Systematic Data Mining of Hippocampal Synaptic Properties

  • Keivan Moradi
  • Giorgio A. AscoliEmail author
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)


Synaptic electrophysiology has been extensively investigated in the rodent hippocampal formation for several decades. The strength, duration, and plasticity of excitatory and inhibitory signals depend both on the presynaptic and postsynaptic neuron types and vary substantially among subregions (dentate gyrus, CA3, CA2, CA1, subiculum, and entorhinal cortex) and layers (e.g., oriens and radiatum). While certain connections are better characterized (e.g., the Schaffer collateral from CA3 pyramidal to CA1 pyramidal cells), the lack of a systematic accounting of published synaptic data prevents a comprehensive comparison across the whole circuit., a knowledge base that identified over 100 neuron types based on morphological, electrophysiological, and molecular evidence, enables integration and dense coverage of the available synaptic data. Peters’ Rule predicts more than 3000 “potential connections” among neuron types. Extensive literature mining revealed electrophysiological properties for approximately 50% of these potential synapses at neuron-type level in peer-reviewed publications. In these cases, we extract information about synaptic amplitude, kinetics, and, when available, short-term and long-term plasticity. Due to widely nonuniform experimental methods and conditions, these data must be normalized and modeled to enable meaningful quantifications. The resulting type-based organized and integrated data will facilitate large-scale data-driven simulations of the entire hippocampal formation.


Neural networks Microcircuits Connectivity Neuroinformatics Physiology Neuron types IPSC IPSP EPSC EPSP 



This project is supported by grants R01NS39600 (NIH), MURI N00014–10–1-0198 (ONR), NAKFI (Keck), CENTEC (AFOSR), Robust Intelligence (NSF), and Northrop Grumman.


  1. Ali AB, Thomson AM (1998) Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol 507(Pt 1):185–199PubMedPubMedCentralCrossRefGoogle Scholar
  2. Amaral D, Witter M (1995) Hippocampal formation, Paxinos G., the rat nervous system, 2nd edn. Academic, San DiegoGoogle Scholar
  3. Andersen P (1959) Interhippocampal impulses. I. Origin, course and distribution in cat, rabbit and rat. Acta Physiol Scand 47:63–90. CrossRefPubMedGoogle Scholar
  4. Andersen P (1960) Interhippocampal impulses. II. Apical dendritic activation of CAI neurons. Acta Physiol Scand 48:178–208. CrossRefPubMedGoogle Scholar
  5. Andersen P (2007) The hippocampus book. In: Oxford. Oxford University Press, New YorkGoogle Scholar
  6. Andersen P, Eccles JC, Loyning Y (1963) Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature 198:540–542PubMedCrossRefGoogle Scholar
  7. Andersen P, Sundberg SH, Sveen O, Wigstrom H (1977) Specific long-lasting potentiation of synaptic transmission in hippocampal slices. Nature 266(5604):736–737PubMedCrossRefGoogle Scholar
  8. Anstotz M, Cosgrove KE, Hack I, Mugnaini E, Maccaferri G, Lubke JH (2014) Morphology, input-output relations and synaptic connectivity of Cajal-Retzius cells in layer 1 of the developing neocortex of CXCR4-EGFP mice. Brain Struct Funct 219(6):2119–2139. CrossRefPubMedGoogle Scholar
  9. Antonov SM, Johnson JW (1999) Permeant ion regulation of N-methyl-D-aspartate receptor channel block by Mg(2+). Proc Natl Acad Sci U S A 96(25):14571–14576PubMedPubMedCentralCrossRefGoogle Scholar
  10. Ascoli GA (2006) Mobilizing the base of neuroscience data: the case of neuronal morphologies. Nat Rev Neurosci 7(4):318–324. CrossRefPubMedGoogle Scholar
  11. Ascoli GA, Donohue DE, Halavi M (2007) NeuroMorpho.Org: a central resource for neuronal morphologies. J Neurosci 27(35):9247–9251. CrossRefPubMedGoogle Scholar
  12. Astori S, Pawlak V, Kohr G (2010) Spike-timing-dependent plasticity in hippocampal CA3 neurons. J Physiol 588(Pt 22):4475–4488. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Baker JL, Perez-Rosello T, Migliore M, Barrionuevo G, Ascoli GA (2011) A computer model of unitary responses from associational/commissural and perforant path synapses in hippocampal CA3 pyramidal cells. J Comput Neurosci 31(1):137–158. CrossRefPubMedGoogle Scholar
  14. Beed P, Bendels MH, Wiegand HF, Leibold C, Johenning FW, Schmitz D (2010) Analysis of excitatory microcircuitry in the medial entorhinal cortex reveals cell-type-specific differences. Neuron 68(6):1059–1066. CrossRefPubMedGoogle Scholar
  15. Beed P, Gundlfinger A, Schneiderbauer S, Song J, Bohm C, Burgalossi A et al (2013) Inhibitory gradient along the dorsoventral axis in the medial entorhinal cortex. Neuron 79(6):1197–1207. CrossRefPubMedGoogle Scholar
  16. Bendels MH, Beed P, Leibold C, Schmitz D, Johenning FW (2008) A novel control software that improves the experimental workflow of scanning photostimulation experiments. J Neurosci Methods 175(1):44–57. CrossRefPubMedGoogle Scholar
  17. Bennett MR (1999) The early history of the synapse: from Plato to Sherrington. Brain Res Bull 50(2):95–118PubMedCrossRefGoogle Scholar
  18. Bezaire MJ, Soltesz I (2013) Quantitative assessment of CA1 local circuits: knowledge base for interneuron-pyramidal cell connectivity. Hippocampus 23(9):751–785. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18(24):10464–10472CrossRefGoogle Scholar
  20. Bi GQ, Wang HX (2002) Temporal asymmetry in spike timing-dependent synaptic plasticity. Physiol Behav 77(4–5):551–555PubMedCrossRefGoogle Scholar
  21. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232(2):331–356PubMedPubMedCentralCrossRefGoogle Scholar
  22. Bota M, Swanson LW (2007) The neuron classification problem. Brain Res Rev 56(1):79–88. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368(6474):823–828. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Burger M (2011) Inverse problems in ion channel modelling. Inverse Prob 27(8):083001CrossRefGoogle Scholar
  25. Campanac E, Gasselin C, Baude A, Rama S, Ankri N, Debanne D (2013) Enhanced intrinsic excitability in basket cells maintains excitatory-inhibitory balance in hippocampal circuits. Neuron 77(4):712–722. CrossRefPubMedGoogle Scholar
  26. Candès EJ, Recht B (2009) Exact matrix completion via convex optimization. Found Comput Math 9(6):717–772CrossRefGoogle Scholar
  27. Canto CB, Witter MP (2012a) Cellular properties of principal neurons in the rat entorhinal cortex. I. The lateral entorhinal cortex. Hippocampus 22(6):1256–1276. CrossRefGoogle Scholar
  28. Canto CB, Witter MP (2012b) Cellular properties of principal neurons in the rat entorhinal cortex. II. The medial entorhinal cortex. Hippocampus 22(6):1277–1299. CrossRefGoogle Scholar
  29. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K et al (2010) Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat Protoc 5(2):247–254. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Chamberland S, Topolnik L (2012) Inhibitory control of hippocampal inhibitory neurons. Front Neurosci 6:165. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Chang H, Ciani S, Kidokoro Y (1994) Ion permeation properties of the glutamate receptor channel in cultured embryonic Drosophila myotubes. J Physiol 476(1):1–16PubMedPubMedCentralGoogle Scholar
  32. Chapeau-Blondeau F, Chambet N (1995) Synapse models for neural networks: from ion channel kinetics to multiplicative coefficient wij. Neural Comput 7(4):713–734PubMedCrossRefGoogle Scholar
  33. Chen C, He B, Yuan X (2012) Matrix completion via an alternating direction method. IMA J Numer Anal 32(1):227–245CrossRefGoogle Scholar
  34. Chiu CQ, Lur G, Morse TM, Carnevale NT, Ellis-Davies GC, Higley MJ (2013) Compartmentalization of GABAergic inhibition by dendritic spines. Science 340(6133):759–762. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Clarke RJ, Johnson JW (2008) Voltage-dependent gating of NR1/2B NMDA receptors. J Physiol 586(Pt 23):5727–5741. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Coalson RD, Kurnikova MG (2005) Poisson-Nernst-Planck theory approach to the calculation of current through biological ion channels. IEEE Trans Nanobioscience 4(1):81–93PubMedCrossRefGoogle Scholar
  37. Cooper KE, Gates PY, Eisenberg RS (1988) Surmounting barriers in ionic channels. Q Rev Biophys 21(3):331–364PubMedCrossRefGoogle Scholar
  38. Cossart R, Petanjek Z, Dumitriu D, Hirsch JC, Ben-Ari Y, Esclapez M et al (2006) Interneurons targeting similar layers receive synaptic inputs with similar kinetics. Hippocampus 16(4):408–420. CrossRefPubMedGoogle Scholar
  39. Couey JJ, Witoelar A, Zhang SJ, Zheng K, Ye J, Dunn B et al (2013) Recurrent inhibitory circuitry as a mechanism for grid formation. Nat Neurosci 16(3):318–324. CrossRefPubMedGoogle Scholar
  40. Dan Y, Poo MM (2006) Spike timing-dependent plasticity: from synapse to perception. Physiol Rev 86(3):1033–1048. CrossRefPubMedGoogle Scholar
  41. Dayan P, Abbott LF (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems (computational neuroscience). Massachusetts Institute of Technology Press, Cambridge, MAGoogle Scholar
  42. De Schutter E (2000) Computational neuroscience: realistic modeling for experimentalists. Boca Raton, CRC PressCrossRefGoogle Scholar
  43. De Schutter E (2010) Computational modeling methods for neuroscientists (computational neuroscience). MIT Press, Cambridge, MAGoogle Scholar
  44. Derrick BE, Martinez JL Jr (1996) Associative, bidirectional modifications at the hippocampal mossy fibre-CA3 synapse. Nature 381(6581):429–434. CrossRefPubMedGoogle Scholar
  45. Destexhe A, Mainen ZF, Sejnowski TJ (1994a) An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Comput 6(1):14–18CrossRefGoogle Scholar
  46. Destexhe A, Mainen ZF, Sejnowski TJ (1994b) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci 1(3):195–230PubMedCrossRefGoogle Scholar
  47. Destexhe A, Mainen ZF, Sejnowski TJ (1995) Fast kinetic models for simulating AMPA, NMDA, GABA A and GABA B receptors. In: The neurobiology of computation. Springer, Boston, MA, pp 9–14CrossRefGoogle Scholar
  48. Dhillon A, Jones RS (2000) Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99(3):413–422PubMedCrossRefGoogle Scholar
  49. Dickson CT, Mena AR, Alonso A (1997) Electroresponsiveness of medial entorhinal cortex layer III neurons in vitro. Neuroscience 81(4):937–950PubMedCrossRefGoogle Scholar
  50. Dudek SM, Bear MF (1993) Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13(7):2910–2918CrossRefGoogle Scholar
  51. Dumitriu D, Cossart R, Huang J, Yuste R (2007) Correlation between axonal morphologies and synaptic input kinetics of interneurons from mouse visual cortex. Cereb Cortex 17(1):81–91. CrossRefPubMedGoogle Scholar
  52. Eisenberg RS (1999) From structure to function in open ionic channels. J Membr Biol 171(1):1–24PubMedCrossRefGoogle Scholar
  53. Eisenberg, B. (2010) Crowded charges in ion channels. arXiv preprint arXiv:1009.1786Google Scholar
  54. Eisenberg B (2012) A leading role for mathematics in the study of ionic solutions. SIAM News 45(9):11–12CrossRefGoogle Scholar
  55. Elfant D, Pal BZ, Emptage N, Capogna M (2008) Specific inhibitory synapses shift the balance from feedforward to feedback inhibition of hippocampal CA1 pyramidal cells. Eur J Neurosci 27(1):104–113. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Empson RM, Heinemann U (1995) The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J Physiol 484(Pt 3):707–720PubMedPubMedCentralCrossRefGoogle Scholar
  57. Evans SM, Janson AM, Nyengaard JR (2004) Quantitative methods in neuroscience: a neuroanatomical approach. Oxford University Press, New YorkCrossRefGoogle Scholar
  58. Feng J (2004) Computational neuroscience: comprehensive approach (Chapman & Hall/CRC mathematical biology and medicine series). Chapman & Hall/CRC, Boca RatonGoogle Scholar
  59. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6(4):347–470 doi:10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIPO1>3.0.CO;2-IPubMedPubMedCentralCrossRefGoogle Scholar
  60. Froemke RC, Dan Y (2002) Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416(6879):433–438. CrossRefGoogle Scholar
  61. Froemke RC, Tsay IA, Raad M, Long JD, Dan Y (2006) Contribution of individual spikes in burst-induced long-term synaptic modification. J Neurophysiol 95(3):1620–1629. CrossRefGoogle Scholar
  62. Fuhrmann G, Segev I, Markram H, Tsodyks M (2002) Coding of temporal information by activity-dependent synapses. J Neurophysiol 87(1):140–148PubMedCrossRefGoogle Scholar
  63. Geiger JR, Lubke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18(6):1009–1023CrossRefGoogle Scholar
  64. Gerhard F, Pipa G, Lima B, Neuenschwander S, Gerstner W (2011) Extraction of network topology from multi-electrode recordings: is there a small-world effect? Front Comput Neurosci 5:4. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Germroth P, Schwerdtfeger WK, Buhl EH (1989) Morphology of identified entorhinal neurons projecting to the hippocampus. A light microscopical study combining retrograde tracing and intracellular injection. Neuroscience 30(3):683–691PubMedCrossRefGoogle Scholar
  66. Germroth P, Schwerdtfeger WK, Buhl EH (1991) Ultrastructure and aspects of functional organization of pyramidal and nonpyramidal entorhinal projection neurons contributing to the perforant path. J Comp Neurol 305(2):215–231. CrossRefPubMedGoogle Scholar
  67. Glickfeld LL, Scanziani M (2006) Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat Neurosci 9(6):807–815. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Gloveli T, Schmitz D, Empson RM, Dugladze T, Heinemann U (1997) Morphological and electrophysiological characterization of layer III cells of the medial entorhinal cortex of the rat. Neuroscience 77(3):629–648PubMedCrossRefGoogle Scholar
  69. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD et al (2005) Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 562(Pt 1):131–147. CrossRefPubMedGoogle Scholar
  70. Glyzin S, Kolesov AY, Rozov NK (2013) On a method for mathematical modeling of chemical synapses. Differ Equ 49(10):1193–1210CrossRefGoogle Scholar
  71. Goldman DE (1943) Potential, impedance, and rectification in membranes. J Gen Physiol 27(1):37–60PubMedPubMedCentralCrossRefGoogle Scholar
  72. Goswami SP, Bucurenciu I, Jonas P (2012) Miniature IPSCs in hippocampal granule cells are triggered by voltage-gated Ca2+ channels via microdomain coupling. J Neurosci 32(41):14294–14304. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Gutig R, Aharonov R, Rotter S, Sompolinsky H (2003) Learning input correlations through nonlinear temporally asymmetric Hebbian plasticity. J Neurosci 23(9):3697–3714PubMedCrossRefGoogle Scholar
  74. Hajos N, Mody I (1997) Synaptic communication among hippocampal interneurons: properties of spontaneous IPSCs in morphologically identified cells. J Neurosci 17(21):8427–8442PubMedCrossRefGoogle Scholar
  75. Han ZS, Buhl EH, Lorinczi Z, Somogyi P (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5(5):395–410CrossRefGoogle Scholar
  76. Hardie JB, Pearce RA (2006) Active and passive membrane properties and intrinsic kinetics shape synaptic inhibition in hippocampal CA1 pyramidal neurons. J Neurosci 26(33):8559–8569. CrossRefPubMedGoogle Scholar
  77. Harney SC, Jones MV (2002) Pre- and postsynaptic properties of somatic and dendritic inhibition in dentate gyrus. Neuropharmacology 43(4):584–594PubMedPubMedCentralCrossRefGoogle Scholar
  78. Harris E, Stewart M (2001) Propagation of synchronous epileptiform events from subiculum backward into area CA1 of rat brain slices. Brain Res 895(1–2):41–49PubMedCrossRefGoogle Scholar
  79. Harsch A, Robinson HP (2000) Postsynaptic variability of firing in rat cortical neurons: the roles of input synchronization and synaptic NMDA receptor conductance. J Neurosci 20(16):6181–6192PubMedCrossRefGoogle Scholar
  80. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8(10):1319–1328. CrossRefPubMedPubMedCentralGoogle Scholar
  81. Hellwig B (2000) A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex. Biol Cybern 82(2):111–121PubMedCrossRefGoogle Scholar
  82. Hennig MH (2013) Theoretical models of synaptic short term plasticity. Front Comput Neurosci 7:45. CrossRefPubMedPubMedCentralGoogle Scholar
  83. Hestrin S, Sah P, Nicoll RA (1990) Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5(3):247–253PubMedCrossRefGoogle Scholar
  84. Hodgkin A i, Huxley A, Katz B (1949) Ionic currents underlying activity in the giant axon of the squid. Arch Sci Physiol 3(2):129–150Google Scholar
  85. Houser CR (2007) Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity. Prog Brain Res 163:217–232. CrossRefGoogle Scholar
  86. Jaffe D, Johnston D (1990) Induction of long-term potentiation at hippocampal mossy-fiber synapses follows a Hebbian rule. J Neurophysiol 64(3):948–960PubMedCrossRefGoogle Scholar
  87. Jahr CE, Stevens CF (1987) Glutamate activates multiple single channel conductances in hippocampal neurons. Nature 325(6104):522–525. CrossRefPubMedGoogle Scholar
  88. Jahr CE, Stevens CF (1990) A quantitative description of NMDA receptor-channel kinetic behavior. J Neurosci 10(6):1830–1837CrossRefGoogle Scholar
  89. Jiang X, Shen S, Cadwell CR, Berens P, Sinz F, Ecker AS et al (2015) Principles of connectivity among morphologically defined cell types in adult neocortex. Science 350(6264):aac9462. CrossRefPubMedPubMedCentralGoogle Scholar
  90. Kandel ER, Spencer WA, Brinley FJ Jr (1961) Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J Neurophysiol 24:225–242PubMedCrossRefGoogle Scholar
  91. Karayannis T, Elfant D, Huerta-Ocampo I, Teki S, Scott RS, Rusakov DA et al (2010) Slow GABA transient and receptor desensitization shape synaptic responses evoked by hippocampal neurogliaform cells. J Neurosci 30(29):9898–9909. CrossRefPubMedPubMedCentralGoogle Scholar
  92. Kaufman A, Dror G, Meilijson I, Ruppin E (2006) Gene expression of Caenorhabditis elegans neurons carries information on their synaptic connectivity. PLoS Comput Biol 2(12):e167–e167PubMedPubMedCentralCrossRefGoogle Scholar
  93. Kelsch W, Li Z, Wieland S, Senkov O, Herb A, Gongrich C et al (2014) GluN2B-containing NMDA receptors promote glutamate synapse development in hippocampal interneurons. J Neurosci 34(48):16022–16030. CrossRefPubMedPubMedCentralGoogle Scholar
  94. Kim NK, Robinson HP (2011) Effects of divalent cations on slow unblock of native NMDA receptors in mouse neocortical pyramidal neurons. Eur J Neurosci 34(2):199–212. CrossRefPubMedGoogle Scholar
  95. Klausberger T (2009) GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci 30(6):947–957. CrossRefPubMedPubMedCentralGoogle Scholar
  96. Koch C (1999) Biophysics of computation: information processing in single neurons (computational neuroscience). Oxford University Press, New YorkGoogle Scholar
  97. Kohara K, Pignatelli M, Rivest AJ, Jung HY, Kitamura T, Suh J et al (2014) Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat Neurosci 17(2):269–279. CrossRefGoogle Scholar
  98. Korinek M, Sedlacek M, Cais O, Dittert I, Vyklicky L Jr (2010) Temperature dependence of N-methyl-D-aspartate receptor channels and N-methyl-D-aspartate receptor excitatory postsynaptic currents. Neuroscience 165(3):736–748. CrossRefPubMedGoogle Scholar
  99. Kumar SS, Buckmaster PS (2006) Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 26(17):4613–4623. CrossRefPubMedGoogle Scholar
  100. Kuner T, Schoepfer R (1996) Multiple structural elements determine subunit specificity of Mg2+ block in NMDA receptor channels. J Neurosci 16(11):3549–3558PubMedCrossRefGoogle Scholar
  101. Lacaille JC, Schwartzkroin PA (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology. J Neurosci 8(4):1400–1410PubMedCrossRefGoogle Scholar
  102. Lacaille JC, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7(7):1979–1993CrossRefGoogle Scholar
  103. Lamsa KP, Heeroma JH, Somogyi P, Rusakov DA, Kullmann DM (2007) Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 315(5816):1262–1266. CrossRefPubMedPubMedCentralGoogle Scholar
  104. Larimer P, Strowbridge BW (2010) Representing information in cell assemblies: persistent activity mediated by semilunar granule cells. Nat Neurosci 13(2):213–222. CrossRefPubMedGoogle Scholar
  105. Le Duigou C, Kullmann DM (2011) Group I mGluR agonist-evoked long-term potentiation in hippocampal oriens interneurons. J Neurosci 31(15):5777–5781. CrossRefPubMedPubMedCentralGoogle Scholar
  106. Le Duigou C, Savary E, Kullmann DM, Miles R (2015) Induction of anti-Hebbian LTP in CA1 stratum Oriens interneurons: interactions between group I metabotropic glutamate receptors and M1 muscarinic receptors. J Neurosci 35(40):13542–13554. CrossRefPubMedPubMedCentralGoogle Scholar
  107. Le Roux N, Cabezas C, Bohm UL, Poncer JC (2013) Input-specific learning rules at excitatory synapses onto hippocampal parvalbumin-expressing interneurons. J Physiol 591(Pt 7):1809–1822. CrossRefPubMedPubMedCentralGoogle Scholar
  108. Ledri M, Sorensen AT, Erdelyi F, Szabo G, Kokaia M (2011) Tuning afferent synapses of hippocampal interneurons by neuropeptide Y. Hippocampus 21(2):198–211. CrossRefPubMedGoogle Scholar
  109. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458(7236):299–304. CrossRefPubMedPubMedCentralGoogle Scholar
  110. Lei S, Pelkey KA, Topolnik L, Congar P, Lacaille JC, McBain CJ (2003) Depolarization-induced long-term depression at hippocampal mossy fiber-CA3 pyramidal neuron synapses. J Neurosci 23(30):9786–9795CrossRefGoogle Scholar
  111. Lewis CA (1979) Ion-concentration dependence of the reversal potential and the single channel conductance of ion channels at the frog neuromuscular junction. J Physiol 286:417–445PubMedPubMedCentralCrossRefGoogle Scholar
  112. Liu YC, Cheng JK, Lien CC (2014) Rapid dynamic changes of dendritic inhibition in the dentate gyrus by presynaptic activity patterns. J Neurosci 34(4):1344–1357. CrossRefPubMedPubMedCentralGoogle Scholar
  113. Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F, Sun XH et al (2012) Regulation of neuronal input transformations by tunable dendritic inhibition. Nat Neurosci 15(3):423–430., S421-423. CrossRefPubMedGoogle Scholar
  114. Maccaferri G, Toth K, McBain CJ (1998) Target-specific expression of presynaptic mossy fiber plasticity. Science 279(5355):1368–1370CrossRefGoogle Scholar
  115. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275(5297):213–215CrossRefGoogle Scholar
  116. Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 95(9):5323–5328PubMedPubMedCentralCrossRefGoogle Scholar
  117. Markram H, Gerstner W, Sjostrom PJ (2012) Spike-timing-dependent plasticity: a comprehensive overview. Front Synaptic Neurosci 4:2. CrossRefPubMedPubMedCentralGoogle Scholar
  118. Markram H, Muller E, Ramaswamy S, Reimann MW, Abdellah M, Sanchez CA et al (2015) Reconstruction and simulation of neocortical microcircuitry. Cell 163(2):456–492. CrossRefPubMedGoogle Scholar
  119. Markwardt SJ, Dieni CV, Wadiche JI, Overstreet-Wadiche L (2011) Ivy/neurogliaform interneurons coordinate activity in the neurogenic niche. Nat Neurosci 14(11):1407–1409. CrossRefPubMedPubMedCentralGoogle Scholar
  120. Marti-Subirana A, Soriano E, Garcia-Verdugo JM (1986) Morphological aspects of the ectopic granule-like cellular populations in the albino rat hippocampal formation: a Golgi study. J Anat 144:31–47PubMedPubMedCentralGoogle Scholar
  121. Mayer ML, Westbrook GL, Guthrie PB (1984) Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309(5965):261–263PubMedCrossRefGoogle Scholar
  122. Mazumder R, Hastie T, Tibshirani R (2010) Spectral regularization algorithms for learning large incomplete matrices. J Mach Learn Res 11:2287–2322PubMedPubMedCentralGoogle Scholar
  123. McCloskey DP, Hintz TM, Pierce JP, Scharfman HE (2006) Stereological methods reveal the robust size and stability of ectopic hilar granule cells after pilocarpine-induced status epilepticus in the adult rat. Eur J Neurosci 24(8):2203–2210. CrossRefPubMedPubMedCentralGoogle Scholar
  124. Melzer S, Michael M, Caputi A, Eliava M, Fuchs EC, Whittington MA et al (2012) Long-range-projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex. Science 335(6075):1506–1510. CrossRefGoogle Scholar
  125. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16(4):815–823PubMedPubMedCentralCrossRefGoogle Scholar
  126. Moradi K, Kaka G, Gharibzadeh S (2012) The role of passive normalization, voltage-gated channels and synaptic scaling in site-independence of somatic EPSP amplitude in CA1 pyramidal neurons. Neurosci Res 73(1):8–16CrossRefGoogle Scholar
  127. Moradi K, Moradi K, Ganjkhani M, Hajihasani M, Gharibzadeh S, Kaka G (2013) A fast model of voltage-dependent NMDA receptors. J Comput Neurosci 34(3):521–531. CrossRefPubMedGoogle Scholar
  128. Morrison A, Aertsen A, Diesmann M (2007) Spike-timing-dependent plasticity in balanced random networks. Neural Comput 19(6):1437–1467. CrossRefPubMedGoogle Scholar
  129. Morrison A, Diesmann M, Gerstner W (2008) Phenomenological models of synaptic plasticity based on spike timing. Biol Cybern 98(6):459–478. CrossRefPubMedPubMedCentralGoogle Scholar
  130. Mullner FE, Wierenga CJ, Bonhoeffer T (2015) Precision of inhibition: dendritic inhibition by individual GABAergic synapses on hippocampal pyramidal cells is confined in space and time. Neuron 87(3):576–589. CrossRefPubMedGoogle Scholar
  131. Nicholson E, Kullmann DM (2014) Long-term potentiation in hippocampal oriens interneurons: postsynaptic induction, presynaptic expression and evaluation of candidate retrograde factors. Philos Trans R Soc Lond Ser B Biol Sci 369(1633):20130133. CrossRefGoogle Scholar
  132. Nikolaev MV, Magazanik LG, Tikhonov DB (2012) Influence of external magnesium ions on the NMDA receptor channel block by different types of organic cations. Neuropharmacology 62(5–6):2078–2085. CrossRefPubMedGoogle Scholar
  133. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307(5950):462–465CrossRefGoogle Scholar
  134. Okazaki MM, Molnar P, Nadler JV (1999) Recurrent mossy fiber pathway in rat dentate gyrus: synaptic currents evoked in presence and absence of seizure-induced growth. J Neurophysiol 81(4):1645–1660PubMedCrossRefGoogle Scholar
  135. Oren I, Nissen W, Kullmann DM, Somogyi P, Lamsa KP (2009) Role of ionotropic glutamate receptors in long-term potentiation in rat hippocampal CA1 oriens-lacunosum moleculare interneurons. J Neurosci 29(4):939–950. CrossRefPubMedPubMedCentralGoogle Scholar
  136. Otis TS, Mody I (1992) Modulation of decay kinetics and frequency of GABAA receptor-mediated spontaneous inhibitory postsynaptic currents in hippocampal neurons. Neuroscience 49(1):13–32PubMedCrossRefGoogle Scholar
  137. Patneau DK, Mayer ML (1991) Kinetic analysis of interactions between kainate and AMPA: evidence for activation of a single receptor in mouse hippocampal neurons. Neuron 6(5):785–798PubMedCrossRefGoogle Scholar
  138. Patneau DK, Mayer ML, Jane DE, Watkins JC (1992) Activation and desensitization of AMPA/kainate receptors by novel derivatives of willardiine. J Neurosci 12(2):595–606PubMedCrossRefGoogle Scholar
  139. Pawelzik H, Hughes DI, Thomson AM (2002) Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol 443(4):346–367PubMedCrossRefGoogle Scholar
  140. Pawelzik H, Hughes DI, Thomson AM (2003) Modulation of inhibitory autapses and synapses on rat CA1 interneurones by GABA(A) receptor ligands. J Physiol 546(Pt 3):701–716PubMedCrossRefGoogle Scholar
  141. Perea G, Araque A (2007) Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317(5841):1083–1086. CrossRefPubMedGoogle Scholar
  142. Perez Y, Morin F, Lacaille JC (2001) A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc Natl Acad Sci U S A 98(16):9401–9406. CrossRefPubMedPubMedCentralGoogle Scholar
  143. Pfister JP, Gerstner W (2006) Triplets of spikes in a model of spike timing-dependent plasticity. J Neurosci 26(38):9673–9682. CrossRefPubMedGoogle Scholar
  144. Pierce JP, McCloskey DP, Scharfman HE (2011) Morphometry of hilar ectopic granule cells in the rat. J Comp Neurol 519(6):1196–1218. CrossRefPubMedPubMedCentralGoogle Scholar
  145. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R et al (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25(29):6775–6786. CrossRefGoogle Scholar
  146. Qian A, Johnson JW (2006) Permeant ion effects on external Mg2+ block of NR1/2D NMDA receptors. J Neurosci 26(42):10899–10910. CrossRefPubMedGoogle Scholar
  147. Quattrocolo G, Maccaferri G (2013) Novel GABAergic circuits mediating excitation/inhibition of Cajal-Retzius cells in the developing hippocampus. J Neurosci 33(13):5486–5498. CrossRefPubMedPubMedCentralGoogle Scholar
  148. Quattrocolo G, Maccaferri G (2014) Optogenetic activation of cajal-retzius cells reveals their glutamatergic output and a novel feedforward circuit in the developing mouse hippocampus. J Neurosci 34(39):13018–13032. CrossRefPubMedPubMedCentralGoogle Scholar
  149. Raghavachari S, Lisman JE (2004) Properties of quantal transmission at CA1 synapses. J Neurophysiol 92(4):2456–2467. CrossRefPubMedGoogle Scholar
  150. Reimann MW, King JG, Muller EB, Ramaswamy S, Markram H (2015) An algorithm to predict the connectome of neural microcircuits. Front Comput Neurosci 9:120. CrossRefPubMedPubMedCentralGoogle Scholar
  151. Ross ST, Soltesz I (2001) Long-term plasticity in interneurons of the dentate gyrus. Proc Natl Acad Sci U S A 98(15):8874–8879. CrossRefPubMedPubMedCentralGoogle Scholar
  152. Rothman JS (2015) Modeling Synapses. In: Jaeger D, Jung R (eds) Encyclopedia of computational neuroscience. Springer New York, New York, NY, pp 1738–1750. Scholar
  153. Rothman JS, Silver RA (2014) Data-driven modeling of synaptic transmission and integration. Prog Mol Biol Transl Sci 123:305–350. CrossRefPubMedPubMedCentralGoogle Scholar
  154. Santhakumar V, Aradi I, Soltesz I (2005) Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography. J Neurophysiol 93(1):437–453. CrossRefPubMedGoogle Scholar
  155. Savanthrapadian S, Meyer T, Elgueta C, Booker SA, Vida I, Bartos M (2014) Synaptic properties of SOM- and CCK-expressing cells in dentate gyrus interneuron networks. J Neurosci 34(24):8197–8209. CrossRefPubMedPubMedCentralGoogle Scholar
  156. Scharfman HE (1994) Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J Neurophysiol 72(5):2167–2180PubMedCrossRefGoogle Scholar
  157. Scharfman HE, Pierce JP (2012) New insights into the role of hilar ectopic granule cells in the dentate gyrus based on quantitative anatomic analysis and three-dimensional reconstruction. Epilepsia 53(Suppl 1):109–115. CrossRefPubMedPubMedCentralGoogle Scholar
  158. Scharfman HE, Sollas AE, Berger RE, Goodman JH, Pierce JP (2003) Perforant path activation of ectopic granule cells that are born after pilocarpine-induced seizures. Neuroscience 121(4):1017–1029PubMedCrossRefGoogle Scholar
  159. Schneider CJ, Bezaire M, Soltesz I (2012) Toward a full-scale computational model of the rat dentate gyrus. Front Neural Circuits 6:83. CrossRefPubMedPubMedCentralGoogle Scholar
  160. Schurmans S, Schiffmann SN, Gurden H, Lemaire M, Lipp HP, Schwam V et al (1997) Impaired long-term potentiation induction in dentate gyrus of calretinin-deficient mice. Proc Natl Acad Sci U S A 94(19):10415–10420PubMedPubMedCentralCrossRefGoogle Scholar
  161. Scimemi A (2014) Plasticity of GABA transporters: an unconventional route to shape inhibitory synaptic transmission. Front Cell Neurosci 8:128. CrossRefPubMedPubMedCentralGoogle Scholar
  162. Scorcioni R, Hamilton DJ, Ascoli GA (2008) Self-sustaining non-repetitive activity in a large scale neuronal-level model of the hippocampal circuit. Neural Netw 21(8):1153–1163. CrossRefPubMedPubMedCentralGoogle Scholar
  163. Scorza CA, Araujo BH, Leite LA, Torres LB, Otalora LF, Oliveira MS et al (2011) Morphological and electrophysiological properties of pyramidal-like neurons in the stratum oriens of Cornu ammonis 1 and Cornu ammonis 2 area of Proechimys. Neuroscience 177:252–268. CrossRefPubMedGoogle Scholar
  164. Sik A, Penttonen M, Buzsaki G (1997) Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study. Eur J Neurosci 9(3):573–588PubMedCrossRefGoogle Scholar
  165. Sjostrom PJ, Turrigiano GG, Nelson SB (2001) Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32(6):1149–1164CrossRefGoogle Scholar
  166. Somogyi P, Klausberger T (2005) Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 562(Pt 1):9–26. CrossRefPubMedPubMedCentralGoogle Scholar
  167. Song S, Miller KD, Abbott LF (2000) Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3(9):919–926. CrossRefPubMedGoogle Scholar
  168. Song S, Sjostrom PJ, Reigl M, Nelson S, Chklovskii DB (2005) Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3(3):e68. CrossRefPubMedPubMedCentralGoogle Scholar
  169. Spencer WA, Kandel ER (1961) Hippocampal neuron responses to selective activation of recurrent collaterals of hippocampofugal axons. Exp Neurol 4(2):149–161CrossRefGoogle Scholar
  170. Sporns O, Zwi JD (2004) The small world of the cerebral cortex. Neuroinformatics 2(2):145–162PubMedCrossRefGoogle Scholar
  171. Spruston N, Jonas P, Sakmann B (1995) Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J Physiol 482(Pt 2):325–352PubMedPubMedCentralCrossRefGoogle Scholar
  172. Standage D, Jalil S, Trappenberg T (2007) Computational consequences of experimentally derived spike-time and weight dependent plasticity rules. Biol Cybern 96(6):615–623. CrossRefPubMedGoogle Scholar
  173. Sterratt D (2011) Principles of computational modelling in neuroscience. In: Cambridge. Cambridge University Press, New YorkGoogle Scholar
  174. Steward O (1976) Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167(3):285–314. CrossRefPubMedGoogle Scholar
  175. Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169(3):347–370. CrossRefPubMedGoogle Scholar
  176. Stiles JR, Bartol TM (2001) Monte Carlo methods for simulating realistic synaptic microphysiology using MCell. Comput Neurosci Realistic Model Exp:87–127Google Scholar
  177. Stiles JR, Van Helden D, Bartol TM Jr, Salpeter EE, Salpeter MM (1996) Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. Proc Natl Acad Sci U S A 93(12):5747–5752PubMedPubMedCentralCrossRefGoogle Scholar
  178. Szabadics J, Soltesz I (2009) Functional specificity of mossy fiber innervation of GABAergic cells in the hippocampus. J Neurosci 29(13):4239–4251. CrossRefGoogle Scholar
  179. Szabadics J, Varga C, Brunner J, Chen K, Soltesz I (2010) Granule cells in the CA3 area. J Neurosci 30(24):8296–8307. CrossRefPubMedPubMedCentralGoogle Scholar
  180. Szabo A, Somogyi J, Cauli B, Lambolez B, Somogyi P, Lamsa KP (2012) Calcium-permeable AMPA receptors provide a common mechanism for LTP in glutamatergic synapses of distinct hippocampal interneuron types. J Neurosci 32(19):6511–6516. CrossRefPubMedPubMedCentralGoogle Scholar
  181. Szabo GG, Papp OI, Mate Z, Szabo G, Hajos N (2014) Anatomically heterogeneous populations of CB1 cannabinoid receptor-expressing interneurons in the CA3 region of the hippocampus show homogeneous input-output characteristics. Hippocampus 24(12):1506–1523. CrossRefPubMedGoogle Scholar
  182. Tahvildari B, Alonso A (2005) Morphological and electrophysiological properties of lateral entorhinal cortex layers II and III principal neurons. J Comp Neurol 491(2):123–140. CrossRefGoogle Scholar
  183. Toth K, McBain CJ (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1(7):572–578. CrossRefPubMedGoogle Scholar
  184. Trappenberg TP (2010) Fundamentals of computational neuroscience, 2nd edn. Oxford University Press, Oxford/New YorkGoogle Scholar
  185. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94(2):719–723PubMedPubMedCentralCrossRefGoogle Scholar
  186. Tsodyks M, Uziel A, Markram H (2000) Synchrony generation in recurrent networks with frequency-dependent synapses. J Neurosci 20(1):RC50PubMedCrossRefGoogle Scholar
  187. Turrigiano G (2012) Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb Perspect Biol 4(1):a005736. CrossRefPubMedPubMedCentralGoogle Scholar
  188. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391(6670):892–896. CrossRefGoogle Scholar
  189. Urban NN, Barrionuevo G (1996) Induction of hebbian and non-hebbian mossy fiber long-term potentiation by distinct patterns of high-frequency stimulation. J Neurosci 16(13):4293–4299PubMedCrossRefGoogle Scholar
  190. van der Linden S, Lopes da Silva FH (1998) Comparison of the electrophysiology and morphology of layers III and II neurons of the rat medial entorhinal cortex in vitro. Eur J Neurosci 10(4):1479–1489PubMedCrossRefGoogle Scholar
  191. van Rossum MC, Bi GQ, Turrigiano GG (2000) Stable Hebbian learning from spike timing-dependent plasticity. J Neurosci 20(23):8812–8821PubMedCrossRefGoogle Scholar
  192. Varadan V, Miller DM 3rd, Anastassiou D (2006) Computational inference of the molecular logic for synaptic connectivity in C. elegans. Bioinformatics 22(14):e497–e506. CrossRefPubMedGoogle Scholar
  193. Varela JA, Sen K, Gibson J, Fost J, Abbott LF, Nelson SB (1997) A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17(20):7926–7940PubMedCrossRefGoogle Scholar
  194. 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(Pt 3):755–773PubMedPubMedCentralCrossRefGoogle Scholar
  195. Vitureira N, Goda Y (2013) The interplay between Hebbian and homeostatic synaptic plasticity. J Cell Biol 203(2):175–186. CrossRefPubMedPubMedCentralGoogle Scholar
  196. Wallisch P (2014) MATLAB for neuroscientists: an introduction to scientific computing in MATLAB, 2nd edn. Academic, AmsterdamGoogle Scholar
  197. Wang HX, Gerkin RC, Nauen DW, Bi GQ (2005) Coactivation and timing-dependent integration of synaptic potentiation and depression. Nat Neurosci 8(2):187–193. CrossRefPubMedGoogle Scholar
  198. Wester JC, McBain CJ (2014) Behavioral state-dependent modulation of distinct interneuron subtypes and consequences for circuit function. Curr Opin Neurobiol 29:118–125. CrossRefPubMedGoogle Scholar
  199. Wheeler DW, White CM, Rees CL, Komendantov AO, Hamilton DJ, Ascoli GA (2015) a knowledge base of neuron types in the rodent hippocampus. Elife 4.
  200. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373(6515):612–615. CrossRefPubMedGoogle Scholar
  201. Williams PA, Larimer P, Gao Y, Strowbridge BW (2007) Semilunar granule cells: glutamatergic neurons in the rat dentate gyrus with axon collaterals in the inner molecular layer. J Neurosci 27(50):13756–13761. CrossRefGoogle Scholar
  202. Woodin MA, Ganguly K, Poo MM (2003) Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39(5):807–820PubMedPubMedCentralCrossRefGoogle Scholar
  203. Yang K, Dani JA (2014) Dopamine D1 and D5 receptors modulate spike timing-dependent plasticity at medial perforant path to dentate granule cell synapses. J Neurosci 34(48):15888–15897. CrossRefPubMedPubMedCentralGoogle Scholar
  204. Yang YC, Lee CH, Kuo CC (2010) Ionic flow enhances low-affinity binding: a revised mechanistic view into Mg2+ block of NMDA receptors. J Physiol 588(Pt 4):633–650. CrossRefPubMedGoogle Scholar
  205. Zhu Y, Auerbach A (2001a) K(+) occupancy of the N-methyl-d-aspartate receptor channel probed by Mg(2+) block. J Gen Physiol 117(3):287–298PubMedPubMedCentralCrossRefGoogle Scholar
  206. Zhu Y, Auerbach A (2001b) Na(+) occupancy and Mg(2+) block of the n-methyl-d-aspartate receptor channel. J Gen Physiol 117(3):275–286PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Krasnow Institute for Advanced StudyGeorge Mason UniversityFairfaxUSA

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