Skip to main content
Log in

A Measure of Concurrent Neural Firing Activity Based on Mutual Information

  • Original Article
  • Published:
Neuroinformatics Aims and scope Submit manuscript

Abstract

Multiple methods have been developed in an attempt to quantify stimulus-induced neural coordination and to understand internal coordination of neuronal responses by examining the synchronization phenomena in neural discharge patterns. In this work we propose a novel approach to estimate the degree of concomitant firing between two neural units, based on a modified form of mutual information (MI) applied to a two-state representation of the firing activity. The binary profile of each single unit unfolds its discharge activity in time by decomposition into the state of neural quiescence/low activity and state of moderate firing/bursting. Then, the MI computed between the two binary streams is normalized by their minimum entropy and is taken as positive or negative depending on the prevalence of identical or opposite concomitant states. The resulting measure, denoted as Concurrent Firing Index based on MI (CFIMI), relies on a single input parameter and is otherwise assumption-free and symmetric. Exhaustive validation was carried out through controlled experiments in three simulation scenarios, showing that CFIMI is independent on firing rate and recording duration, and is sensitive to correlated and anti-correlated firing patterns. Its ability to detect non-correlated activity was assessed using ad-hoc surrogate data. Moreover, the evaluation of CFIMI on experimental recordings of spiking activity in retinal ganglion cells brought insights into the changes of neural synchrony over time. The proposed measure offers a novel perspective on the estimation of neural synchrony, providing information on the co-occurrence of firing states in the two analyzed trains over longer temporal scales compared to existing measures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allen, A.E., Storchi, R., Martial, F.P., Bedford, R.A., & Lucas, R.J. (2017). Melanopsin contributions to the representation of images in the early visual system. Current Biology, 27(11), 1623–1632.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brivanlou, I.H., Warland, D.K., & Meister, M. (1998). Mechanisms of concerted firing among retinal ganglion cells. Neuron, 20(3), 527–539.

    Article  CAS  PubMed  Google Scholar 

  • Brown, E.N., Kass, R.E., & Mitra, P.P. (2004). Multiple neural spike train data analysis: state-of-the-art and future challenges. Nature Neuroscience, 7(5), 456–461.

    Article  CAS  PubMed  Google Scholar 

  • Brown, T.M., Gias, C., Hatori, M., Keding, S.R., Semo, M., Coffey, P.J., Gigg, J., Piggins, H.D., Panda, S., & Lucas, R.J. (2010). Melanopsin contributions to irradiance coding in the thalamo-cortical visual system. PLoS Biology 8(12).

  • Buzsaki, G. (2006). Rhythms of the Brain. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Cutts, C.S., & Eglen, S.J. (2014). Detecting pairwise correlations in spike trains: an objective comparison of methods and application to the study of retinal waves. Journal of Neuroscience, 34(43), 14288–14303.

    Article  CAS  PubMed  Google Scholar 

  • Daw, C.S., Finney, C.E.A., & Tracy, E.R. (2003). A review of symbolic analysis of experimental data. Review of Scientific Instruments, 74(2), 915–930.

    Article  CAS  Google Scholar 

  • Eggermont, J.J. (2010). Pair-correlation in the time and frequency domain. In Analysis of parallel spike trains (pp. 77–102): Springer,.

  • Ermentrout, G.B., Galán, R F, & Urban, N.N. (2008). Reliability, synchrony and noise. Trends in Neurosciences, 31(8), 428–434.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fred, A.L., & Leitão, J.M. (2003). A new cluster isolation criterion based on dissimilarity increments. IEEE Transactions on Pattern Analysis and Machine Intelligence, 25(8), 944–958.

    Article  Google Scholar 

  • Gollisch, T., & Meister, M. (2008). Rapid neural coding in the retina with relative spike latencies. Science, 319(5866), 1108–1111.

    Article  CAS  PubMed  Google Scholar 

  • Gray, R.M. (2011). Entropy and information theory. Berlin: Springer Science & Business Media.

    Book  Google Scholar 

  • Gray, R.M., & Shields, P.C. (1977). The maximum mutual information between two random processes. Information and Control, 33(4), 273–280.

    Article  Google Scholar 

  • Grewe, J., Kruscha, A., Lindner, B., & Benda, J. (2017). Synchronous spikes are necessary but not sufficient for a synchrony code in populations of spiking neurons. Proceedings of the National Academy of Sciences, 114(10), E1977–E1985.

    Article  CAS  Google Scholar 

  • Guzzetti, S., Borroni, E.A., Garbelli, P.E., Ceriani, E., Della Bella, P., Montano, N., Cogliati, C., Somers, V.K., Malliani, A., & Porta, A. (2005). Symbolic dynamics of heart rate variability - a probe to investigate cardiac autonomic modulation. Circulation, 112(4), 465–470.

    Article  PubMed  Google Scholar 

  • Ishikane, H., Gangi, M., Honda, S., & Tachibana, M. (2005). Synchronized retinal oscillations encode essential information for escape behavior in frogs. Nature Neuroscience, 8(8), 1087–1095.

    Article  CAS  PubMed  Google Scholar 

  • Izhikevich, E.M. (2003). Simple model of spiking neurons. IEEE Transactions on Neural Networks, 14(6), 1569–1572.

    Article  CAS  PubMed  Google Scholar 

  • Izhikevich, E.M. (2007). Dynamical systems in neuroscience. Cambridge: MIT press.

    Google Scholar 

  • Kandel, E.R., Schwartz, J.H., Jessell, T.M., Biochemistry, D., Jessell, M.B.T., Siegelbaum, S., & Hudspeth, A. (2000). Principles of neural science Vol. 4. New York: McGraw-hill.

    Google Scholar 

  • Kerschensteiner, D., & Wong, R.O. (2008). A precisely timed asynchronous pattern of on and off retinal ganglion cell activity during propagation of retinal waves. Neuron, 58(6), 851– 858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreuz, T., Mulansky, M., & Bozanic, N. (2015). Spiky: a graphical user interface for monitoring spike train synchrony. Journal of Neurophysiology, 113(9), 3432–3445.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li, W. (1990). Mutual information functions versus correlation functions. Journal of Statistical Physics, 60(5-6), 823–837.

    Article  Google Scholar 

  • Meister, M., Lagnado, L., & Baylor, D.A. (1995). Concerted signaling by retinal ganglion cells. Science, 270(5239), 1207–1210.

    Article  CAS  PubMed  Google Scholar 

  • Mijatović, G, Lončar-Turukalo, T., Procyk, E., & Bajić, D. (2018). A novel approach to probabilistic characterisation of neural firing patterns. Journal of Neuroscience Methods, 305, 67–81.

    Article  PubMed  Google Scholar 

  • Mijatovic, G., Loncar-Turukalo, T., Bozanic, N., & Faes, L. (2020). Information–theoretic characterization of concurrent activity of neural spike trains. In 2020 28th european signal processing conference (pp. 925–929). EUSIPCO: IEEE.

  • Milosavljevic, N., Storchi, R., Eleftheriou, C.G., Colins, A., Petersen, R.S., & Lucas, R.J. (2018). Photoreceptive retinal ganglion cells control the information rate of the optic nerve. Proceedings of the National Academy of Sciences, 115(50), E11817– E11826.

    Article  CAS  Google Scholar 

  • Niebur, E. (2007). Generation of synthetic spike trains with defined pairwise correlations. Neural Computation, 19(7), 1720–1738.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ostojic, S. (2011). Interspike interval distributions of spiking neurons driven by fluctuating inputs. Journal of Neurophysiology, 106(1), 361–373.

    Article  PubMed  Google Scholar 

  • Pasquale, V., Massobrio, P., Bologna, L., Chiappalone, M., & Martinoia, S. (2008). Self-organization and neuronal avalanches in networks of dissociated cortical neurons. Neuroscience, 153(4), 1354– 1369.

    Article  CAS  PubMed  Google Scholar 

  • Porta, A., Baumert, M., Cysarz, D., & Wessel. N. (2015). Enhancing dynamical signatures of complex systems through symbolic computation.

  • Puchalla, J.L., Schneidman, E., Harris, R.A., & Berry, M.J. (2005). Redundancy in the population code of the retina. Neuron, 46(3), 493–504.

    Article  CAS  PubMed  Google Scholar 

  • Ricci, L., Castelluzzo, M., Minati, L., & Perinelli, A. (2019). Generation of surrogate event sequences via joint distribution of successive inter-event intervals. Chaos: An Interdisciplinary Journal of Nonlinear Science, 29(12), 121102.

    Article  Google Scholar 

  • Schlather, M., Ribeiro, P.J. Jr, & Diggle, P.J. (2004). Detecting dependence between marks and locations of marked point processes. Journal of the Royal Statistical Society: Series B (Statistical Methodology), 66 (1), 79–93.

    Article  Google Scholar 

  • Schneidman, E., Bialek, W., & Berry, M.J. (2003). Synergy, redundancy, and independence in population codes. Journal of Neuroscience, 23(37), 11539–11553.

    Article  CAS  PubMed  Google Scholar 

  • Schneidman, E., Berry, M.J., Segev, R., & Bialek, W. (2006). Weak pairwise correlations imply strongly correlated network states in a neural population. Nature, 440(7087), 1007–1012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnitzer, M.J., & Meister, M. (2003). Multineuronal firing patterns in the signal from eye to brain. Neuron, 37(3), 499– 511.

    Article  CAS  PubMed  Google Scholar 

  • Shannon, C.E. (1948). A mathematical theory of communication. Bell System Technical Journal, 27(3), 379–423.

    Article  Google Scholar 

  • Shlens, J., Field, G.D., Gauthier, J.L., Grivich, M.I., Petrusca, D., Sher, A., Litke, A.M., & Chichilnisky, E. (2006). The structure of multi-neuron firing patterns in primate retina. Journal of Neuroscience, 26(32), 8254–8266.

    Article  CAS  PubMed  Google Scholar 

  • Shlens, J., Rieke, F., & Chichilnisky, E. (2008). Synchronized firing in the retina. Current Opinion in Neurobiology, 18(4), 396– 402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singer, W. (1999). Neuronal synchrony: A versatile code for the definition of relations?. Neuron, 24(1), 49–65.

    Article  CAS  PubMed  Google Scholar 

  • Spavieri, D.L., Eichner, H., & Borst, A. (2010). Coding efficiency of fly motion processing is set by firing rate, not firing precision. PLoS Computational Biology, 6(7), e1000860.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Steuer, R., Ebeling, W., Russell, D., Bahar, S., Neiman, A., & Moss, F. (2001). Entropy and local uncertainty of data from sensory neurons. Physical Review E, 64(6), 061911.

    Article  CAS  Google Scholar 

  • Usher, M., & Donnelly, N. (1998). Visual synchrony affects binding and segmentation in perception. Nature, 394(6689), 179–182.

    Article  CAS  PubMed  Google Scholar 

  • Usrey, W.M., & Reid, R.C. (1999). Synchronous activity in the visual system. Annual Review of Physiology, 61(1), 435–456.

    Article  CAS  PubMed  Google Scholar 

  • Wong, K.Y. (2012). A retinal ganglion cell that can signal irradiance continuously for 10 hours. Journal of Neuroscience, 32(33), 11478–11485.

    Article  CAS  PubMed  Google Scholar 

  • Wong, R.O., Meister, M., & Shatz, C.J. (1993). Transient period of correlated bursting activity during development of the mammalian retina. Neuron, 11(5), 923–938.

    Article  CAS  PubMed  Google Scholar 

  • Hp, X u, Furman, M., Mineur, Y.S., Chen, H., King, S.L., Zenisek, D., Zhou, Z.J., Butts, D.A., Tian, N., Picciotto, M.R., & et al. (2011). An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron, 70(6), 1115–1127.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research has been supported by the Ministry of Education, Science and Technological Development through the project no. 451-03-68/2020-14/200156: “Innovative scientific and artistic research from the FTS (activity) domain” and from the European Union’s Horizon 2020 research and innovation programme under Grant Agreement number 856967. Luca Faes acknowledges funding from Ministero dell’Istruzione, dell’Università e della Ricerca—PRIN 2017 (PRJ-0167), “Stochastic forecasting in complex systems”. The authors express gratitude to Leonardo Ricci and Alessio Perinelli for sharing Matlab code for JODI method, and to Danica Despotovic for useful discussion.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gorana Mijatovic.

Ethics declarations

Conflict of Interests

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mijatovic, G., Loncar-Turukalo, T., Bozanic, N. et al. A Measure of Concurrent Neural Firing Activity Based on Mutual Information. Neuroinform 19, 719–735 (2021). https://doi.org/10.1007/s12021-021-09515-w

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12021-021-09515-w

Keywords

Navigation