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Role of interneuronal systems in the formation of main patterns of field electrical activity in the hippocampus

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Abstract

Studies on the cellular and subcellular levels promote elucidation of the fundamental principles of formation of effective neuronal systems from cell units. To estimate the interrelations between electrical activity of neuronal networks and processes realized on the cellular level, we need to adequately understand the general patterns of behavior of populations of interneurons, which are components of these networks, under different physiological conditions. In this review, we describe and discuss the relations between the electrical activity of single hippocampal neurons and different components of the field electrical activity, as well as modern concepts on the mode of involvement of the system of hippocampal interneurons in the formation of physiologically important patterns of efferent activity of the above-mentioned structure (in particular in encoding of information on the neuronal level).

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References

  1. J. Csicsvari, H. Hirase, A. Czurko, et al., “Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat,” J. Neurosci., 19, 274–287 (1999).

    PubMed  CAS  Google Scholar 

  2. C. J. Price, B. Cauli, E. R. Kovacs, et al., “Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area,” J. Neurosci., 25, 6775–6786 (2005).

    Article  PubMed  CAS  Google Scholar 

  3. H. Hirase, X. Leinekugel, J. Csicsvari, et al., “Behavior-dependent states of the hippocampal network affect functional clustering of neurons,” J. Neurosci., 21, RC145 (2001).

    PubMed  CAS  Google Scholar 

  4. G. Silberberg and H. Markram, “Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells,” Neuron, 53, 735–746 (2007).

    Article  PubMed  CAS  Google Scholar 

  5. J. Csicsvari, H. Hirase, A. Czurko, and G. Buzsaki, “Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat,” Neuron, 21, 179–189 (1998).

    Article  PubMed  CAS  Google Scholar 

  6. J. Csicsvari, H. Hirase, A. Czurko, et al., “Fast network oscillations in the hippocampal CA1 region of the behaving rat,” J. Neurosci., 19, RC20 (1999).

    PubMed  CAS  Google Scholar 

  7. P. Bartho, H. Hirase, L. Monconduit, et al., “Characterization of neocortical principal cells and interneurons by network interactions and extracellular features,” J. Neurophysiol., 92, 600–608 (2004).

    Article  PubMed  Google Scholar 

  8. H. Markram, M. Toledo-Rodriguez, Y. Wang, et al., “Interneurons of the neocortical inhibitory system,” Nature Rev. Neurosci., 5, 793–807 (2004).

    Article  CAS  Google Scholar 

  9. M. Beierlein, J. R. Gibson, and B. W. Connors, “Two dynamically distinct inhibitory networks in layer 4 of the neocortex,” J. Neurophysiol., 90, 2987–3000 (2003).

    Article  PubMed  Google Scholar 

  10. G. Silberberg and H. Markram, “Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells,” Neuron, 53, 735–746 (2007).

    Article  PubMed  CAS  Google Scholar 

  11. B. Haider, A. Duque, A. R. Hasenstaub, and D. A. McCormick, “Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition,” J. Neurosci., 26, 4535–4545 (2006).

    Article  PubMed  CAS  Google Scholar 

  12. P. Somogyi and T. Klausberger, “Defined types of cortical interneuron structure space and spike timing in the hippocampus,” J. Physiol., 562, 9–26 (2005).

    Article  PubMed  CAS  Google Scholar 

  13. J. Huxter, N. Burgess, and J. O’Keefe, “Independent rate and temporal coding in hippocampal pyramidal cells,” Nature, 425, 828–832 (2003).

    Article  PubMed  CAS  Google Scholar 

  14. G. Buzsaki, D. L. Buhl, K. D. Harris, et al., “Hippocampal network patterns of activity in the mouse,” Neuroscience, 116, 201–211 (2003).

    Article  PubMed  CAS  Google Scholar 

  15. S. Grillner, H. Markram, E. De Schutter, et al., “Microcircuits in action — from CPGs to neocortex,” Trends Neurosci., 28, 525–533 (2005).

    Article  PubMed  CAS  Google Scholar 

  16. D. L. Buhl and G. Buzsaki, “Developmental emergence of hippocampal fast-field ‘ripple’ oscillations in the behaving rat pups,” Neuroscience, 134, 1423–1430 (2005).

    Article  PubMed  CAS  Google Scholar 

  17. X. Leinekugel, R. Khazipov, R. Cannon, et al., “Correlated bursts of activity in the neonatal hippocampus in vivo,” Science, 296, 2049–2052 (2002).

    Article  PubMed  CAS  Google Scholar 

  18. T. T. Hahn, B. Sakmann, and M. R. Mehta, “Phase-locking of hippocampal interneurons’ membrane potential to neocortical up-down states,” Nature Neurosci., 9, 1359–1361 (2006).

    Article  PubMed  CAS  Google Scholar 

  19. Y. Isomura, A. Sirota, S. Ozen, et al., “Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations,” Neuron, 52, 871–882 (2006).

    Article  PubMed  CAS  Google Scholar 

  20. A. Luczak, P. Bartho, S. L. Marguet, et al., “Sequential structure of neocortical spontaneous activity in vivo,” Proc. Natl. Acad. Sci. USA, 104, 347–352 (2007).

    Article  PubMed  CAS  Google Scholar 

  21. V. Ego-Stengel and M. A. Wilson, “Spatial selectivity and theta phase precession in CA1 interneurons,” Hippocampus, 17, 161–174 (2007).

    Article  PubMed  Google Scholar 

  22. F. P. Battaglia, G. R. Sutherland, and B. L. McNaughton, “Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions,” Learning Memory, 11, 697–704 (2004).

    Article  PubMed  Google Scholar 

  23. Y. Ben-Ari, “Basic developmental rules and their implications for epilepsy in the immature brain,” Epileptic Disord., 8, 91–102 (2006).

    PubMed  Google Scholar 

  24. I. L. Hanganu, Y. Ben-Ari, and R. Khazipov, “Retinal waves trigger spindle bursts in the neonatal rat visual cortex,” J. Neurosci., 26, 6728–6736 (2006).

    Article  PubMed  CAS  Google Scholar 

  25. R. Khazipov, A. Sirota, X. Leinekugel, et al., “Early motor activity drives spindle bursts in the developing somatosensory cortex,” Nature, 432, 758–761 (2004).

    Article  PubMed  CAS  Google Scholar 

  26. T. Klausberger, L. F. Marton, A. Baude, et al., “Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo,” Nature Neurosci., 7, 41–47 (2004).

    Article  PubMed  CAS  Google Scholar 

  27. T. Klausberger, P. J. Magill, L. F. Marton, et al., “Brain-state-and cell-type-specific firing of hippocampal interneurons in vivo,” Nature, 421, 844–848 (2003).

    Article  PubMed  CAS  Google Scholar 

  28. T. Klausberger, L. F. Marton, J. O’Neill, et al., “Complementary roles of cholecystokinin-and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations,” J. Neurosci., 25, 9782–9793 (2005).

    Article  PubMed  CAS  Google Scholar 

  29. D. Robbe, S. M. Montgomery, A. Thome, et al., “Cannabinoids reveal importance of spike timing coordination in hippocampal function,” Nature Neurosci., 9, 1526–1533 (2006).

    Article  PubMed  CAS  Google Scholar 

  30. M. Bartos, I. Vida, and P. Jonas, “Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks,” Nature Rev. Neurosci., 8, 45–56 (2007).

    Article  CAS  Google Scholar 

  31. R. D. Traub, A. Bibbig, F. E. LeBeau, et al., “Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro,” Annu. Rev. Neurosci., 27, 247–278 (2004).

    Article  PubMed  CAS  Google Scholar 

  32. I. Soltesz, Diversity in the Neuronal Machine: Order and Variability in Interneuronal Microcircuits, Oxford Univ. Press, Oxford (2005).

    Google Scholar 

  33. Y. Ben-Ari, I. Khalilov, A. Represa, and H. Gozlan, “Interneurons set the tune of developing networks,” Trends Neurosci., 27, 422–427 (2004).

    Article  PubMed  CAS  Google Scholar 

  34. Handbook of Brain Theory and Neural Networks, M. A. Arbib (ed.), The MIT Press, Boston (2003).

    Google Scholar 

  35. H. Tamura, H. Kaneko, K. Kawasaki, and I. Fujita, “Presumed inhibitory neurons in the macaque inferior temporal cortex: visual response properties and functional interactions with adjacent neurons,” J. Neurophysiol., 91, 2782–2796 (2004).

    Article  PubMed  Google Scholar 

  36. A. P. Maurer, S. L. Cowen, S. N. Burke, et al., “Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells,” J. Neurosci., 26, 13485–13492 (2006).

    Article  PubMed  CAS  Google Scholar 

  37. L. Lin, R. Osan, S. Shoham, et al., “Identification of network-level coding units for real-time representation of episodic experiences in the hippocampus,” Proc. Natl. Acad. Sci. USA, 102, 6125–6130 (2005).

    Article  PubMed  CAS  Google Scholar 

  38. R. I. Wilson and G. Laurent, “Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe,” J. Neurosci., 25, 9069–9079 (2005).

    Article  PubMed  CAS  Google Scholar 

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Correspondence to O. A. Markova.

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Neirofiziologiya/Neurophysiology, Vol. 40, No. 1, pp. 58–68, January–February, 2008.

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Markova, O.A., Tsugorka, T.M., Dovgan’, O.V. et al. Role of interneuronal systems in the formation of main patterns of field electrical activity in the hippocampus. Neurophysiology 40, 53–63 (2008). https://doi.org/10.1007/s11062-008-9014-7

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  • DOI: https://doi.org/10.1007/s11062-008-9014-7

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