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Neurophysiology

, Volume 40, Issue 1, pp 53–63 | Cite as

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

  • O. A. Markova
  • T. M. Tsugorka
  • O. V. Dovgan’
  • A. R. Stepanyuk
  • V. P. Cherkas
Reviews
  • 31 Downloads

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).

Keywords

electrical activity of interneurons types of interneurons field electrical activity principles of neuronal encoding 

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References

  1. 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).PubMedGoogle Scholar
  2. 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).PubMedCrossRefGoogle Scholar
  3. 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).PubMedGoogle Scholar
  4. 4.
    G. Silberberg and H. Markram, “Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells,” Neuron, 53, 735–746 (2007).PubMedCrossRefGoogle Scholar
  5. 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).PubMedCrossRefGoogle Scholar
  6. 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).PubMedGoogle Scholar
  7. 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).PubMedCrossRefGoogle Scholar
  8. 8.
    H. Markram, M. Toledo-Rodriguez, Y. Wang, et al., “Interneurons of the neocortical inhibitory system,” Nature Rev. Neurosci., 5, 793–807 (2004).CrossRefGoogle Scholar
  9. 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).PubMedCrossRefGoogle Scholar
  10. 10.
    G. Silberberg and H. Markram, “Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells,” Neuron, 53, 735–746 (2007).PubMedCrossRefGoogle Scholar
  11. 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).PubMedCrossRefGoogle Scholar
  12. 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).PubMedCrossRefGoogle Scholar
  13. 13.
    J. Huxter, N. Burgess, and J. O’Keefe, “Independent rate and temporal coding in hippocampal pyramidal cells,” Nature, 425, 828–832 (2003).PubMedCrossRefGoogle Scholar
  14. 14.
    G. Buzsaki, D. L. Buhl, K. D. Harris, et al., “Hippocampal network patterns of activity in the mouse,” Neuroscience, 116, 201–211 (2003).PubMedCrossRefGoogle Scholar
  15. 15.
    S. Grillner, H. Markram, E. De Schutter, et al., “Microcircuits in action — from CPGs to neocortex,” Trends Neurosci., 28, 525–533 (2005).PubMedCrossRefGoogle Scholar
  16. 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).PubMedCrossRefGoogle Scholar
  17. 17.
    X. Leinekugel, R. Khazipov, R. Cannon, et al., “Correlated bursts of activity in the neonatal hippocampus in vivo,” Science, 296, 2049–2052 (2002).PubMedCrossRefGoogle Scholar
  18. 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).PubMedCrossRefGoogle Scholar
  19. 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).PubMedCrossRefGoogle Scholar
  20. 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).PubMedCrossRefGoogle Scholar
  21. 21.
    V. Ego-Stengel and M. A. Wilson, “Spatial selectivity and theta phase precession in CA1 interneurons,” Hippocampus, 17, 161–174 (2007).PubMedCrossRefGoogle Scholar
  22. 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).PubMedCrossRefGoogle Scholar
  23. 23.
    Y. Ben-Ari, “Basic developmental rules and their implications for epilepsy in the immature brain,” Epileptic Disord., 8, 91–102 (2006).PubMedGoogle Scholar
  24. 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).PubMedCrossRefGoogle Scholar
  25. 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).PubMedCrossRefGoogle Scholar
  26. 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).PubMedCrossRefGoogle Scholar
  27. 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).PubMedCrossRefGoogle Scholar
  28. 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).PubMedCrossRefGoogle Scholar
  29. 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).PubMedCrossRefGoogle Scholar
  30. 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).CrossRefGoogle Scholar
  31. 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).PubMedCrossRefGoogle Scholar
  32. 32.
    I. Soltesz, Diversity in the Neuronal Machine: Order and Variability in Interneuronal Microcircuits, Oxford Univ. Press, Oxford (2005).Google Scholar
  33. 33.
    Y. Ben-Ari, I. Khalilov, A. Represa, and H. Gozlan, “Interneurons set the tune of developing networks,” Trends Neurosci., 27, 422–427 (2004).PubMedCrossRefGoogle Scholar
  34. 34.
    Handbook of Brain Theory and Neural Networks, M. A. Arbib (ed.), The MIT Press, Boston (2003).Google Scholar
  35. 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).PubMedCrossRefGoogle Scholar
  36. 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).PubMedCrossRefGoogle Scholar
  37. 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).PubMedCrossRefGoogle Scholar
  38. 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).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2008

Authors and Affiliations

  • O. A. Markova
    • 1
    • 2
  • T. M. Tsugorka
    • 1
  • O. V. Dovgan’
    • 1
  • A. R. Stepanyuk
    • 1
  • V. P. Cherkas
    • 1
  1. 1.Bogomolets Institute of PhysiologyNational Academy of Sciences of UkraineKyivUkraine
  2. 2.Institut de Neurobiologie de la MediterraneeMarseilleFrance

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