seizures in mice lacking kv3.2 K+ channel proteins. J. Neurosci. 20, 9071–9085 (2000)

    Article  CAS  Google Scholar 

  28. Tsodyks, M. V. & Markram, H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl Acad. Sci. USA 94, 719–723 (1997)

    Article  ADS  CAS  Google Scholar 

  29. Polsky, A., Mel, B. & Schiller, J. Computational subunits in thin dendrites of pyramidal cells. Nature Neurosci. 7, 621–627 (2004)

    Article  CAS  Google Scholar 

  30. Larkum, M. E., Senn, W. & Lüscher, H.-R. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 14, 1059–1070 (2004)

    Article  Google Scholar 

Download references

Acknowledgements

We thank C. Colbert, A. Kohn, L. Maler, D. Nikolic, A.-M. Oswald and A. Renart for their critical reading of the manuscript, and R. Moreno-Bote, M. Schiff and J. Rinzel for insightful discussions. Funding was provided by the Spanish MEC (J.R.), HFSP (B.D.), a Burroughs Welcome Fund career award and an NSF postdoctoral fellowship (E.S.-B.), NSF (K.J.) and NIH (A.R.).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jaime de la Rocha or Brent Doiron.

Ethics declarations

Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Figures S1-S6 with Legends illustrating additional analysis of the correlation-rate relation and a complete derivation of Eq. (3) presented in the main text. (PDF 1362 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

de la Rocha, J., Doiron, B., Shea-Brown, E. et al. Correlation between neural spike trains increases with firing rate. Nature 448, 802–806 (2007). https://doi.org/10.1038/nature06028

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06028

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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