Export citation

Export citation

Choose format for download:

Download Citation
  • Access by Xinjiang University

Prospective coding and path integration emerge as equilibrium solutions of self-organizing neural networks with firing-rate adaptation

Facundo Emina1,2,* and Emilio Kropff2,†

  • *Contact author: femina@leloir.org.ar
  • †Contact author: ekropff@leloir.org.ar

Phys. Rev. E 114, 054405 – Published 12 November, 2026

DOI: https://doi.org/10.1103/syk9-5c24

Abstract

Continuous attractor neural networks traditionally rely on prewired recurrent connectivity to model spatial representations, path integration, and anticipatory dynamics. However, the biological mechanisms through which this structured connectivity emerges via learning remain relatively unexplored. This work presents a theoretical framework revealing how continuous attractor connectivity and its computational properties self-organize through Hebbian plasticity, firing-rate adaptation, and global inhibition. We show that translationally invariant inputs naturally drive the emergence of stable, Gaussian-profiled feedforward weights. Crucially, anticipatory dynamics arise spontaneously within these feedforward architectures, shifting the activity bump forward without requiring recurrent excitatory collaterals. This predictive shift can be linearly amplified across multilayer networks, consistent with anticipatory activity observed in the superficial layers of the entorhinal cortex. Furthermore, introducing recurrent interactions allows the network to learn connections capable of self-sustaining a moving bump of activity. Finally, by modulating the network with an external, time-varying baseline current that encodes speed, the system adjusts its intrinsic velocity to function as a precise unidirectional path integrator. Ultimately, this study suggests that prospective coding and path integration are not manually engineered features, but rather naturally coemergent properties of a single self-organizing competitive network.

Physics Subject Headings (PhySH)

Article Text

References (45)

  1. J. J. Hopfield, Neural networks and physical systems with emergent collective computational abilities, Proc. Natl. Acad. Sci. USA 79, 2554 (1982).
  2. F. P. Battaglia and A. Treves, Attractor neural networks storing multiple space representations: A model for hippocampal place fields, Phys. Rev. E 58, 7738 (1998).
  3. Y. Burak and I. R. Fiete, Accurate path integration in continuous attractor network models of grid cells, PLoS Comput. Biol. 5, e1000291 (2009).
  4. W. E. Skaggs, J. J. Knierim, H. S. Kudrimoti, and B. L. McNaughton, A model of the neural basis of the rat's sense of direction, Adv. Neural Inf. Process. Syst. 7, 173 (1995).
  5. A. D. Redish, A. N. Elga, and D. S. Touretzky, A coupled attractor model of the rodent head direction system, Netw. Comput. Neural Syst. 7, 671 (1996).
  6. R. Nijhawan and S. Wu, Compensating time delays with neural predictions: Are predictions sensory or motor? Philos. Trans. R. Soc. A 367, 1063 (2009).
  7. J.-R. Duhamel, C. L. Colby, and M. E. Goldberg, The updating of the representation of visual space in parietal cortex by intended eye movements, Science 255, 90 (1992).
  8. M. J. Berry, I. H. Brivanlou, T. A. Jordan, and M. Meister, Anticipation of moving stimuli by the retina, Nature (London) 398, 334 (1999).
  9. D. N. Lee and P. E. Reddish, Plummeting gannets: A paradigm of ecological optics, Nature (London) 293, 293 (1981).
  10. H. T. Blair and P. E. Sharp, Anticipatory head direction signals in anterior thalamus: Evidence for a thalamocortical circuit that integrates angular head motion to compute head direction, J. Neurosci. 15, 6260 (1995).
  11. P. E. Sharp, A. Tinkelman, and J. Cho, Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: Implications for path integration in the head direction cell circuit, Behav. Neurosci. 115, 571 (2001).
  12. B. L. McNaughton, F. P. Battaglia, O. Jensen, E. I. Moser, and M.-B. Moser, Path integration and the neural basis of the ‘cognitive map', Nat. Rev. Neurosci. 7, 663 (2006).
  13. M. Gil, M. Ancau, M. I. Schlesiger, A. Neitz, K. Allen, R. J. De Marco, and H. Monyer, Impaired path integration in mice with disrupted grid cell firing, Nat. Neurosci. 21, 81 (2018).
  14. E. Kropff, J. E. Carmichael, M.-B. Moser, and E. I. Moser, Speed cells in the medial entorhinal cortex, Nature (London) 523, 419 (2015).
  15. F. Sargolini, M. Fyhn, T. Hafting, B. L. McNaughton, M. P. Witter, M.-B. Moser, and E. I. Moser, Conjunctive representation of position, direction, and velocity in entorhinal cortex, Science 312, 758 (2006).
  16. I. Zutshi, M. L. Fu, V. Lilascharoen, J. K. Leutgeb, B. K. Lim, and S. Leutgeb, Recurrent circuits within medial entorhinal cortex superficial layers support grid cell firing, Nat. Commun. 9, 3701 (2018).
  17. Ø. A. Høydal, E. R. Skytøen, S. O. Andersson, M.-B. Moser, and E. I. Moser, Object-vector coding in the medial entorhinal cortex, Nature (London) 568, 400 (2019).
  18. T. Solstad, C. N. Boccara, E. Kropff, M.-B. Moser, and E. I. Moser, Representation of geometric borders in the entorhinal cortex, Science 322, 1865 (2008).
  19. A. Ouchi and S. Fujisawa, Predictive grid coding in the medial entorhinal cortex, Science 385, 776 (2024).
  20. Y. Mi, C. Fung, K. Wong, and S. Wu, Spike frequency adaptation implements anticipative tracking in continuous attractor neural networks, Adv. Neural Inf. Process. Syst. 27, 505 (2014).
  21. L. Yu, T. Chu, Z. Zhao, Y. Mi, Y. Yang, and S. Wu, Spiking continuous attractor neural networks with spike frequency adaptation for anticipative tracking, in Proceedings of the 2019 IEEE International Workshop on Future Computing (IWOFC) (IEEE, New York, 2019), pp. 1–3.
  22. Y. Li, T. Chu, and S. Wu, Dynamics of continuous attractor neural networks with spike frequency adaptation, Neural Comput. 37, 1057 (2025).
  23. D. Spalla, I. M. Cornacchia, and A. Treves, Continuous attractors for dynamic memories, eLife 10, e69499 (2021).
  24. W. Zhang and S. Wu, Neural information processing with feedback modulations, Neural Comput. 24, 1695 (2012).
  25. M. Yan, W.-H. Zhang, H. Wang, and K. Y. M. Wong, Bimodular continuous attractor neural networks with static and moving stimuli, Phys. Rev. E 107, 064302 (2023).
  26. S. Deneve, P. E. Latham, and A. Pouget, Reading population codes: A neural implementation of ideal observers, Nat. Neurosci. 2, 740 (1999).
  27. S. Wu, S.-I. Amari, and H. Nakahara, Population coding and decoding in a neural field: A computational study, Neural Comput. 14, 999 (2002).
  28. C. A. Fung, K. M. Wong, and S. Wu, Dynamics of neural networks with continuous attractors, Europhys. Lett. 84, 18002 (2008).
  29. C. A. Fung, K. M. Wong, and S. Wu, A moving bump in a continuous manifold: A comprehensive study of the tracking dynamics of continuous attractor neural networks, Neural Comput. 22, 752 (2010).
  30. P. Földiák, Learning invariance from transformation sequences, Neural Comput. 3, 194 (1991).
  31. P. E. Sharp, Computer simulation of hippocampal place cells, Psychobiology 19, 103 (1991).
  32. M. C. Fuhs and D. S. Touretzky, A spin glass model of path integration in rat medial entorhinal cortex, J. Neurosci. 26, 4266 (2006).
  33. E. Kropff and A. Treves, The emergence of grid cells: Intelligent design or just adaptation? Hippocampus 18, 1256 (2008).
  34. J. Widloski and I. R. Fiete, A model of grid cell development through spatial exploration and spike time-dependent plasticity, Neuron 83, 481 (2014).
  35. S. M. Stringer, E. T. Rolls, T. P. Trappenberg, and I. E. T. de Araujo, Self-organizing continuous attractor networks and motor function, Neural Networks 16, 161 (2003).
  36. P. Vafidis, D. Owald, T. D'Albis, and R. Kempter, Learning accurate path integration in ring attractor models of the head direction system, eLife 11, e69841 (2022).
  37. A. Treves, Computational constraints between retrieving the past and predicting the future, and the CA3-CA1 differentiation, Hippocampus 14, 539 (2004).
  38. A. Dhillon and R. S. Jones, Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro, Neuroscience 99, 413 (2000).
  39. J. J. Couey, A. Witoelar, S.-J. Zhang, K. Zheng, J. Ye, B. Dunn, R. Czajkowski, M.-B. Moser, E. I. Moser, Y. Roudi, and M. P. Witter, Recurrent inhibitory circuitry as a mechanism for grid formation, Nat. Neurosci. 16, 318 (2013).
  40. H. Pastoll, L. Solanka, M. W. vanRossum, and M. Nolan, Feedback inhibition enables theta-nested gamma oscillations and grid firing fields, Neuron 77, 141 (2013).
  41. J. Basu and S. A. Siegelbaum, The corticohippocampal circuit, synaptic plasticity, and memory, Cold Spring Harbor Perspect. Biol. 7, a021733 (2015).
  42. E. Park, D. Dvorak, and A. A. Fenton, Ensemble place codes in hippocampus: CA1, CA3, and dentate gyrus place cells have multiple place fields in large environments, PLoS ONE 6, e22349 (2011).
  43. T. Eliav, S. R. Maimon, J. Aljadeff, M. Tsodyks, G. Ginosar, L. Las, and N. Ulanovsky, Multiscale representation of very large environments in the hippocampus of flying bats, Science 372, eabg4020 (2021).
  44. N. Mainali, R. Azeredo da Silveira, and Y. Burak, Universal statistics of hippocampal place fields across species and dimensionalities, Neuron 113, 1110 (2025).
  45. F. Schönsberg, R. Monasson, and A. Treves, Continuous quasi-attractors dissolve with too much—or too little—variability, PNAS Nexus 3, pgae525 (2024).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation