Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Open Access

How Random Connectivity Shapes the Fluctuating Dynamics of Finite-Size Neural Populations

Nils E. Greven1,2, Jonas Ranft3,*, and Tilo Schwalger1,2,†

  • *Contact author: jonas.ranft@ens.psl.eu
  • †Contact author: tilo.schwalger@bccn-berlin.de

PRX Life 4, 013007 – Published 14 January, 2026

DOI: https://doi.org/10.1103/shvm-x4x6

Abstract

Mesoscopic models of finite-size neuronal populations are crucial to understand the dynamics of neural networks in the brain, especially their fluctuations and response to stimuli. However, current theories to derive such models are based on the assumption of homogeneous all-to-all (full) connectivity, neglecting the variance in the connectivity of biologically realistic networks with connection probabilities p<1 (nonfull connectivity). To gain insight into the different fluctuation mechanisms underlying the neural variability of populations of spiking neurons, we derive and analyze a stochastic mean-field model for finite-size networks of Poisson neurons with random connectivity (including nonfull connectivity), external noise, and disordered mean inputs. We treat the quenched disorder of the connectivity by an annealed approximation enabling a doubly stochastic description of synaptic inputs for finite network size. A further reduction leads to a low-dimensional closed system of coupled Langevin equations for the mean and variance of the neuronal membrane potentials as well as a variable capturing finite-size fluctuations arising specifically in the case of connectivity disorder. Comparing to microscopic simulations, we find that the mesoscopic model describes the fluctuations and nonlinearities well and outperforms previous mesoscopic models that neglected the variance in the connectivity. The joint effect of connectivity disorder and finite network size can be analytically understood by a softening of the effective nonlinearity and the multiplicative character of spiking noise. The mesoscopic theory shows that quenched disorder can stabilize the asynchronous state, and it correctly predicts large quantitative and nontrivial qualitative effects of connection probability on the variance of the population firing rate and its dependence on stimulus strength. Our theory thus elucidates how disordered connectivity shapes nonlinear dynamics and fluctuations of neural populations at the mesoscopic scale and showcases a useful mean-field method to treat random connectivity in finite-size, spiking neural networks.

View figure in article

Physics Subject Headings (PhySH)

Article Text

References (89)

  1. M. B. Elowitz, A. J. Levine, E. D. Siggia, and P. S. Swain, Stochastic gene expression in a single cell, Science 297, 1183 (2002).
  2. A. Raj and A. Van Oudenaarden, Nature, nurture, or chance: Stochastic gene expression and its consequences, Cell 135, 216 (2008).
  3. S. Taheri-Araghi, S. Bradde, J. T. Sauls, N. S. Hill, P. A. Levin, J. Paulsson, M. Vergassola, and S. Jun, Cell-Size control and homeostasis in bacteria, Curr. Biol. 25, 385 (2015).
  4. S. Arzash, I. Tah, A. J. Liu, and M. L. Manning, Rigidity of epithelial tissues as a double optimization problem, Phys. Rev. Res. 7, 013157 (2025).
  5. A. A. Faisal, L. P. J. Selen, and D. M. Wolpert, Noise in the nervous system, Nat. Rev. Neurosci. 9, 292 (2008).
  6. B. Doiron, A. Litwin-Kumar, R. Rosenbaum, G. K. Ocker, and K. Josić, The mechanics of state dependent neural correlations, Nat. Neurosci. 19, 383 (2016).
  7. L. Waschke, N. A. Kloosterman, J. Obleser, and D. D. Garrett, Behavior needs neural variability, Neuron 109, 751 (2021).
  8. T. B. Kepler and T. C. Elston, Stochasticity in transcriptional regulation: Origins, consequences, and mathematical representation, Biophys. J. 81, 3116 (2001).
  9. T. Guérin, J. Prost, and J.-F. Joanny, Bidirectional motion of motor assemblies and the weak-noise escape problem, Phys. Rev. E 84, 041901 (2011).
  10. C. Touya, T. Schwalger, and B. Lindner, Relation between cooperative molecular motors and active Brownian particles, Phys. Rev. E 83, 051913 (2011).
  11. R. Ma, G. S. Klindt, I. H. Riedel-Kruse, F. Jülicher, and B. M. Friedrich, Active phase and amplitude fluctuations of flagellar beating, Phys. Rev. Lett. 113, 048101 (2014).
  12. A. Dobrinevski and E. Frey, Extinction in neutrally stable stochastic Lotka-Volterra models, Phys. Rev. E 85, 051903 (2012).
  13. H. R. Wilson and J. D. Cowan, Excitatory and inhibitory interactions in localized populations of model neurons, Biophys. J. 12, 1 (1972).
  14. Y. Lu and J. Rinzel, Firing rate models for gamma oscillations in I-I and E-I networks, J. Comput. Neurosci. 52, 247 (2024).
  15. D. Levenstein, G. Buzsáki, and J. Rinzel, Nrem sleep in the rodent neocortex and hippocampus reflects excitable dynamics, Nat. Commun. 10, 2478 (2019).
  16. Y. Ahmadian, D. B. Rubin, and K. D. Miller, Analysis of the stabilized supralinear network, Neural Comput. 25, 1994 (2013).
  17. K.-F. Wong and X.-J. Wang, A recurrent network mechanism of time integration in perceptual decisions, J. Neurosci. 26, 1314 (2006).
  18. A. Shpiro, R. Moreno-Bote, N. Rubin, and J. Rinzel, Balance between noise and adaptation in competition models of perceptual bistability, J. Comput. Neurosci. 27, 37 (2009).
  19. G. Dumont, G. Northoff, and A. Longtin, Linear noise approximation for oscillations in a stochastic inhibitory network with delay, Phys. Rev. E 90, 012702 (2014).
  20. T. Kanashiro, G. K. Ocker, M. R. Cohen, and B. Doiron, Attentional modulation of neuronal variability in circuit models of cortex, eLife 6, e23978 (2017).
  21. G. Hennequin, Y. Ahmadian, D. B. Rubin, M. Lengyel, and K. D. Miller, The dynamical regime of sensory cortex: Stable dynamics around a single stimulus-tuned attractor account for patterns of noise variability, Neuron 98, 846 (2018).
  22. S.-I. Amari, Characteristics of random nets of analog neuron-like elements, IEEE Trans. Syst. Man Cybern. SMC-2, 643 (1972).
  23. W. Gerstner, W. M. Kistler, R. Naud, and L. Paninski, Neuronal Dynamics: From Single Neurons to Networks and Models of Cognition (Cambridge University Press, Cambridge, UK, 2014).
  24. G. Deco, V. K. Jirsa, P. A. Robinson, M. Breakspear, and K. Friston, The dynamic brain: From spiking neurons to neural masses and cortical fields, PLoS Comput. Biol. 4, e1000092 (2008).
  25. O. D. Faugeras, J. D. Touboul, and B. Cessac, A constructive mean-field analysis of multi population neural networks with random synaptic weights and stochastic inputs, Front. Comput. Neurosci. 3, 323 (2009).
  26. S. El Boustani and A. Destexhe, A master equation formalism for macroscopic modeling of asynchronous irregular activity states, Neural Comput. 21, 46 (2009).
  27. G. La Camera, The mean field approach for populations of spiking neurons, in Computational Modelling of the Brain: Modelling Approaches to Cells, Circuits and Networks, edited by M. Giugliano, M. Negrello, and D. Linaro (Springer International, Cham, 2022), pp. 125–157.
  28. G. K. Ocker, Republished: Dynamics of stochastic integrate-and-fire networks, Phys. Rev. X 13, 041047 (2023).
  29. N. Brunel and V. Hakim, Fast global oscillations in networks of integrate-and-fire neurons with low firing rates, Neural Comput. 11, 1621 (1999).
  30. N. Brunel, Sparsely connected networks of spiking neurons, J. Comput. Neurosci. 8, 183 (2000).
  31. W. Gerstner, Population dynamics of spiking neurons: Fast transients, asynchronous states, and locking, Neural Comput. 12, 43 (2000).
  32. E. Montbrió, D. Pazó, and A. Roxin, Macroscopic description for networks of spiking neurons, Phys. Rev. X 5, 021028 (2015).
  33. V. Schmutz, E. Löcherbach, and T. Schwalger, On a finite-size neuronal population equation, SIAM J. Appl. Dyn. Syst. 22, 996 (2023).
  34. D. Q. Nykamp and D. Tranchina, A population density approach that facilitates large-scale modeling of neural networks: Analysis and an application to orientation tuning, J. Comput. Neurosci. 8, 19 (2000).
  35. N. Cain, R. Iyer, C. Koch, and S. Mihalas, The computational properties of a simplified cortical column model, PLoS Comput. Biol. 12, e1005045 (2016).
  36. T. Schwalger, M. Deger, and W. Gerstner, Towards a theory of cortical columns: From spiking neurons to interacting neural populations of finite size, PLoS Comput. Biol. 13, e1005507 (2017).
  37. M. Augustin, J. Ladenbauer, F. Baumann, and K. Obermayer, Low-dimensional spike rate models derived from networks of adaptive integrate-and-fire neurons: Comparison and implementation, PLoS Comput. Biol. 13, e1005545 (2017).
  38. A. René, A. Longtin, and J. H. Macke, Inference of a mesoscopic population model from population spike trains, Neural Comput. 32, 1448 (2020).
  39. S. Wang, V. Schmutz, G. Bellec, and W. Gerstner, Mesoscopic modeling of hidden spiking neurons, Adv. Neural Inf. Process. Syst. 35, 23566 (2022).
  40. C. Pozzorini, S. Mensi, O. Hagens, R. Naud, C. Koch, and W. Gerstner, Automated high-throughput characterization of single neurons by means of simplified spiking models, PLoS Comput. Biol. 11, e1004275 (2015).
  41. Y. N. Billeh, B. Cai, S. L. Gratiy, K. Dai, R. Iyer, N. W. Gouwens, R. Abbasi-Asl, X. Jia, J. H. Siegle, S. R. Olsen, C. Koch, S. Mihalas, and A. Arkhipov, Systematic integration of structural and functional data into multi-scale models of mouse primary visual cortex, Neuron 106, 388 (2020).
  42. M. A. Buice, J. D. Cowan, and C. C. Chow, Systematic fluctuation expansion for neural network activity equations, Neural Comput. 22, 377 (2010).
  43. M. A. Buice and C. C. Chow, Dynamic finite size effects in spiking neural networks, PLoS Comput. Biol. 9, e1002872 (2013).
  44. G. Dumont, A. Payeur, and A. Longtin, A stochastic-field description of finite-size spiking neural networks, PLoS Comput. Biol. 13, e1005691 (2017).
  45. S. Heesen and W. Stannat, Fluctuation limits for mean-field interacting nonlinear Hawkes processes, Stochast. Process. Appl. 139, 280 (2021).
  46. V. V. Klinshov and S. Y. Kirillov, Shot noise in next-generation neural mass models for finite-size networks, Phys. Rev. E 106, L062302 (2022).
  47. M. Deger, T. Schwalger, R. Naud, and W. Gerstner, Fluctuations and information filtering in coupled populations of spiking neurons with adaptation, Phys. Rev. E 90, 062704 (2014).
  48. H. Sompolinsky, A. Crisanti, and H. J. Sommers, Chaos in random neural networks, Phys. Rev. Lett. 61, 259 (1988).
  49. L. Molgedey, J. Schuchhardt, and H. G. Schuster, Suppressing chaos in neural networks by noise, Phys. Rev. Lett. 69, 3717 (1992).
  50. C. van Vreeswijk and H. Sompolinsky, Chaos in neuronal networks with balanced excitatory and inhibitory activity, Science 274, 1724 (1996).
  51. A. Renart, R. Moreno-Bote, X.-J. Wang, and N. Parga, Mean-driven and fluctuation-driven persistent activity in recurrent networks, Neural Comput. 19, 1 (2007).
  52. M. Helias, T. Tetzlaff, and M. Diesmann, The correlation structure of local neuronal networks intrinsically results from recurrent dynamics, PLoS Comput. Biol. 10, e1003428 (2014).
  53. D. S. Goldobin, M. di Volo, and A. Torcini, Reduction methodology for fluctuation driven population dynamics, Phys. Rev. Lett. 127, 038301 (2021).
  54. S. Lefort, C. Tomm, J. C. F. Sarria, and C. C. H. Petersen, The excitatory neuronal network of the c2 barrel column in mouse primary somatosensory cortex, Neuron 61, 301 (2009).
  55. A. Compte, N. Brunel, P. S. Goldman-Rakic, and X.-J. Wang, Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model, Cereb. Cortex 10, 910 (2000).
  56. L. Mazzucato, A. Fontanini, and G. La Camera, Dynamics of multistable states during ongoing and evoked cortical activity, J. Neurosci. 35, 8214 (2015).
  57. G. Gigante, G. Deco, S. Marom, and P. Del Giudice, Network events on multiple space and time scales in cultured neural networks and in a stochastic rate model, PLoS Comput. Biol. 11, e1004547 (2015).
  58. V. Schmutz, W. Gerstner, and T. Schwalger, Mesoscopic population equations for spiking neural networks with synaptic short-term plasticity, J. Math. Neurosc. 10, 5 (2020).
  59. B. Pietras, V. Schmutz, and T. Schwalger, Mesoscopic description of hippocampal replay and metastability in spiking neural networks with short-term plasticity, PLoS Comput. Biol. 18, e1010809 (2022).
  60. H. Ko, S. B. Hofer, B. Pichler, K. A. Buchanan, P. J. Sjöström, and T. D. Mrsic-Flogel, Functional specificity of local synaptic connections in neocortical networks, Nature (London) 473, 87 (2011).
  61. M. M. Churchland, M. Y. Byron, J. P. Cunningham, L. P. Sugrue, M. R. Cohen, G. S. Corrado, W. T. Newsome, A. M. Clark, P. Hosseini, B. B. Scott et al., Stimulus onset quenches neural variability: A widespread cortical phenomenon, Nat. Neurosci. 13, 369 (2010).
  62. S. Wieland, D. Bernardi, T. Schwalger, and B. Lindner, Slow fluctuations in recurrent networks of spiking neurons, Phys. Rev. E 92, 040901(R) (2015).
  63. A. Sanzeni, M. H. Histed, and N. Brunel, Response nonlinearities in networks of spiking neurons, PLoS Comput. Biol. 16, e1008165 (2020).
  64. N. Schieferstein, T. Schwalger, B. Lindner, and R. Kempter, Intra-ripple frequency accommodation in an inhibitory network model for hippocampal ripple oscillations, PLoS Comput. Biol. 20, e1011886 (2024).
  65. P. Ekelmans, N. Kraynyukova, and T. Tchumatchenko, Targeting operational regimes of interest in recurrent neural networks, PLoS Comput. Biol. 19, e1011097 (2023).
  66. M. Mattia and P. Del Giudice, Population dynamics of interacting spiking neurons, Phys. Rev. E 66, 051917 (2002).
  67. B. Derrida and Y. Pomeau, Random networks of automata: A simple annealed approximation, Europhys. Lett. 1, 45 (1986).
  68. R. Jolivet, A. Rauch, H. R. Lüscher, and W. Gerstner, Predicting spike timing of neocortical pyramidal neurons by simple threshold models, J. Comput. Neurosci. 21, 35 (2006).
  69. N. J. Priebe and D. Ferster, Inhibition, spike threshold, and stimulus selectivity in primary visual cortex, Neuron 57, 482 (2008).
  70. N. Brunel and D. Hansel, How noise affects the synchronization properties of recurrent networks of inhibitory neurons, Neural Comput. 18, 1066 (2006).
  71. B. Lindner, B. Doiron, and A. Longtin, Theory of oscillatory firing induced by spatially correlated noise and delayed inhibitory feedback, Phys. Rev. E 72, 061919 (2005).
  72. S. P. Muscinelli, W. Gerstner, and T. Schwalger, How single neuron properties shape chaotic dynamics and signal transmission in random neural networks, PLoS Comput. Biol. 15, e1007122 (2019).
  73. N. Brunel and V. Hakim, Sparsely synchronized neuronal oscillations, Chaos 18, 015113 (2008).
  74. E. Ledoux and N. Brunel, Dynamics of networks of excitatory and inhibitory neurons in response to time-dependent inputs, Front. Comput. Neurosci. 5, 25 (2011).
  75. J. Kadmon and H. Sompolinsky, Transition to chaos in random neuronal networks, Phys. Rev. X 5, 041030 (2015).
  76. D. Dahmen, S. Grün, M. Diesmann, and M. Helias, Second type of criticality in the brain uncovers rich multiple-neuron dynamics, Proc. Natl. Acad. Sci. USA 116, 13051 (2019).
  77. G. Hennequin, T. P. Vogels, and W. Gerstner, Optimal control of transient dynamics in balanced networks supports generation of complex movements, Neuron 82, 1394 (2014).
  78. Y.-L. Shi, R. Zeraati, I. B. Laboratory, A. Levina, and T. A. Engel, Brain-wide organization of intrinsic timescales at single-neuron resolution, https://doi.org/10.1101/2025.08.30.673281 (2025).
  79. A. Kulkarni, J. Ranft, and V. Hakim, Synchronization, stochasticity, and phase waves in neuronal networks with spatially-structured connectivity, Front. Comput. Neurosci. 14, 569644 (2020).
  80. A. Sanzeni, B. Akitake, H. C. Goldbach, C. E. Leedy, N. Brunel, and M. H. Histed, Inhibition stabilization is a widespread property of cortical networks, eLife 9, e54875 (2020).
  81. L. Kang, J. Ranft, and V. Hakim, Beta oscillations and waves in motor cortex can be accounted for by the interplay of spatially structured connectivity and fluctuating inputs, eLife 12, e81446 (2023).
  82. G. Hahn, A. Kumar, H. Schmidt, T. R. Knösche, and G. Deco, Rate and oscillatory switching dynamics of a multilayer visual microcircuit model, eLife 11, e77594 (2022).
  83. L. Yu and T. O. Taillefumier, Metastable spiking networks in the replica-mean-field limit, PLoS Comput. Biol. 18, e1010215 (2022).
  84. G. Dumont, J. Henry, and C. O. Tarniceriu, Oscillations in a fully connected network of leaky integrate-and-fire neurons with a poisson spiking mechanism, J. Nonlin. Sci. 34, 18 (2024).
  85. B. W. Knight, D. Manin, and L. Sirovich, Dynamical models of interacting neuron populations in visual cortex, in Symposium on Robotics and Cybernetics: Computational Engineering in Systems Applications, edited by E. C. Geil (Cite Scientifique, Lille, 1996), Vol. 54, pp. 4–8.
  86. G. V. Vinci, R. Benzi, and M. Mattia, Self-consistent stochastic dynamics for finite-size networks of spiking neurons, Phys. Rev. Lett. 130, 097402 (2023).
  87. https://github.com/Nils-Greven/random-connectivity-finite-size-network.
  88. H. Risken, The Fokker-Planck Equation (Springer, Berlin, 1984).
  89. D. B. Owen, A table of normal integrals, Commun. Stat. Simul. Comput. 9, 389 (1980).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation