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Hippocampal synchronization in a realistic CA1 neuron model

Alessandro Fiasconaro1,2,3,* and Michele Migliore3,†

  • *Contact author: afiascon@unizar.es
  • †Contact author: migliore@cnr.it
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Phys. Rev. E 110, 044406 – Published 25 October, 2024

DOI: https://doi.org/10.1103/PhysRevE.110.044406

Abstract

This work delves into studying the synchronization in two realistic neuron models using Hodgkin-Huxley dynamics. Unlike simplistic pointlike models, excitatory synapses are here randomly distributed along the dendrites, introducing strong stochastic contributions into their signal propagation. To focus on the role of different synaptic locations, we use two copies of the same neuron whose synapses are located at different distances from the soma and activated by identical Poisson distributed pulses. The synchronization is investigated through a specifically defined spiking correlation function, and its behavior is analyzed as a function of several parameters: inhibition weight, distance from the soma of one synaptic group, weight and decay time constants of the excitatory synapses.

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References (39)

  1. J. O'Keefe and M. L. Recce, Phase relationship between hippocampal place units and the EEG theta rhythm, Hippocampus 3, 317 (1993).
  2. P. Fries, Rhythms for cognition: Communication through coherence, Neuron 88, 220 (2015).
  3. Z. F. Mainen and T. J. Sejnowski, Reliability of spike timing in neocortical neurons, Science 268, 1503 (1995).
  4. J. E. Lisman and M. A. P. Idiart, Storage of 7 ± 2 short-term memories in oscillatory subcycles, Science 267, 1512 (1995).
  5. J. J. Hopfield, Pattern recognition computation using action potential timing for stimulus representation, Nature (Lond.) 376, 33 (1995).
  6. J. J. Hopfield and C. D. Brody, What is a moment? “Cortical” sensory integration over a brief interval, Proc. Natl. Acad. Sci. USA 97, 13919 (2000).
  7. Y. Kuramoto, Self-entrainment of a population of coupled nonlinear oscillators, Lect. Notes Phys. 39, 420 (1975).
  8. J. A. Acebrón, L. L. Bonilla, C. J. Pérez-Vicente, F. Ritort, and R. Spigler, The kuramoto model: A simple paradigm for synchronization phenomena, Rev. Mod. Phys. 77, 137 (2005).
  9. E. M. Izhikevich, Simple model of spiking neurons, IEEE Trans. Neural Netw. 14, 1569 (2003).
  10. L. F. Abbott, Lapicque's introduction of the integrate-and-fire model neuron (1907), Brain Res. Bull. 50, 303 (1999).
  11. R. Brette and W. Gerstner, Adaptive exponential integrate-and-fire model as an effective description of neuronal activity, J. Neurophysiol. 94, 3637 (2005).
  12. T. Górski, D. Depannemaecker, and A. Destexhe, Conductance-based adaptive exponential integrate-and-fire model, Neural Comput. 33, 41 (2021).
  13. A. Marasco, E. Spera, V. De Falco et al., An adaptive generalized leaky integrate-and-fire model for hippocampal ca1 pyramidal neurons and interneurons, Bull. Math. Biol. 85, 109 (2023).
  14. A. L. Hodgkin and A. F. Huxley, A quantitative description of membrane current and its application to conduction and excitation in nerve, J. Physiol. 117, 500 (1952).
  15. J. C. Magee, Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons, Nat. Neurosci. 2, 508 (1999).
  16. S. M. Crook, G. B. Ermentrout, and J. M. Bower, Dendritic and synaptic effects in systems of coupled cortical oscillators, J. Comput. Neurosci. 5, 315 (1998)
  17. R. Migliore, C. A. Lupascu, L. L. Bologna, A. Romani, J.-D. Courcol, S. Antonel et al., The physiological variability of channel density in hippocampal CA1 pyramidal cells and interneurons explored using a unified data-driven modeling workflow, PLoS Comput. Biol. 14, e1006423 (2018).
  18. C. Günay, J. R. Edgerton, and D. Jaeger, Channel density distributions explain spiking variability in the globus pallidus: A combined physiology and computer simulation database approach, J. Neurosci. 28, 7476 (2008).
  19. L. Li, N. Gervasi, and J. A. Girault, Dendritic geometry shapes neuronal cAMP signalling to the nucleus, Nat. Commun. 6, 6319 (2015).
  20. A. T. Gulledge, B. M. Kampa, and G. J. Stuart, Synaptic integration in dendritic trees, J. Neurophysiol. 64, 75 (2005).
  21. M. Migliore and G. M. Sheperd, Emerging rules for the distributions of active dendritic conductances, Nat. Rev. Neurosci. 3, 362 (2002).
  22. N. W. Schultheiss, J. R. Edgerton, and D. Jaeger, Phase response curve analysis of a full morphological globus pallidus neuron model reveals distinct perisomatic and dendritic modes of synaptic integration, J. Neurosci. 30, 2767 (2010).
  23. M. Lankarany, D. Al-Basha, S. Ratté, and S. A. Prescott, Differentially synchronized spiking enables multiplexed neural coding, Proc. Natl. Acad. Sci. USA 116, 10097 (2019).
  24. M. L. Hines and N. T. Carnevale, The NEURON simulation environment, Neural Comput. 9, 1179 (1997).
  25. G. A. Ascoli, S. Gasparini, V. Medinilla, and M. Migliore, Local control of postinhibitory rebound spiking in CA1 pyramidal neuron dendrites, J. Neurosci. 30, 6434 (2010).
  26. T. M. Morse, N. T. Carnevale, P. G. Mutalik, M. Migliore, and G. M. Shepherd, Abnormal excitability of oblique dendrites implicated in early Alzheimer's: A computational study, Front. Neural Circ. 4, 16 (2010).
  27. D. A. Hoffman and D. Johnston, Neuromodulation of dendritic action potentials, J. Neurophysiol. 81, 408 (1999).
  28. N. Spruston, Pyramidal neurons: Dendritic structure and synaptic integration, Nat. Rev. Neurosci. 9, 206 (2008).
  29. M. Bazhenov and M. Stopfer, Forward and back: Motifs of inhibition in olfactory processing, Neuron 67, 357 (2010).
  30. M. Megıás, Z. S. Emri, T. F. Freund, and A. I. Gulyás, Total number and distribution of inhibitory and excitatory synapses on hippocampal ca1 pyramidal cells, Neuroscience 102, 527 (2001).
  31. T. Pérez, G. C. Garcia, V. M. Eguíluz, R. Vicente, G. Pipa, and C. Mirasso, Effect of the topology and delayed interactions in neuronal networks synchronization, PLoS ONE 6, e19900 (2011).
  32. A. Pikovsky, M. Rosenblum, G. Osipov, and J. Kurths, Phase synchronization of chaotic oscillators by external driving, Physica D 104, 219 (1997).
  33. M. Migliore, M. Ferrante, and G. A. Ascoli, Signal propagation in oblique dendrites of CA1 pyramidal cells, J. Neurophysiol. 94, 4145 (2005).
  34. J. L. Noebels, M. Avoli, M. A. Rogawski, R. W. Olsen, and A. V. Delgado-Escueta, Jasper's Basic Mechanisms of the Epilepsies, Fourth Edition (Oxford University Press, New York, 2012), pp. 170–171.
  35. X.-J. Wang and G. Buzsáki, Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model, J. Neurosci. 16, 6402 (1996).
  36. C. Van Vreeswijk, L. F. Abbott, and G. B. Ermentrout, When inhibition not excitation synchronizes neural firing, J. Comput. Neurosci. 1, 313 (1994).
  37. N. Hájos and I. Mody, Synaptic communication among hippocampal interneurons: Properties of spontaneous ipscs in morphologically identified cells, J. Neurosci. 17, 8427 (1997).
  38. I. C. Kleppe and H. P. C. Robinson, Determining the activation time course of synaptic ampa receptors from openings of colocalized nmda receptors, Biophys. J. 77, 1418 (1999).
  39. M. Vargas-Caballero and H. P. C. Robinson, Fast and slow voltage-dependent dynamics of magnesium block in the nmda receptor: The asymmetric trapping block model, J. Neurosci. 24, 6171 (2004).

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Phys. Rev. E 110, 044406– Published 25 October, 2024
  • Received 15 February 2024
  • Revised 23 May 2024
  • Accepted 2 October 2024
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Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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