- Letter
- Open Access
Exactly solvable statistical physics models for large neuronal populations
Phys. Rev. Research 7, L022039 – Published 19 May, 2025
DOI: https://doi.org/10.1103/PhysRevResearch.7.L022039
Abstract
Maximum-entropy methods provide a principled path connecting measurements of neural activity directly to statistical physics models, and this approach has been successful for populations of neurons. As increases in new experiments, we enter an undersampled regime where we have to choose which observables should be constrained in the maximum-entropy construction. The best choice is the one that provides the greatest reduction in entropy, defining a “minimax entropy” principle. This principle becomes tractable if we restrict attention to correlations among pairs of neurons that link together into a tree; we can find the best tree efficiently, and the underlying statistical physics models are exactly solved. We use this approach to analyze experiments on neurons in the mouse hippocampus, and we find that the resulting model captures key features of collective activity in the network.
Physics Subject Headings (PhySH)
See Also
Exact minimax entropy models of large-scale neuronal activity
Article Text
References (44)
- N. Wiener, Nonlinear Problems in Random Theory (MIT Press, Cambridge, MA, 1958).
- L. N. Cooper, A possible organization of animal memory and learning, in Collective Properties of Physical Systems: Proceedings of Nobel Symposium 24, edited by B. Lundqvist and S. Lundqvist (Academic, New York, 1973), pp. 252–264.
- W. A. Little, The existence of persistent states in the brain, Math. Biosci. 19, 101 (1974).
- J. J. Hopfield, Neural networks and physical systems with emergent collective computational abilities, Proc. Natl. Acad. Sci. USA 79, 2554 (1982).
- D. J. Amit, Modeling Brain Function: The World of Attractor Neural Networks (Cambridge University Press, 1989).
- J. Hertz, A. Krogh, and R. G. Palmer, Introduction to the Theory of Neural Computation (Addison-Wesley, Redwood City, CA, 1991).
- L. Meshulam and W. Bialek, Statistical mechanics for networks of real neurons, arXiv:2409.00412.
- R. Segev, J. Goodhouse, J. Puchalla, and M. J. Berry II, Recording spikes from a large fraction of the ganglion cells in a retinal patch, Nat. Neurosci. 7, 1155 (2004).
- A. M. Litke, N. Bezayiff, E. J. Chichilnisky, W. Cunningham, W. Dabrowski, A. A. Grillo, M. Grivich, P. Grybos, P. Hottowy, S. Kachiguine et al., What does the eye tell the brain? Development of a system for the large-scale recording of retinal output activity, IEEE Trans. Nucl. Sci. 51, 1434 (2004).
- J. E. Chung, H. R. Joo, J. L. Fan, D. F. Liu, A. H. Barnett, S. Chen, C. Geaghan-Breiner, M. P. Karlsson, M. Karlsson, K. Y. Lee et al., High-density, long-lasting, and multi-region electrophysiological recordings using polymer electrode arrays, Neuron 101, 21 (2019).
- D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, Functional imaging of hippocampal place cells at cellular resolution during virtual navigation, Nat. Neurosci. 13, 1433 (2010).
- L. Tian, J. Akerboom, E. R. Schreiter, and L. L. Looger, Neural activity imaging with genetically encoded calcium indicators, Prog. Brain Res. 196, 79 (2012).
- J. Demas, J. Manley, F. Tejera, K. Barber, H. Kim, F. M. Traub, B. Chen, and A. Vaziri, High-speed, cortex-wide volumetric recording of neuroactivity at cellular resolution using light beads microscopy, Nat. Methods 18, 1103 (2021).
- N. A. Steinmetz, C. Aydin, A. Lebedeva, M. Okun, M. Pachitariu, M. Bauza, M. Beau, J. Bhagat, C. Böhm, M. Broux et al., Neuropixels 2.0: A miniaturized high-density probe for stable, long-term brain recordings, Science 372, eabf4588 (2021).
- H. C. Nguyen, R. Zecchina, and J. Berg, Inverse statistical problems: From the inverse Ising problem to data science, Adv. Phys. 66, 197 (2017).
- E. Schneidman, M. J. Berry II, R. Segev, and W. Bialek, Weak pairwise correlations imply strongly correlated network states in a neural population, Nature (London) 440, 1007 (2006).
- L. Meshulam, J. L. Gauthier, C. D. Brody, D. W. Tank, and W. Bialek, Collective behavior of place and non-place neurons in the hippocampal network, Neuron 96, 1178 (2017).
- L. Meshulam, J. L. Gauthier, C. D. Brody, D. W. Tank, and W. Bialek, Successes and failures of simplified models for a network of real neurons, arXiv:2112.14735.
- T. R. Lezon, J. R. Banavar, M. Cieplak, A. Maritan, and N. V. Fedoroff, Using the principle of entropy maximization to infer genetic interaction networks from gene expression patterns, Proc. Natl. Acad. Sci. USA 103, 19033 (2006).
- M. Weigt, R. A. White, H. Szurmant, J. A. Hoch, and T. Hwa, Identification of direct residue contacts in protein–protein interaction by message passing, Proc. Natl. Acad. Sci. USA 106, 67 (2009).
- D. S. Marks, L. J. Colwell, R. Sheridan, T. A. Hopf, A. Pagnani, R. Zecchina, and C. Sander, Protein 3D structure computed from evolutionary sequence variation, PLoS One 6, e28766 (2011).
- A. Lapedes, B. Giraud, and C. Jarzynski, Using sequence alignments to predict protein structure and stability with high accuracy, arXiv:1207.2484.
- W. Bialek, A. Cavagna, I. Giardina, T. Mora, E. Silvestri, M. Viale, and A. M. Walczak, Statistical mechanics for natural flocks of birds, Proc. Natl. Acad. Sci. USA 109, 4786 (2012).
- W. P. Russ, M. Figliuzzi, C. Stocker, P. Barrat-Charlaix, M. Socolich, P. Kast, D. Hilvert, R. Monasson, S. Cocco, M. Weigt et al., An evolution-based model for designing chorismate mutase enzymes, Science 369, 440 (2020).
- C. W. Lynn, L. Papadopoulos, D. D. Lee, and D. S. Bassett, Surges of collective human activity emerge from simple pairwise correlations, Phys. Rev. X 9, 011022 (2019).
- C. E. Shannon, A mathematical theory of communication, Bell Syst. Tech. J. 27, 379 (1948).
- E. T. Jaynes, Information theory and statistical mechanics, Phys. Rev. 106, 620 (1957).
- S. C. Zhu, Y. N. Wu, and D. Mumford, Minimax entropy principle and its application to texture modeling, Neural Comput. 9, 1627 (1997).
- E. Schneidman, S. Still, M. J. Berry II, and W. Bialek, Network information and connected correlations, Phys. Rev. Lett. 91, 238701 (2003).
- J. P. Sethna, Statistical Mechanics: Entropy, Order Parameters, and Complexity (Oxford University Press, USA, 2021), Vol. 14.
- C. Chow and C. Liu, Approximating discrete probability distributions with dependence trees, IEEE Trans. Inf. Theor. 14, 462 (1968).
- C. Moore and S. Mertens, The Nature of Computation (Oxford University Press, Oxford, 2011).
- C. W. Lynn, Q. Yu, R. Pang, S. E. Palmer, and W. Bialek, companion paper, Exact minimax entropy models of large-scale neuronal activity, Phys. Rev. E 111, 054411 (2025).
- J. L. Gauthier and D. W. Tank, A dedicated population for reward coding in the hippocampus, Neuron 99, 179 (2018).
- J. O'Keefe and D. H. Conway, Hippocampal place units in the freely moving rat: Why they fire where they fire, Exp. Brain Res. 31, 573 (1978).
- J. O'Keefe and L. Nadel, The Hippocampus as a Cognitive Map (Oxford University Press, 1978).
- L. T. Thompson and P. J. Best, Place cells and silent cells in the hippocampus of freely-behaving rats, J. Neurosci. 9, 2382 (1989).
- S. Leutgeb, J. K. Leutgeb, A. Treves, M.-B. Moser, and E. I. Moser, Distinct ensemble codes in hippocampal areas CA3 and CA1, Science 305, 1295 (2004).
- M. C. Fuhs and D. S. Touretzky, A spin glass model of path integration in rat medial entorhinal cortex, J. Neurosci. 26, 4266 (2006).
- S. Káli and P. Dayan, The involvement of recurrent connections in area Ca3 in establishing the properties of place fields: A model, J. Neurosci. 20, 7463 (2000).
- A. Samsonovich and B. L. McNaughton, Path integration and cognitive mapping in a continuous attractor neural network model, J. Neurosci. 17, 5900 (1997).
- G. Tkačik, T. Mora, O. Marre, D. Amodei, S. E. Palmer, M. J. Berry II, and W. Bialek, Thermodynamics and signatures of criticality in a network of neurons, Proc. Natl. Acad. Sci. USA 112, 11508 (2015).
- D. Sherrington and S. Kirkpatrick, Solvable model of a spin-glass, Phys. Rev. Lett. 35, 1792 (1975).
- C. W. Lynn, C. M. Holmes, and S. E. Palmer, Heavy-tailed neuronal connectivity arises from Hebbian self-organization, Nat. Phys. 20, 484 (2024).