Cell Type-Specific Activity During Hippocampal Network Oscillations In Vitro

  • Tengis GloveliEmail author
  • Sam A. Booker
  • Nancy Kopell
  • Tamar DugladzeEmail author
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)


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.


  1. Amilhon B, Huh CY, Manseau F, Ducharme G, Nichol H, Adamantidis A, Williams S (2015) Parvalbumin interneurons of hippocampus tune population activity at theta frequency. Neuron 5:1277–1289CrossRefGoogle Scholar
  2. Andersson RH, Johnston A, Herman PA, Winzer-Serhan UH, Karavanova I, Vullhorst D, Fisahn A, Buonanno A (2012) Neuregulin and dopamine modulation of hippocampal gamma oscillations is dependent on dopamine D4 receptors. Proc Natl Acad Sci U S A 109:13118–13123PubMedPubMedCentralCrossRefGoogle Scholar
  3. Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Rev 29:83–120PubMedCrossRefGoogle Scholar
  4. Aponte Y, Lien CC, Reisinger E, Jonas P (2006) Hyperpolarization-activated cation channels in fast-spiking interneurons of rat hippocampus. J Physiol 574:229–243PubMedPubMedCentralCrossRefGoogle Scholar
  5. 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 194:76–90PubMedCrossRefGoogle Scholar
  6. 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 50:324–328PubMedCrossRefGoogle Scholar
  7. Arrang JM, Garbarg M, Schwartz JC (1983) Auto-inhibition of brain histamine release mediated by a novel class (H3) of histamine receptor. Nature (Lond) 302:832–837CrossRefGoogle Scholar
  8. Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403–450PubMedCrossRefGoogle Scholar
  9. Baldeweg T, Spence S, Hirsch SR, Gruzelier J (1998) Gamma-band electroencephalographic oscillations in a patient with somatic hallucinations. Lancet 352:620–621PubMedCrossRefGoogle Scholar
  10. Banks MI, White JA, Pearce RA (2000) Interactions between distinct GABA(A) circuits in hippocampus. Neuron 25:449–457PubMedCrossRefGoogle Scholar
  11. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687–2698PubMedPubMedCentralCrossRefGoogle Scholar
  12. 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 U S A 99:13222–13227PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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 8:1560–1567PubMedCrossRefGoogle Scholar
  14. 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 318:1645–1647PubMedCrossRefGoogle Scholar
  15. Berridge CW, Foote SL (1991) Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. J Neurosci 11:3135–3145PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bland BH (1986) Physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1–54PubMedCrossRefGoogle Scholar
  17. Booker SA, Vida I (2018) Morphological diversity and connectivity of hippocampal interneurons. Cell Tissue Res 373:619–641PubMedPubMedCentralCrossRefGoogle Scholar
  18. Booker SA, Gross A, Althof D, Shigemoto R, Bettler B, Frotscher M, Hearing M, Wickman K, Watanabe M, Kulik Á, Vida I (2013) Differential GABAB-receptor-mediated effects in perisomatic-and dendrite-targeting parvalbumin interneurons. J Neurosci 18:7961–7974CrossRefGoogle Scholar
  19. Both M, Bähner F, von Bohlen und Halbach O, Draguhn A (2008) Propagation of specific network patterns through the mouse hippocampus. Hippocampus 18:899–908PubMedCrossRefGoogle Scholar
  20. 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 27:1942–1953PubMedCrossRefGoogle Scholar
  21. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268PubMedCrossRefGoogle Scholar
  22. 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 15:47–60PubMedCrossRefGoogle Scholar
  23. Bragin A, Engel J Jr, Wilson CL, Fried I, Mathern GW (1999) Hippocampal and entorhinal cortex high-frequency oscillations (100–500 Hz) in human epileptic brain and in kainic acid--treated rats with chronic seizures. Epilepsia 40:127–137PubMedCrossRefGoogle Scholar
  24. Bragin A, Mody I, Wilson CL, Engel J Jr (2002) Local generation of fast ripples in epileptic brain. J Neurosci 22:2012–2021PubMedCrossRefGoogle Scholar
  25. 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 48:1883–1894PubMedCrossRefGoogle Scholar
  26. 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 97:254–263PubMedCrossRefGoogle Scholar
  27. Brown RA, Walling SG, Milway JS, Harley CW (2005) Locus ceruleus activation suppresses feedforward interneurons and reduces β-γ electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus. J Neurosci 25:1985–1991PubMedCrossRefGoogle Scholar
  28. Bucci P, Mucci A, Merlotti E, Volpe U, Galderisi S (2007) Induced gamma activity and event-related coherence in schizophrenia. Clin EEG Neurosci 38:96–104PubMedCrossRefGoogle Scholar
  29. Bucher D, Goaillard JM (2011) Beyond faithful conduction: short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon. Prog Neurobiol 94:307–346PubMedPubMedCentralCrossRefGoogle Scholar
  30. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823–828PubMedPubMedCentralCrossRefGoogle Scholar
  31. Buhl EH, Tamás G, Fisahn A (1998) Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 513:117–126PubMedPubMedCentralCrossRefGoogle Scholar
  32. Buzsáki G (1989) Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31:551–570PubMedCrossRefGoogle Scholar
  33. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340PubMedCrossRefGoogle Scholar
  34. Buzsáki G, Buhl DL, Harris KD, Csicsvari J, Czéh B, Morozov A (2003) Hippocampal network patterns of activity in the mouse. Neuroscience 116:201–211PubMedCrossRefGoogle Scholar
  35. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929PubMedCrossRefGoogle Scholar
  36. Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171PubMedCrossRefGoogle Scholar
  37. 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 365:125–137PubMedCrossRefGoogle Scholar
  38. Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027PubMedCrossRefGoogle Scholar
  39. Callaway EM (2002) Cell type specificity of local cortical connections. J Neurocytol 31:231–237PubMedCrossRefGoogle Scholar
  40. Carr MF, Karlsson MP, Frank LM (2012) Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 75:700–713PubMedPubMedCentralCrossRefGoogle Scholar
  41. Chen K, Aradi I, Santhakumar V, Soltesz I (2002) H-channels in epilepsy: new targets for seizure control? Trends Pharmacol Sci 23:552–557PubMedCrossRefGoogle Scholar
  42. Chevaleyre V, Siegelbaum SA (2010) Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 66:560–572PubMedPubMedCentralCrossRefGoogle Scholar
  43. Chittajallu R, Craig MT, McFarland A, Yuan X, Gerfen S, Tricoire L, Erkkila B, Barron SC, Lopez CM, Liang BJ, Jeffries BW, Pelkey KA, McBain CJ (2013) Dual origins of functionally distinct O-LM interneurons revealed by differential 5-HT 3A R expression. Nat Neurosci 11:1598–1607CrossRefGoogle Scholar
  44. Cho RY, Konecky RO, Carter CS (2006) Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci U S A 103:19878–19883PubMedPubMedCentralCrossRefGoogle Scholar
  45. Chrobak JJ, Buzsáki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056–3066PubMedCrossRefGoogle Scholar
  46. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronisation of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75–78PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 23:1933–1942CrossRefGoogle Scholar
  48. 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 95:3645–3653PubMedCrossRefGoogle Scholar
  49. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y (1998) GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1:470–478CrossRefGoogle Scholar
  50. 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 35:147–159CrossRefGoogle Scholar
  51. Craig MT, McBain CJ (2015) Fast gamma oscillations are generated intrinsically in CA1 without the involvement of fast-spiking basket cells. J Neurosci 35:3616–3624PubMedPubMedCentralCrossRefGoogle Scholar
  52. Csicsvari J, Hirase H, Czurko´ A, Mamiya A, Buzsáki G (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274–287PubMedCrossRefGoogle Scholar
  53. Csicsvari J, Hirase H, Mamiya A, Buzsáki G (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28:585–594PubMedCrossRefGoogle Scholar
  54. Csicsvari J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322PubMedCrossRefGoogle Scholar
  55. Cunningham MO, Hunt J, Middleton S, FE LB, 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 26:2767–2776PubMedCrossRefGoogle Scholar
  56. Daw MI, Tricoire L, Erdelyi F, Daw MI, Tricoire L, Erdelyi F, Szabo G, McBain CJ (2009) Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent. J Neurosci 29:11112–11122PubMedPubMedCentralCrossRefGoogle Scholar
  57. Debanne D, Campanac E, Bialowas A, Carlier E, Alcaraz G (2011) Axon physiology. Physiol Rev 91:555–602PubMedCrossRefGoogle Scholar
  58. Deisseroth K, Hegemann P (2017) The form and function of channelrhodopsin. Science 357:eaan5544PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 26:10380–10386PubMedPubMedCentralCrossRefGoogle Scholar
  60. Dodt HU, Zieglgänsberger W (1994) Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci 17:453–458PubMedCrossRefGoogle Scholar
  61. Draguhn A, Traub RD, Schmitz D, Jefferys JG (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189–192PubMedCrossRefGoogle Scholar
  62. 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 U S A 104:17530–17535PubMedPubMedCentralCrossRefGoogle Scholar
  63. Dugladze T, Schmitz D, Whittington MA, Vida I, Gloveli T (2012) Segregation of axonal and somatic activity during fast network oscillations. Science 336:1458–1461PubMedPubMedCentralCrossRefGoogle Scholar
  64. Dugladze T, Maziashvili N, Börgers C, Gurgenidze S, Häussler U, Winkelmann A, Haas CA, Meier JC, Vida I, Kopell NJ (2013) GABAB autoreceptor-mediated cell type-specific reduction of inhibition in epileptic mice. Proc Natl Acad Sci U S A 110(37):15073–15078PubMedPubMedCentralCrossRefGoogle Scholar
  65. Eller J, Zarnadze S, Bäuerle P, Dugladze T, Gloveli T (2015) Cell type-specific separation of subicular principal neurons during network activities. PLoS One 10(4):e0123636PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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 10:187–197PubMedCrossRefGoogle Scholar
  67. Ferguson KA, Huh CY, Amilhon B, Williams S, Skinner FK (2013) Experimentally constrained CA1 fast-firing parvalbumin-positive interneuron network models exhibit sharp transitions into coherent high frequency rhythms. Front Comput Neurosci 7:144PubMedPubMedCentralCrossRefGoogle Scholar
  68. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186–189PubMedCrossRefGoogle Scholar
  69. 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 33:615–624PubMedCrossRefGoogle Scholar
  70. 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 24:9658–9668PubMedCrossRefGoogle Scholar
  71. Fischer Y, Gähwiler BH, Thompson SM (1999) Activation of intrinsic hippocampal theta oscillations by acetylcholine in rat septo-hippocampal cocultures. J Physiol 519:405–413PubMedPubMedCentralCrossRefGoogle Scholar
  72. Fisher RS, Webber WR, Lesser RP, Arroyo S, Uematsu S (1992) High-frequency EEG activity at the start of seizures. J Clin Neurophysiol 9:441–448PubMedCrossRefGoogle Scholar
  73. 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 55:930–941PubMedCrossRefGoogle Scholar
  74. Ford JM, Krystal JH, Mathalon DH (2007) Neural synchrony in schizophrenia: from networks to new treatments. Schizophr Bull 33:848–852PubMedPubMedCentralCrossRefGoogle Scholar
  75. Frauscher B, Bartolomei F, Kobayashi K, Cimbalnik J, van ‘t Klooster MA, Rampp S, Otsubo H, Höller Y, Wu JY, Asano E, Engel J Jr, Kahane P, Jacobs J, Gotman J (2017) High-frequency oscillations: The state of clinical research. Epilepsia 58:1316–1329PubMedPubMedCentralCrossRefGoogle Scholar
  76. Frerking M, Ohliger-Frerking P (2002) AMPA receptors and kainate receptors encode different features of afferent activity. J Neurosci 22:7434–7443PubMedPubMedCentralCrossRefGoogle Scholar
  77. Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1:479–486PubMedCrossRefGoogle Scholar
  78. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470PubMedPubMedCentralCrossRefGoogle Scholar
  79. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33–42PubMedCrossRefGoogle Scholar
  80. 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 57:917–929PubMedPubMedCentralCrossRefGoogle Scholar
  81. Galarreta M, Erdélyi F, Szabó G, Hestrin S (2008) Cannabinoid sensitivity and synaptic properties of 2 GABAergic networks in the neocortex. Cereb Cortex 18:2296–2305PubMedPubMedCentralCrossRefGoogle Scholar
  82. Ganguly K, Kiss L, Poo M (2000) Enhancement of presynaptic neuronal excitability by correlated presynaptic and postsynaptic spiking. Nat Neurosci 3:1018–1026PubMedCrossRefGoogle Scholar
  83. 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 15:193–204CrossRefGoogle Scholar
  84. Geiger JR, Lübke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009–1023CrossRefGoogle Scholar
  85. Giepmans BN, Adams SR, Ellisman MH, Tsien RY (2006) The fluorescent toolbox for assessing protein location and function. Science 312:217–224PubMedCrossRefGoogle Scholar
  86. 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) 543:779–793CrossRefGoogle Scholar
  87. Girardeau G, Benchenane K, Wiener SI, Buzsáki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222–1223PubMedCrossRefGoogle Scholar
  88. 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 562:131–147PubMedCrossRefGoogle Scholar
  89. 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 U S A 102:13295–13300PubMedPubMedCentralCrossRefGoogle Scholar
  90. 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 27:9560–9572PubMedCrossRefGoogle Scholar
  91. Gonzalez-Burgos G, Lewis DA (2008) GABA Neurons and the Mechanisms of Network Oscillations: Implications for Understanding Cortical Dysfunction in Schizophrenia. Schizophr Bull 34:944–961PubMedPubMedCentralCrossRefGoogle Scholar
  92. Goutagny R, Jackson J, Williams S (2009) Self-generated theta oscillations in the hippocampus. Nat Neurosci 12:1491–1493PubMedCrossRefGoogle Scholar
  93. 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 566:689–715PubMedPubMedCentralCrossRefGoogle Scholar
  94. Gulyás AI, Freund TT (2015) Generation of physiological and pathological highfrequency oscillations: the role of perisomatic inhibition in sharp-wave rippleand interictal spike generation. Curr Opin Neurobiol 31:26–32PubMedCrossRefGoogle Scholar
  95. Gulyás AI, Szabó GG, Ulbert I, Holderith N, Monyer H, Erdélyi F, Szabó G, Freund TF, Hájos N (2010) Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 30:15134–15145PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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 24:9127–9137PubMedCrossRefGoogle Scholar
  97. Hajós M, Siok CJ, Hoffmann WE, Li S, Kocsis B (2008) Modulation of hippocampal theta oscillation by histamine H3 receptors. J Pharmacol Exp Ther 324:391–398PubMedCrossRefGoogle Scholar
  98. Hájos N, Ellender TJ, Zemankovics R, Mann EO, Exley R, Cragg SJ, Freund TF, Paulsen O (2009) Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci 29:319–327PubMedPubMedCentralCrossRefGoogle Scholar
  99. 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 6:306–329PubMedCrossRefGoogle Scholar
  100. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319–1328PubMedPubMedCentralCrossRefGoogle Scholar
  101. Hollnagel JO, Maslarova A, Haq RU, Heinemann U (2014) GABAB receptor dependent modulation of sharp wave-ripple complexes in the rat hippocampus in vitro. Neurosci Lett 574:15–20PubMedCrossRefGoogle Scholar
  102. 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 545:783–805PubMedPubMedCentralCrossRefGoogle Scholar
  103. Huh CY, Amilhon B, Ferguson KA, Manseau F, Torres-Platas SG, Peach JP, Scodras S, Mechawar N, Skinner FK, Williams S (2016) Excitatory inputs determine phase-locking strength and spike-timing of CA1 stratum oriens/alveus parvalbumin and somatostatin interneurons during intrinsically generated hippocampal theta rhythm. J Neurosci 36:6605–6622PubMedPubMedCentralCrossRefGoogle Scholar
  104. Jackson J, Amilhon B, Goutagny R, Bott J-B, Manseau F, Kortleven C, Bressler SL, Williams S (2014) Reversal of theta rhythm flow through intact hippocampal circuits. Nat Neurosci 17:1362–1370PubMedCrossRefGoogle Scholar
  105. Jacobs J, Staba R, Asano E, Otsubo H, Wu JY, Zijlmans M, Mohamed I, Kahane P, Dubeau F, Navarro V, Gotman J (2012) High-frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol 98:302–315PubMedPubMedCentralCrossRefGoogle Scholar
  106. Jadhav SP, Kemere C, German PW, Frank LM (2012) Awake hippocampal sharp-wave ripples support spatial memory. Science 336:1454–1458PubMedPubMedCentralCrossRefGoogle Scholar
  107. 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 472:615–663PubMedPubMedCentralCrossRefGoogle Scholar
  108. Jouvet M (1969) Biogenic amines and the states of sleep. Science 163:32–41PubMedCrossRefGoogle Scholar
  109. Jutras MJ, Buffalo EA (2010) Synchronous neural activity and memory formation. Curr Opin Neurobiol 20:150–155PubMedPubMedCentralCrossRefGoogle Scholar
  110. Kandel ER, Spencer WA (1961) Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. J Neurophysiol 24:243–259PubMedCrossRefGoogle Scholar
  111. 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 25:545–552PubMedCrossRefGoogle Scholar
  112. Kehrer C, Maziashvili N, Dugladze T, Gloveli T (2008) Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front Mol Neurosci 1:6PubMedPubMedCentralCrossRefGoogle Scholar
  113. Kittelberger K, Hur EE, Sazegar S, Keshavan V, Kocsis B (2012) Comparison of the effects of acute and chronic administration of ketamine on hippocampal oscillations: relevance for the NMDA receptor hypofunction model of schizophrenia. Brain Struct Funct 217:395–409PubMedCrossRefGoogle Scholar
  114. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57PubMedPubMedCentralCrossRefGoogle Scholar
  115. 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 421:844–848PubMedPubMedCentralCrossRefGoogle Scholar
  116. 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 7:41–47PubMedPubMedCentralCrossRefGoogle Scholar
  117. 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 U S A 103:1059–1064PubMedPubMedCentralCrossRefGoogle Scholar
  118. Kocsis B, Li S, Hajos M (2007) Behavior-dependent modulation of hippocampal EEG activity by the selective norepinephrine reuptake inhibitor reboxetine in rats. Hippocampus 17:627–633PubMedCrossRefGoogle Scholar
  119. Konopacki J, Gołebiewski H, Eckersdorf B (1992) Carbachol-induced rhythmic slow activity (theta) in cat hippocampal formation slices. Brain Res 578:13–16PubMedCrossRefGoogle Scholar
  120. Korotkova T, Fuchs EC, Ponomarenko A, von Engelhardt J, Monyer H (2010) NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68:557–569PubMedCrossRefGoogle Scholar
  121. Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ (2006) Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J Physiol 570:595–610PubMedCrossRefGoogle Scholar
  122. 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 542:167–179PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 62:3–13PubMedCrossRefGoogle Scholar
  124. Lerma J (2003) Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4:481–495PubMedCrossRefGoogle Scholar
  125. 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 60:65–77PubMedCrossRefGoogle Scholar
  126. Leung LS, Yim CY (1986) Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res 367:323–327PubMedCrossRefGoogle Scholar
  127. Leung LS, Yu HW (1998) Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection. J Neurophysiol 79:1592–1596PubMedCrossRefGoogle Scholar
  128. Leung LS, Lopes da Silva F, Wadman WJ (1982) Spectral characteristics of the hippocampal EEG in the freely moving rat. Clin Neurophysiol 54:203–219CrossRefGoogle Scholar
  129. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312–324PubMedCrossRefGoogle Scholar
  130. Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208CrossRefGoogle Scholar
  131. Lisman JE (2005) The theta/gamma discrete phase code occurring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15:913–922PubMedCrossRefGoogle Scholar
  132. Lisman JE, Idiart MAP (1995) Storage of 7+- 2 short term memories in oscillatory subcycles. Science 267:1512–1515PubMedCrossRefGoogle Scholar
  133. 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 497:119–130PubMedPubMedCentralCrossRefGoogle Scholar
  134. 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 524:91–116PubMedPubMedCentralCrossRefGoogle Scholar
  135. Madison DV, Lancaster B, Nicoll RA (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7:733–741PubMedCrossRefGoogle Scholar
  136. Magee JC (1999) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613–7624CrossRefGoogle Scholar
  137. Maier N, Nimmrich V, Draguhn A (2003) Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550:873–887PubMedPubMedCentralCrossRefGoogle Scholar
  138. Mann EO, Suckling JM, Hájos N, Greenfield SA, Paulsen O (2005) Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45:105–117PubMedPubMedCentralCrossRefGoogle Scholar
  139. Marek KW, Davis GW (2003) Controlling the active properties of excitable cells. Curr Opin Neurobiol 13:607–611PubMedCrossRefGoogle Scholar
  140. 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 500:409–440PubMedPubMedCentralCrossRefGoogle Scholar
  141. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11–23PubMedPubMedCentralCrossRefGoogle Scholar
  142. 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 22:7055–7064CrossRefGoogle Scholar
  143. 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 U S A 105:18572–18577PubMedPubMedCentralCrossRefGoogle Scholar
  144. Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol 428:61–77PubMedPubMedCentralCrossRefGoogle Scholar
  145. Miles R, Poncer JC (1996) Paired recordings from neurones. Curr Opin Neurobiol 6:387–394PubMedCrossRefGoogle Scholar
  146. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815–823PubMedPubMedCentralCrossRefGoogle Scholar
  147. Montplaisir J, Laverdiere M, Saint-Hilaire JM, Rouleau I (1987) Nocturnal sleep recording in partial epilepsy: a study with depth electrodes. J Clin Neurophysiol 4:383–388PubMedCrossRefGoogle Scholar
  148. Morales M, Bloom FE (1997) The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17:3157–3167PubMedCrossRefGoogle Scholar
  149. 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 402:385–401PubMedCrossRefGoogle Scholar
  150. 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 18:1575–1587PubMedPubMedCentralCrossRefGoogle Scholar
  151. 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 28:475–484PubMedCrossRefGoogle Scholar
  152. 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 563:663–670PubMedPubMedCentralCrossRefGoogle Scholar
  153. Notomi T, Shigemoto R (2004) Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol 471:241–276PubMedCrossRefGoogle Scholar
  154. 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 21:545–559PubMedCrossRefGoogle Scholar
  155. 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 20:3354–3368PubMedPubMedCentralCrossRefGoogle Scholar
  156. 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 49:143–155PubMedCrossRefPubMedCentralGoogle Scholar
  157. Oren I, Mann EO, Paulsen O, Hájos N (2006) Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro. J Neurosci 26:9923–9934PubMedCrossRefPubMedCentralGoogle Scholar
  158. Pálhalmi J, Paulsen O, Freund TF, Hájos N (2004) Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices. Neuropharmacology 47:381–289PubMedCrossRefPubMedCentralGoogle Scholar
  159. Pan WX, McNaughton N (2002) The role of the medial supramammillary nucleus in the control of hippocampal theta activity and behaviour in rats. Eur J Neurosci 16:1797–1809PubMedCrossRefPubMedCentralGoogle Scholar
  160. Pangalos M, Donoso JR, Winterer J, Zivkovic AR, Kempter R, Maier N, Schmitz D (2013) Recruitment of oriens-lacunosum-moleculare interneurons during hippocampal ripples. Proc Natl Acad Sci U S A 110:4398–4403PubMedPubMedCentralCrossRefGoogle Scholar
  161. Paré D, Collins DR (2000) Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats. J Neurosci 20:2701–2710PubMedCrossRefPubMedCentralGoogle Scholar
  162. Peng Y, Barreda Tomás FJ, Klisch C, Vida I, Geiger JRP (2017) Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum. Cereb Cortex 27:2435–2452PubMedPubMedCentralCrossRefGoogle Scholar
  163. 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 10:718–728PubMedCrossRefPubMedCentralGoogle Scholar
  164. 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 14:202–211PubMedCrossRefPubMedCentralGoogle Scholar
  165. 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 529:205–213PubMedPubMedCentralCrossRefGoogle Scholar
  166. 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 65:113–136PubMedCrossRefPubMedCentralGoogle Scholar
  167. 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 63:730–735PubMedCrossRefPubMedCentralGoogle Scholar
  168. Pitler TA, Alger BE (1992) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450:127–142PubMedPubMedCentralCrossRefGoogle Scholar
  169. Polleux F (2005) Genetic mechanisms specifying cortical connectivity: let’s make some projections together. Neuron 46:395–400PubMedCrossRefPubMedCentralGoogle Scholar
  170. Pöschel B, Draguhn A, Heinemann U (2002) Glutamate-induced gamma oscillations in the dentate gyrus of rat hippocampal slices. Brain Res 938:22–28PubMedCrossRefPubMedCentralGoogle Scholar
  171. Pouille F, Scanziani M (2004) Routing of spike series by dynamic circuits in the hippocampus. Nature 429:717–723PubMedCrossRefPubMedCentralGoogle Scholar
  172. 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 25:6775–6786CrossRefGoogle Scholar
  173. 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 34:962–973PubMedPubMedCentralCrossRefGoogle Scholar
  174. Ropert N, Guy N (1991) Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampus in vitro. J Physiol (Lond) 441:121–136CrossRefGoogle Scholar
  175. 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 94:1509–1518PubMedCrossRefPubMedCentralGoogle Scholar
  176. Ruiz AJ, Kullmann DM (2013) Ionotropic receptors at hippocampal mossy fibers: roles in axonal excitability, synaptic transmission, and plasticity. Front Neural Circ 6:1–12Google Scholar
  177. 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 28:143–150PubMedCrossRefPubMedCentralGoogle Scholar
  178. Sasaki T, Matsuki N, Ikegaya Y (2012) Targeted axon-attached recording with fluorescent patch-clamp pipettes in brain slices. Nat Protoc 7:1228–1234PubMedCrossRefGoogle Scholar
  179. 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 85:1986–1997PubMedCrossRefGoogle Scholar
  180. Schlingloff D, Káli S, Freund TF, Hájos N, Gulyás AI (2014) Mechanisms of sharp wave initiation and ripple generation. J Neurosci. 34:11385–11398PubMedPubMedCentralCrossRefGoogle Scholar
  181. 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 15:7217–7225PubMedCrossRefGoogle Scholar
  182. Schmitz D, Gloveli T, Empson RM, Heinemann U (1998) Comparison of the effects of serotonin in the hippocampus and the entorhinal cortex. Mol Neurobiol 17:59–72PubMedCrossRefGoogle Scholar
  183. 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 31:831–840PubMedCrossRefGoogle Scholar
  184. Sheffield ME, Best TK, Mensh BD, Kath WL, Spruston N (2011) Slow integration leads to persistent action potential firing in distal axons of coupled interneurons. Nat Neurosci 14:200–207PubMedCrossRefGoogle Scholar
  185. Shen RY, Andrade R (1998) 5-Hydroxytryptamine2 receptor facilitates GABAergic neurotransmission in rat hippocampus. J Pharmacol Exp Ther 285:805–812PubMedGoogle Scholar
  186. Shimono K, Brucher F, Granger R, Lynch G, Taketani M (2000) Origins and distribution of cholinergically induced beta rhythms in hippocampal slices. J Neurosci 20:8462–8473PubMedCrossRefGoogle Scholar
  187. Sik A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651–6665PubMedPubMedCentralCrossRefGoogle Scholar
  188. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49–65PubMedCrossRefGoogle Scholar
  189. Slewa-Younan S, Gordon E, Williams L, Haig AR, Goldberg E (2001) Sex differences, gamma activity and schizophrenia. Int J Neurosci 107:131–144PubMedCrossRefGoogle Scholar
  190. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698–702PubMedPubMedCentralCrossRefGoogle Scholar
  191. Somogyi P, Klausberger T (2005) Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol (Lond) 562:9–26CrossRefGoogle Scholar
  192. Spampanato J, Mody I (2007) Spike timing of lacunosom-moleculare targeting interneurons and CA3 pyramidal cells during high-frequency network oscillations in vitro. J Neurophysiol 98:96–104PubMedCrossRefGoogle Scholar
  193. Spencer KM (2008) Visual gamma oscillations in schizophrenia: implications for understanding neural circuitry abnormalities. Clin EEG Neurosci 39:65–68PubMedCrossRefGoogle Scholar
  194. 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 U S A 101:17288–11793PubMedPubMedCentralCrossRefGoogle Scholar
  195. Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206–221PubMedCrossRefGoogle Scholar
  196. Stark E, Roux L, Eichler R, Senzai Y, Royer S, Buzsáki G (2014) Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 83:467–480PubMedPubMedCentralCrossRefGoogle Scholar
  197. 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 U S A 104:14831–14836PubMedPubMedCentralCrossRefGoogle Scholar
  198. Szabo G, McBain CJ (2009) Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent. J Neurosci 29:11112–11122PubMedPubMedCentralCrossRefGoogle Scholar
  199. Tecott LH, Maricq AV, Julius D (1993) Nervous system distribution of the serotonin 5-HT3 receptor mRNA. Proc Natl Acad Sci U S A 90:1430–1434PubMedPubMedCentralCrossRefGoogle Scholar
  200. Tesche CD, Karhu J (2000) Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci USA 97:919–924PubMedCrossRefGoogle Scholar
  201. 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 U S A 104:13490–13495PubMedPubMedCentralCrossRefGoogle Scholar
  202. 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 20:8279–8289CrossRefGoogle Scholar
  203. 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 87:1165–1168PubMedCrossRefGoogle Scholar
  204. 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 12:4093–4106PubMedCrossRefGoogle Scholar
  205. 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 U S A 100:11047–11052PubMedPubMedCentralCrossRefGoogle Scholar
  206. 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 27:8184–8189PubMedPubMedCentralCrossRefGoogle Scholar
  207. 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 20:3544–3551PubMedCrossRefGoogle Scholar
  208. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407–418PubMedCrossRefGoogle Scholar
  209. 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 506:755–773PubMedPubMedCentralCrossRefGoogle Scholar
  210. Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49:107–117PubMedPubMedCentralCrossRefGoogle Scholar
  211. 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 99:2656–2671PubMedPubMedCentralCrossRefGoogle Scholar
  212. Wang X-J, Buzsáki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16:6402–6413PubMedCrossRefGoogle Scholar
  213. Wang CZ, Yang SF, Xia Y, Johnson KM (2008) Postnatal Phencyclidine Administration Selectively Reduces Adult Cortical Parvalbumin-Containing Interneurons. Neuropsychopharmacology 33:2442–2455PubMedCrossRefGoogle Scholar
  214. Weiss T, Veh RW, Heinemann U (2003) Dopamine depresses cholinergic oscillatory network activity in rat hippocampus. Eur J Neurosci 18:2573–2580PubMedCrossRefGoogle Scholar
  215. White JA, Chow CC, Ritt J, Soto-Treviño C, Kopell N (1998) Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons. J Comput Neurosci 5:5–16PubMedCrossRefGoogle Scholar
  216. Whittington MA, Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676–682PubMedCrossRefGoogle Scholar
  217. Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612–615PubMedCrossRefGoogle Scholar
  218. 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 502:591–607PubMedPubMedCentralCrossRefGoogle Scholar
  219. Williams SR, Stuart GJ (2003) Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J Neurosci 23:7358–7367PubMedCrossRefGoogle Scholar
  220. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–679PubMedCrossRefGoogle Scholar
  221. 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 212:75–83PubMedPubMedCentralCrossRefGoogle Scholar
  222. Wulff P, Ponomarenko AA, Bartos M, Korotkova TM, Fuchs EC, Bähner F, Both M, Tort AB, Kopell NJ, Wisden W, Monyer H (2009) Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 106:3561–3566PubMedPubMedCentralCrossRefGoogle Scholar
  223. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsáki G (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: Network and intracellular mechanisms. J Neurosci 15:30–46PubMedCrossRefGoogle Scholar
  224. Zarnadze S, Bäuerle P, Santos-Torres J, Böhm C, Schmitz D, Geiger JR, Dugladze T, Gloveli T (2016) Cell-specific synaptic plasticity induced by network oscillations. Elife 5:pii: e14912CrossRefGoogle Scholar
  225. Zhang ZJ, Reynolds GP (2002) A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr Res 55:1–10PubMedCrossRefGoogle Scholar
  226. 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 446:633–639PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Cellular and Network Physiology Lab, Neuroscience Research CenterCharité – Universitätsmedizin BerlinBerlinGermany
  2. 2.Centre for Discovery Brain SciencesUniversity of EdinburghEdinburghUK
  3. 3.Department of MathematicsBoston UniversityBostonUSA
  4. 4.Institute of Integrative NeuroanatomyCharité – Universitätsmedizin BerlinBerlinGermany

Personalised recommendations