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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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).
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).
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).
G. Silberberg and H. Markram, “Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells,” Neuron, 53, 735–746 (2007).
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).
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).
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).
H. Markram, M. Toledo-Rodriguez, Y. Wang, et al., “Interneurons of the neocortical inhibitory system,” Nature Rev. Neurosci., 5, 793–807 (2004).
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).
G. Silberberg and H. Markram, “Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells,” Neuron, 53, 735–746 (2007).
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).
P. Somogyi and T. Klausberger, “Defined types of cortical interneuron structure space and spike timing in the hippocampus,” J. Physiol., 562, 9–26 (2005).
J. Huxter, N. Burgess, and J. O’Keefe, “Independent rate and temporal coding in hippocampal pyramidal cells,” Nature, 425, 828–832 (2003).
G. Buzsaki, D. L. Buhl, K. D. Harris, et al., “Hippocampal network patterns of activity in the mouse,” Neuroscience, 116, 201–211 (2003).
S. Grillner, H. Markram, E. De Schutter, et al., “Microcircuits in action — from CPGs to neocortex,” Trends Neurosci., 28, 525–533 (2005).
D. L. Buhl and G. Buzsaki, “Developmental emergence of hippocampal fast-field ‘ripple’ oscillations in the behaving rat pups,” Neuroscience, 134, 1423–1430 (2005).
X. Leinekugel, R. Khazipov, R. Cannon, et al., “Correlated bursts of activity in the neonatal hippocampus in vivo,” Science, 296, 2049–2052 (2002).
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).
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).
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).
V. Ego-Stengel and M. A. Wilson, “Spatial selectivity and theta phase precession in CA1 interneurons,” Hippocampus, 17, 161–174 (2007).
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).
Y. Ben-Ari, “Basic developmental rules and their implications for epilepsy in the immature brain,” Epileptic Disord., 8, 91–102 (2006).
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).
R. Khazipov, A. Sirota, X. Leinekugel, et al., “Early motor activity drives spindle bursts in the developing somatosensory cortex,” Nature, 432, 758–761 (2004).
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).
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).
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).
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).
M. Bartos, I. Vida, and P. Jonas, “Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks,” Nature Rev. Neurosci., 8, 45–56 (2007).
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).
I. Soltesz, Diversity in the Neuronal Machine: Order and Variability in Interneuronal Microcircuits, Oxford Univ. Press, Oxford (2005).
Y. Ben-Ari, I. Khalilov, A. Represa, and H. Gozlan, “Interneurons set the tune of developing networks,” Trends Neurosci., 27, 422–427 (2004).
Handbook of Brain Theory and Neural Networks, M. A. Arbib (ed.), The MIT Press, Boston (2003).
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).
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).
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).
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).
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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