Neuronal Activity Patterns During Hippocampal Network Oscillations In Vitro

Part of the Springer Series in Computational Neuroscience book series (NEUROSCI, volume 5)

Abstract

Neurons form transient, functionally specialized assemblies by coordinating their activity within networks. Assembly activity is important for coding and information processing in the brain; oscillations are assumed to entrain and provide temporal structure to this. Recent work from different laboratories has uncovered cell type-specific activity patterns during network oscillations, indicating that the cells may differentially contribute to the generation of oscillation and thereby the coordination of cell assemblies. The purpose of this chapter is to summarize recent findings from these works in in vitro preparations highlighting the importance of different neuronal activity patterns of hippocampal principal cells and different subtypes of interneurons. Special attention will be paid to the role of the firing properties of hippocampal interneurons on the network oscillatory activity at the theta and gamma frequency range. Models based on these ideas are found in “Gamma and Theta Rhythms in Biophysical Models of Hippocampal Circuits” by Kopell et al., this book.

Keywords

Dopamine Serotonin Coherence Histamine Neurol 

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Further Reading

  1. Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Rev 29:83–120.PubMedGoogle Scholar
  2. Aponte Y, Lien CC, Reisinger E, Jonas P (2006) Hyperpolarization-activated cation channels in fast-spiking interneurons of rat hippocampus. J Physiol 574:229–243.PubMedGoogle Scholar
  3. Arabadzisz D, Antal K, Parpan F, Emri Z, Fritschy JM (2005) Epileptogenesis and chronic seizures in a mouse model of temporal lobe epilepsy are associated with distinct EEG patterns and selective neurochemical alterations in the contralateral hippocampus. Exp Neurol 194:76–90.PubMedGoogle Scholar
  4. Arnolds DE, Lopes da Silva FH, Aitink JW, Kamp A, Boeijinga, P (1980) The spectral properties of hippocampal EEG related to behaviour in man. Electroencephalogr Clin Neurophysiol 50:324–328.PubMedGoogle Scholar
  5. Arrang JM, Garbarg M, Schwartz JC (1983) Auto-inhibition of brain histamine release mediated by a novel class (H3) of histamine receptor. Nature (Lond) 302:832–837.Google Scholar
  6. Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403–450.PubMedGoogle Scholar
  7. Baldeweg T, Spence S, Hirsch SR, Gruzelier J (1998) Gamma-band electroencephalographic oscillations in a patient with somatic hallucinations. Lancet 352:620–621.PubMedGoogle Scholar
  8. Banks MI, White JA, Pearce RA (2000) Interactions between distinct GABA(A) circuits in hippocampus. Neuron 25:449–457.PubMedGoogle Scholar
  9. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687–2698.PubMedGoogle Scholar
  10. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99:13222–13227.PubMedGoogle Scholar
  11. Behrens CJ, van den Boom LP, de Hoz L, Friedman A, Heinemann U (2005) Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nat Neurosci 8:1560–1567.PubMedGoogle Scholar
  12. Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL, Dugan LL (2007) Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318:1645–1647.PubMedGoogle Scholar
  13. Berridge CW, Foote SL (1991) Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. J Neurosci 11:3135–3145.PubMedGoogle Scholar
  14. Bland BH (1986) Physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1–54.PubMedGoogle Scholar
  15. Both M, Bähner F, von Bohlen und Halbach O, Draguhn A (2008) Propagation of specific network patterns through the mouse hippocampus. Hippocampus 18:899–908.PubMedGoogle Scholar
  16. Bourdeau ML, Morin F, Laurent CE, Azzi M, Lacaille JC (2007) Kv4.3-mediated A-type K+ currents underlie rhythmic activity in hippocampal interneurons. J Neurosci 27:1942–1953.PubMedGoogle Scholar
  17. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268.PubMedGoogle Scholar
  18. Bragin A, Jandó G, Nádasdy Z, Hetke J, Wise K, Buzsáki G (1995) Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47–60.PubMedGoogle Scholar
  19. Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsáki G (1999) High-frequency oscillations in human brain. Hippocampus 9:137–142.PubMedGoogle Scholar
  20. Bragin A, Mody I, Wilson CL, Engel J Jr (2002) Local generation of fast ripples in epileptic brain. J Neurosci 22:2012–2021.PubMedGoogle Scholar
  21. Bragin A, Claeys P, Vonck K, Van Roost D, Wilson C, Boon P, Engel J Jr (2007) Analysis of initial slow waves (ISWs) at the seizure onset in patients with drug resistant temporal lobe epilepsy. Epilepsia 48:1883–1894.PubMedGoogle Scholar
  22. Braun I, Genius J, Grunze H, Bender A, Möller HJ, Rujescu D (2007) Alterations of hippocampal and prefrontal GABAergic interneurons in an animal model of psychosis induced by NMDA receptor antagonism. Schizophr Res 97:254–263.PubMedGoogle Scholar
  23. Brown RA, Walling SG, Milway JS, Harley CW (2005) Locus coeruleus activation suppresses feedforward interneurons and reduces β-γ electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus. J Neurosci 25:1985–1991.PubMedGoogle Scholar
  24. Bucci P, Mucci A, Merlotti E, Volpe U, Galderisi S (2007) Induced gamma activity and event-related coherence in schizophrenia. Clin EEG Neurosci 38:96–104.PubMedGoogle Scholar
  25. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823–828.PubMedGoogle Scholar
  26. Buhl EH, Tamás G, Fisahn A (1998) Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 513:117–126PubMedGoogle Scholar
  27. Buzsáki, G (1989) Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31:3551–3570.Google Scholar
  28. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340.PubMedGoogle Scholar
  29. Buzsáki G, Buhl DL, Harris KD, Csicsvari J, Czéh B, Morozov A (2003) Hippocampal network patterns of activity in the mouse. Neuroscience 116:201–211.PubMedGoogle Scholar
  30. Buzsáki G, Czopf J, Kondakor J, Kellenyi L (1986) Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat; current source density analysis, effects of urethane and atropine. Brain Res 365:125–137.PubMedGoogle Scholar
  31. Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929.PubMedGoogle Scholar
  32. Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027.PubMedGoogle Scholar
  33. Buzsaki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171.PubMedGoogle Scholar
  34. Callaway EM (2002) Cell type specificity of local cortical connections. J Neurocytol 31:231–237.PubMedGoogle Scholar
  35. Chen K, Aradi I, Santhakumar V, Soltesz I (2002) H-channels in epilepsy: new targets for seizure control? Trends Pharmacol Sci 23:552–557.PubMedGoogle Scholar
  36. Cho RY, Konecky RO, Carter CS (2006) Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci USA 103:19878–19883.PubMedGoogle Scholar
  37. Chrobak JJ, Buzsaki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056–3066.PubMedGoogle Scholar
  38. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronisation of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75–78.PubMedGoogle Scholar
  39. Cobb SR, Butlers DO, Davies CH (2000) Coincident activation of mGluRs and MAChRs imposes theta frequency patterning on synchronised network activity in the hippocampal CA3 region. Neuropharmacology 23:1933–1942.Google Scholar
  40. Colom LV, Garcia-Hernandez A, Castaneda MT, Perez-Cordova MG, Garrido-Sanabria ER (2006) Septo-hippocampal networks in chronically epileptic rats: potential antiepileptic effects of theta rhythm generation. J Neurophysiol 95:3645–3653.PubMedGoogle Scholar
  41. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y (1998) GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nature Neurosci 1:470–478.PubMedGoogle Scholar
  42. Cossart R, Epsztein J, Tyzio R, Becq H, Hirsch J, Ben-Ari Y, Crépel V (2002) Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 35:147–159PubMedGoogle Scholar
  43. Csicsvari J, Hirase H, Czurko’ A, Mamiya A, Buzsa’ki G (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274–287.PubMedGoogle Scholar
  44. Csicsvari J, Hirase H, Mamiya A, Buzsaki G (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28:585–594.PubMedGoogle Scholar
  45. Csicsvari J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322.PubMedGoogle Scholar
  46. Cunningham MO, Hunt J, Middleton S, LeBeau FE, Gillies MJ, Davies CH, Maycox PR, Whittington MA, Racca C (2006) Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness. J Neurosci 26:2767–2776.PubMedGoogle Scholar
  47. Deisseroth K, Feng G, Majewska AK, Miesenböck G, Ting A, Schnitzer MJ (2006) Next-generation optical technologies for illuminating genetically targeted brain circuits. J Neurosci 26:10380–10386.PubMedGoogle Scholar
  48. Dodt HU, Zieglgänsberger W (1994) Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci 17:453–458.PubMedGoogle Scholar
  49. Draguhn A, Traub RD, Schmitz D, Jefferys JG (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189–192.PubMedGoogle Scholar
  50. Dugladze T, Vida I, Tort AB, Gross A, Otahal J, Heinemann U, Kopell NJ, Gloveli T (2007) Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc Natl Acad Sci USA 104:17530–17535.PubMedGoogle Scholar
  51. Fellous JM, Sejnowski TJ (2000) Cholinergic induction of oscillations in the hippocampal slice in the slow bands (0.5–2 Hz), theta (5–12 Hz), and gamma (35–70 Hz). Hippocampus 10:187–197.PubMedGoogle Scholar
  52. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186–189.PubMedGoogle Scholar
  53. Fisahn A, Yamada M, Duttaroy A, Gan JW, Deng CX, McBain CJ, Wess J (2002) Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 33:615–624.PubMedGoogle Scholar
  54. Fisahn A, Contractor A, Traub RD, Buhl EH, Heinemann SF, McBain CJ (2004) Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci 24:9658–9668.PubMedGoogle Scholar
  55. Fisher RS, Webber WR, Lesser RP, Arroyo S, Uematsu S (1992) High-frequency EEG activity at the start of seizures. J Clin Neurophysiol 9:441–448.PubMedGoogle Scholar
  56. Ford JM, Krystal JH, Mathalon DH (2007) Neural synchrony in schizophrenia: from networks to new treatments. Schizophr Bull 33:848–852.PubMedGoogle Scholar
  57. Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1:479–486.PubMedGoogle Scholar
  58. Frerking M, Ohliger-Frerking P (2002) AMPA receptors and kainate receptors encode different features of afferent activity. J Neurosci 22:7434–7443.PubMedGoogle Scholar
  59. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470.PubMedGoogle Scholar
  60. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33–42.PubMedGoogle Scholar
  61. Foffani G, Uzcategui YG, Gal B, Menendez de la Prida L (2007) Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 55:930–941.PubMedGoogle Scholar
  62. Fuentealba P, Begum R, Capogna M, Jinno S, Márton LF, Csicsvari J, Thomson A, Somogyi P, Klausberger T (2008) Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 57:917–929.PubMedGoogle Scholar
  63. Galarreta M, Erdélyi F, Szabó G, Hestrin S (2008) Cannabinoid sensitivity and synaptic properties of 2 GABAergic networks in the neocortex. Cereb Cortex 18:2296–22305.PubMedGoogle Scholar
  64. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H (1995) Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193–204.PubMedGoogle Scholar
  65. Geiger JR, Lübke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009–1023.PubMedGoogle Scholar
  66. Gillies MJ, Traub RD, LeBeau FE, Davies CH, Gloveli T, Buhl EH, Whittington MA (2002) A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol (Lond) 543:779–793.Google Scholar
  67. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH (2005a) Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 562:131–147PubMedGoogle Scholar
  68. Gloveli T, Dugladze T, Rotstein HG, Traub RD, Monyer H, Heinemann U, Whittington MA, Kopell NJ (2005b) Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus. Proc Natl Acad Sci USA 102:13295–13300.PubMedGoogle Scholar
  69. Goldin M, Epsztein J, Jorquera I, Represa A, Ben-Ari Y, Crépel V, Cossart R (2007) Synaptic kainate receptors tune oriens-lacunosum moleculare interneurons to operate at theta frequency. J Neurosci 27:9560–9572.PubMedGoogle Scholar
  70. Gonzalez-Burgos G, Lewis DA (2008) GABA Neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr Bull 34:944–961.PubMedGoogle Scholar
  71. Gu N, Vervaeke K, Hu H, Storm JF (2005) Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566:689–715.PubMedGoogle Scholar
  72. Hájos N, Pálhalmi J, Mann EO, Németh B, Paulsen O, Freund TF (2004) Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci 24:9127–9137.PubMedGoogle Scholar
  73. Hajós M, Siok CJ, Hoffmann WE, Li S, Kocsis B (2008) Modulation of hippocampal theta oscillation by histamine H3 receptors. J Pharmacol Exp Ther 324:391–398.PubMedGoogle Scholar
  74. Halasy K, Buhl EH, Lörinczi Z, Tamás G, Somogyi P (1996) Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus. Hippocampus 6:306–329.PubMedGoogle Scholar
  75. Hu H, Vervaeke K, Storm JF (2002) Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells. J Physiol 545:783–805.PubMedGoogle Scholar
  76. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol 472:615–663.PubMedGoogle Scholar
  77. Jouvet M (1969) Biogenic amines and the states of sleep. Science 163:32–41.PubMedGoogle Scholar
  78. Kandel ER, Spencer WA (1961) Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. J Neurophysiol 24:243–259.PubMedGoogle Scholar
  79. Kehrer C, Dugladze T, Maziashvili N, Wójtowicz A, Schmitz D, Heinemann U, Gloveli T (2007) Increased inhibitory input to CA1 pyramidal cells alters hippocampal gamma frequency oscillations in the MK-801 model of acute psychosis. Neurobiol Dis 25:545–552.PubMedGoogle Scholar
  80. Kehrer C, Maziashvili N, Dugladze T, Gloveli T (2008) Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front Mol Neurosci 1:6.Google Scholar
  81. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57.PubMedGoogle Scholar
  82. Klausberger T, Magill PJ, Márton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844–848.PubMedGoogle Scholar
  83. Klausberger T, Márton LF, Baude A, Roberts JD, Magill PJ, Somogyi P (2004) Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41–47.PubMedGoogle Scholar
  84. Kocsis B, Varga V, Dahan L, Sik A (2006) Serotonergic neuron diversity: identification of raphe neurons with discharges time-locked to the hippocampal theta rhythm. Proc Natl Acad Sci USA 103:1059–1064.PubMedGoogle Scholar
  85. Kocsis B, Li S, Hajos M (2007) Behavior-dependent modulation of hippocampal EEG activity by the selective norepinephrine reuptake inhibitor reboxetine in rats. Hippocampus 17:627–633.PubMedGoogle Scholar
  86. Konopacki J, Gołebiewski H, Eckersdorf B (1992) Carbachol-induced rhythmic slow activity (theta) in cat hippocampal formation slices. Brain Res 578:13–16.PubMedGoogle Scholar
  87. Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ (2006) Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J Physiol 570:595–610PubMedGoogle Scholar
  88. LeBeau FEN, Towers SK, Traub RD, Whittington MA, Buhl EH (2002) Fast network oscillations induced by potassium transients in the rat hippocampus in vitro. J Physiol (Lond) 542:167–179.Google Scholar
  89. LeBeau FE, Traub RD, Monyer H, Whittington MA, Buhl EH (2003) The role of electrical signaling via gap junctions in the generation of fast network oscillations. Brain Res Bull 62:3–13.PubMedGoogle Scholar
  90. Lerma J (2003) Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4:481–495.PubMedGoogle Scholar
  91. Leung LW (1985) Spectral analysis of hippocampal EEG in the freely moving rat effects of centrally active drugs and relations to evoked potentials. Electroencephalogr Clin Neurophysiol 60:65–77.PubMedGoogle Scholar
  92. Leung LS, Yim CY (1986) Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res 367:323–327.PubMedGoogle Scholar
  93. Leung LS, Yu HW (1998) Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection. J Neurophysiol 79:1592–1596.PubMedGoogle Scholar
  94. Leung LS, Lopes da Silva F, Wadman WJ (1982) Spectral characteristics of the hippocampal EEG in the freely moving rat. Clin Neurophysiol 54:203–219.Google Scholar
  95. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312–324.PubMedGoogle Scholar
  96. Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208.PubMedGoogle Scholar
  97. Lisman JE (2005) The theta/gamma discrete phase code occurring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15:913–922.PubMedGoogle Scholar
  98. Lisman JE, Idiart MAP (1995) Storage of 7+– 2 short term memories in oscillatory subcycles. Science 267:1512–1515.PubMedGoogle Scholar
  99. Maccaferri G, McBain CJ (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497:119–130.PubMedGoogle Scholar
  100. Maccaferri G, Roberts JD, Szucs P, Cottingham CA, Somogyi P (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol 524:91–116.PubMedGoogle Scholar
  101. Madison DV, Lancaster B, Nicoll RA (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7:733–741.PubMedGoogle Scholar
  102. Magee JC (1999) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613–7624.Google Scholar
  103. Maier N, Nimmrich V, Draguhn A (2003) Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550:873–887.PubMedGoogle Scholar
  104. Mann EO, Suckling JM, Hajos N, Greenfield SA, Paulsen O (2005) Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45:105–117.PubMedGoogle Scholar
  105. Marek KW, Davis GW (2003) Controlling the active properties of excitable cells. Curr Opin Neurobiol 13:607–611.PubMedGoogle Scholar
  106. Markram H, Lubke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500:409–440.PubMedGoogle Scholar
  107. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11–23.PubMedGoogle Scholar
  108. Meyer AH, Katona I, Blatow M, Rozov A, Monyer H (2002) In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22:7055–7064.PubMedGoogle Scholar
  109. Middleton S, Jalics J, Kispersky T, Lebeau FE, Roopun AK, Kopell NJ, Whittington MA, Cunningham MO (2008) NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex. Proc Natl Acad Sci USA 105:18572–18577.PubMedGoogle Scholar
  110. Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol 428:61–77.PubMedGoogle Scholar
  111. Miles R, Poncer JC (1996) Paired recordings from neurones. Curr Opin Neurobiol 6:387–394.PubMedGoogle Scholar
  112. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815–823.PubMedGoogle Scholar
  113. Montplaisir J, Laverdiere M, Saint-Hilaire JM, Rouleau I (1987) Nocturnal sleep recording in partial epilepsy: a study with depth electrodes, J Clin Neurophysiol 4:383–388.PubMedCrossRefGoogle Scholar
  114. Morales M, Bloom FE (1997) The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17:3157–3167.PubMedGoogle Scholar
  115. Morales M, Battenberg E, Bloom F (1998) Distribution of neurons expressing immunoreactivity for the 5HT3 receptor subtype in the rat brain and spinal cord. J Comp Neurol 402:385–401.PubMedGoogle Scholar
  116. Morris HM, Hashimoto T, Lewis DA (2008) Alterations in somatostatin mRNA expression in the dorsolateral prefrontal cortex of subjects with schizophrenia or schizoaffective disorder. Cereb Cortex 18:1575–1587.PubMedGoogle Scholar
  117. Mulle C, Sailer A, Swanson GT, Brana C, O’Gorman S, Bettler B, Heinemann SF (2000) Subunit composition of kainate receptors in hippocampal interneurons. Neuron 28:475–484.PubMedGoogle Scholar
  118. Nimmrich V, Maier N, Schmitz D, Draguhn A (2005) Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. J Physiol 563:663–670.PubMedGoogle Scholar
  119. Notomi T, Shigemoto R (2004) Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol 471:241–276.PubMedGoogle Scholar
  120. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545–559.PubMedGoogle Scholar
  121. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20:3354–3368.PubMedGoogle Scholar
  122. O’Neill J, Senior T, Csicsvari J (2006) Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49:143–155.PubMedGoogle Scholar
  123. Oren I, Mann EO, Paulsen O, Hajos N (2006) Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro. J Neurosci 26:9923–9934.PubMedGoogle Scholar
  124. Pálhalmi J, Paulsen O, Freund TF, Hájos N (2004) Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices. Neuropharmacology 47:381–289.PubMedGoogle Scholar
  125. Penttonen M, Kamondi A, Acsády L, Buzsáki G (1998) Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci 10:718–728.PubMedGoogle Scholar
  126. Petsche H, Stumpf C, Gogolák G (1962) The significance of the rabbit’s septum as a relay station between midbrain and the hippocampus: I. The control of hippocampus arousal activity by the septum cells. Electroencephalogr Clin Neurophysiol 14:202–211.PubMedGoogle Scholar
  127. Pike FG, Goddard RS, Suckling JM, Ganter P, Kasthuri N, Paulsen O (2000) Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents. J Physiol 529:205–213.PubMedGoogle Scholar
  128. Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Methods 65:113–136.PubMedGoogle Scholar
  129. Pinault D (2008) N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex. Biol Psychiatry 63:730–735.PubMedGoogle Scholar
  130. Pitler TA, Alger BE (1992) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450:127–142.PubMedGoogle Scholar
  131. Polleux F (2005) Genetic mechanisms specifying cortical connectivity: let’s make some projections together. Neuron 46:395–400.PubMedGoogle Scholar
  132. Pöschel B, Draguhn A, Heinemann U (2002) Glutamate-induced gamma oscillations in the dentate gyrus of rat hippocampal slices. Brain Res 938:22–28.PubMedGoogle Scholar
  133. Pouille F, Scanziani M (2004) Routing of spike series by dynamic circuits in the hippocampus. Nature 429:717–723.PubMedGoogle Scholar
  134. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25:6775–6786.PubMedGoogle Scholar
  135. Roopun AK, Cunningham MO, Racca C, Alter K, Traub RD, Whittington MA (2008) Region-specific changes in gamma and beta2 rhythms in NMDA receptor dysfunction models of schizophrenia. Schizophr Bull 34:962–973.PubMedGoogle Scholar
  136. Ropert N, Guy N (1991) Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampus in vitro. J Physiol (Lond) 441:121–136.Google Scholar
  137. Rotstein HG, Pervouchine DD, Acker CD, Gillies MJ, White JA, Buhl EH, Whittington MA, Kopell N (2005) Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. J Neurophysiol 94:1509–1518.PubMedGoogle Scholar
  138. Sakai T, Oshima A, Nozaki Y, Ida I, Haga C, Akiyama H, Nakazato Y, Mikuni M (2008) Changes in density of calcium-binding-protein-immunoreactive GABAergic neurons in prefrontal cortex in schizophrenia and bipolar disorder. Neuropathology 28:143–150.PubMedGoogle Scholar
  139. Savić N, Pedarzani P, Sciancalepore M (2001) Medium afterhyperpolarization and firing pattern modulation in interneurons of stratum radiatum in the CA3 hippocampal region. J Neurophysiol 85:1986–1997.PubMedGoogle Scholar
  140. Schmitz D, Empson RM, Heinemann U (1995) Serotonin reduces inhibition via 5-HT1A receptors in area CA1 of rat hippocampal slices in vitro. J Neurosci 15:7217–7225.PubMedGoogle Scholar
  141. Schmitz D, Gloveli T, Empson RM, Heinemann U (1998) Comparison of the effects of serotonin in the hippocampus and the entorhinal cortex. Mol Neurobiol 17:59–72.PubMedGoogle Scholar
  142. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31:831–840.PubMedGoogle Scholar
  143. Shen RY, Andrade R (1998) 5-Hydroxytryptamine2 receptor facilitates GABAergic neurotransmission in rat hippocampus. J Pharmacol Exp Ther 285:805–12.PubMedGoogle Scholar
  144. Shimono K, Brucher F, Granger R, Lynch G, Taketani M (2000) Origins and distribution of cholinergically induced beta rhythms in hippocampal slices. J Neurosci 20:8462–8473.PubMedGoogle Scholar
  145. Sik A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651–6665.PubMedGoogle Scholar
  146. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49–65.PubMedGoogle Scholar
  147. Slewa-Younan S, Gordon E, Williams L, Haig AR, Goldberg E (2001) Sex differences, gamma activity and schizophrenia. Int J Neurosci 107:131–144.PubMedGoogle Scholar
  148. Somogyi P, Klausberger T (2005) Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol (Lond) 562:9–26.Google Scholar
  149. Spampanato J, Mody I (2007) Spike timing of lacunosum-moleculare targeting interneurons and CA3 pyramidal cells during high-frequency network oscillations in vitro. J Neurophysiol 98:96–104.PubMedGoogle Scholar
  150. Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW (2004) Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci USA 101:17288–17293.PubMedGoogle Scholar
  151. Spencer KM (2008) Visual gamma oscillations in schizophrenia: implications for understanding neural circuitry abnormalities. Clin EEG Neurosci 39:65–68.PubMedGoogle Scholar
  152. Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206–221.PubMedGoogle Scholar
  153. Szabadics J, Tamas G, Soltesz I (2007) Different transmitter transients underlie presynaptic cell type specificity of GABAA, slow and GABAA, fast. Proc Natl Acad Sci USA 104:14831–14836.PubMedGoogle Scholar
  154. Tecott LH, Maricq AV, Julius D (1993) Nervous system distribution of the serotonin 5-HT3 receptor mRNA. Proc Natl Acad Sci USA 90:1430–1434.PubMedGoogle Scholar
  155. Tesche CD, Karhu J (2000) Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci USA 97:919–924.PubMedGoogle Scholar
  156. Tort AB, Rotstein HG, Dugladze T, Gloveli T, Kopell NJ (2007) On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus. Proc Natl Acad Sci USA 104:13490–13495.PubMedGoogle Scholar
  157. Toth K, Suares G, Lawrence JJ, Philips-Tansey E, McBain CJ (2000) Differential mechanisms of transmission at three types of mossy fiber synapse. J Neurosci 20:8279–8289.PubMedGoogle Scholar
  158. Towers SK, LeBeau FE, Gloveli T, Traub RD, Whittington MA, Buhl EH (2002) Fast network oscillations in the rat dentate gyrus in vitro. J Neurophysiol 87:1165–1168.PubMedGoogle Scholar
  159. Traub RD, Bibbig A, Fisahn A, LeBeau FE, Whittington MA, Buhl EH (2000) A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur J Neurosci 12:4093–4106.PubMedGoogle Scholar
  160. Traub RD, Cunningham MO, Gloveli T, LeBeau FE, Bibbig A, Buhl EH, Whittington MA (2003) GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations. Proc Natl Acad Sci USA 100:11047–11052.PubMedGoogle Scholar
  161. Tukker JJ, Fuentealba P, Hartwich K, Somogyi P, Klausberger T (2007) Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo. J Neurosci 27:8184–8189.PubMedGoogle Scholar
  162. van Hooft JA, Giuffrida R, Blatow M, Monyer H (2000) Differential expression of group I metabotropic glutamate receptors in functionally distinct hippocampal interneurons. J Neurosci 20:3544–3551.PubMedGoogle Scholar
  163. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407–418.PubMedGoogle Scholar
  164. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH (1998) Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506:755–773.PubMedGoogle Scholar
  165. Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49:107–117.PubMedGoogle Scholar
  166. Vierling-Claassen D, Siekmeier P, Stufflebeam S, Kopell N (2008) Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. J Neurophysiol 99:2656–2671.PubMedGoogle Scholar
  167. Wang X-J, Buzsáki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16:6402–6413.PubMedGoogle Scholar
  168. Wang CZ, Yang SF, Xia Y, Johnson KM (2008) Postnatal phencyclidine administration selectively reduces adult cortical parvalbumin-containing interneurons. Neuropsychopharmacology 33:2442–2455.PubMedGoogle Scholar
  169. Weiss T, Veh RW, Heinemann U (2003) Dopamine depresses cholinergic oscillatory network activity in rat hippocampus. Eur J Neurosci 18:2573–2580.PubMedGoogle Scholar
  170. White JA, Chow CC, Ritt J, Soto-Treviño C, Kopell N (1998) Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons. J Comput Neurosci 5:5–16.PubMedGoogle Scholar
  171. Whittington MA, Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676–682.PubMedGoogle Scholar
  172. Whittington MA, Stanford IM, Colling SB, Jefferys JG, Traub RD (1997) Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol 502:591–607.PubMedGoogle Scholar
  173. Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612–615.PubMedGoogle Scholar
  174. Williams SR, Stuart GJ (2003) Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J Neurosci 23:7358–7367.PubMedGoogle Scholar
  175. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–679.PubMedGoogle Scholar
  176. Wittner L, Henze DA, Záborszky L, Buzsáki G (2007) Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct Funct 212:75–83.PubMedGoogle Scholar
  177. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsaki G (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30–46.PubMedGoogle Scholar
  178. Zhang ZJ, Reynolds GP (2002) A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr Res 55:1–10.PubMedGoogle Scholar
  179. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, Watzke N, Wood PG, Bamberg E, Nagel G, Gottschalk A, Deisseroth K (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446:633–639.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Institute of Neurophysiology, Charité – Universitätsmedizin BerlinBerlinGermany
  2. 2.Department of Mathematics and Center for BioDynamicsBoston UniversityBostonUSA

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