Advertisement

Neuromodulation of Hippocampal Cells and Circuits

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

Abstract

Neuromodulation is the process by which the properties of neurons and synapses are altered by neuroactive substances termed neuromodulators. The distinction between neuromodulation and classical neurotransmission can be fuzzy but in general neuromodulation is more diffuse, less targeted, and acts over a longer time course than classical fast neurotransmission. Often the same neurochemical may have rapid neurotransmitter-like effects followed by more sustained modulator-like actions. What makes neuromodulation an important consideration is that it appears to be a fundamental process in modifying all aspects of neural network functioning and information processing. Neural networks are not hard-wired, but plastic, and the neuromodulation of its components yields distinct activity patterns that are associated with behavioral state, allowing the same neural circuit to have added computational power.

Keywords

Synaptic Transmission Pyramidal Cell Gaba Release Hippocampal Cell Basket Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Further Reading

  1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19–29.PubMedCrossRefGoogle Scholar
  2. Alkondon M, Pereira EF, Albuquerque EX (1998) Alpha-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 810:257–263.PubMedCrossRefGoogle Scholar
  3. Alzheimer C, Rohrenbeck J, ten Bruggencate G (1991) Adenosine depresses induction of LTP at the mossy fiber-CA3 synapse in vitro. Brain Res 543:163–165.PubMedCrossRefGoogle Scholar
  4. Andrade R (1998) Regulation of membrane excitability in the central nervous system by serotonin receptor subtypes. Ann N Y Acad Sci 861:190–203.PubMedCrossRefGoogle Scholar
  5. Andrade R, Nicoll RA (1987) Pharmacologically distinct actions of serotonin on single pyramidal neurones of the rat hippocampus recorded in vitro. J Physiol 394:99–124.PubMedGoogle Scholar
  6. Andrade R, Malenka RC, Nicoll RA (1986) A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234:1261–1265.PubMedCrossRefGoogle Scholar
  7. Arancio O, Kiebler M, Lee CJ, Lev-Ram V, Tsien RY, Kandel ER, Hawkins RD (1996) Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87:1025–1035.PubMedCrossRefGoogle Scholar
  8. Arrigoni E, Rosenberg PA (2006) Nitric oxide-induced adenosine inhibition of hippocampal synaptic transmission depends on adenosine kinase inhibition and is cyclic GMP independent. Eur J Neurosci 24:2471–2480.PubMedCrossRefGoogle Scholar
  9. Ascoli GA et al. (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568.PubMedCrossRefGoogle Scholar
  10. Atzori M, Lau D, Tansey EP, Chow A, Ozaita A, Rudy B, McBain CJ (2000) H2 histamine receptor-phosphorylation of Kv3.2 modulates interneuron fast spiking. Nat Neurosci 3: 791–798.PubMedCrossRefGoogle Scholar
  11. Auerbach JM, Segal M (1994) A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 72:2034–2040.PubMedGoogle Scholar
  12. Auerbach JM, Segal M (1996) Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492(Pt 2):479–493.PubMedGoogle Scholar
  13. Bacci A, Huguenard JR, Prince DA (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431:312–316.PubMedCrossRefGoogle Scholar
  14. Bacci A, Huguenard JR, Prince DA (2005) Modulation of neocortical interneurons: extrinsic influences and exercises in self-control. Trends Neurosci 28:602–610.PubMedCrossRefGoogle Scholar
  15. Baraban SC, Tallent MK (2004) Interneuron diversity series: interneuronal neuropeptides – endogenous regulators of neuronal excitability. Trends Neurosci 27:135–142.PubMedCrossRefGoogle Scholar
  16. Baratta MV, Lamp T, Tallent MK (2002) Somatostatin depresses long-term potentiation and Ca2+ signaling in mouse dentate gyrus. J Neurophysiol 88:3078–3086.PubMedCrossRefGoogle Scholar
  17. Barbin G, Garbarg M, Schwartz JC, Storm-Mathisen J (1976) Histamine synthesizing afferents to the hippocampal region. J Neurochem 26:259–263.PubMedCrossRefGoogle Scholar
  18. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083–1152.PubMedCrossRefGoogle Scholar
  19. Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8:45–56.PubMedCrossRefGoogle Scholar
  20. Battey J, Wada E (1991) Two distinct receptor subtypes for mammalian bombesin-like peptides. Trends Neurosci 14:524–528.PubMedCrossRefGoogle Scholar
  21. Behr J, Gloveli T, Schmitz D, Heinemann U (2000) Dopamine depresses excitatory synaptic transmission onto rat subicular neurons via presynaptic D1-like dopamine receptors. J Neurophysiol 84:112–119.PubMedGoogle Scholar
  22. Behr J, Empson RM, Schmitz D, Gloveli T, Heinemann U (1997) Effects of serotonin on synaptic and intrinsic properties of rat subicular neurons in vitro. Brain Res 773:217–222.PubMedCrossRefGoogle Scholar
  23. Behrends JC, ten Bruggencate G (1993) Cholinergic modulation of synaptic inhibition in the guinea pig hippocampus in vitro: excitation of GABAergic interneurons and inhibition of GABA-release. J Neurophysiol 69:626–629.PubMedGoogle Scholar
  24. Bekkers JM (1993) Enhancement by histamine of NMDA-mediated synaptic transmission in the hippocampus. Science 261:104–106.PubMedCrossRefGoogle Scholar
  25. Belelli D, Lambert JJ (2005) Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6:565–575.PubMedCrossRefGoogle Scholar
  26. Benardo LS, Prince DA (1982a) Cholinergic pharmacology of mammalian hippocampal pyramidal cells. Neuroscience 7:1703–1712.PubMedCrossRefGoogle Scholar
  27. Benardo LS, Prince DA (1982b) Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells. Brain Res 249:333–344.PubMedCrossRefGoogle Scholar
  28. Benardo LS, Prince DA (1982c) Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res 249:315–331.PubMedCrossRefGoogle Scholar
  29. Benardo LS, Prince DA (1982d) Dopamine action on hippocampal pyramidal cells. J Neurosci 2:415–423.PubMedGoogle Scholar
  30. Benardo LS, Prince DA (1982e) Dopamine modulates a $\mathrm{Ca}2+$-activated potassium conductance in mammalian hippocampal pyramidal cells. Nature 297:76–79.PubMedCrossRefGoogle Scholar
  31. Bergles DE, Doze VA, Madison DV, Smith SJ (1996) Excitatory actions of norepinephrine on multiple classes of hippocampal CA1 interneurons. J Neurosci 16:572–585.PubMedGoogle Scholar
  32. Bergson C, Mrzljak L, Smiley JF, Pappy M, Levenson R, Goldman-Rakic PS (1995) Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J Neurosci 15:7821–7836.PubMedGoogle Scholar
  33. Bernardi G, Calabresi P, Mercuri N, Stanzione P (1984) Effect of dopamine on the threshold of the voltage-dependent ionic channels in the rat brain. Ann Ist Super Sanita 20:1–4.PubMedGoogle Scholar
  34. Bickmeyer U, Heine M, Manzke T, Richter DW (2002) Differential modulation of I(h) by 5-HT receptors in mouse CA1 hippocampal neurons. Eur J Neurosci 16:209–218.PubMedCrossRefGoogle Scholar
  35. Bijak M (1989) Antidepressant drugs potentiate the alpha 1-adrenoceptor effect in hippocampal slices. Eur J Pharmacol 166:183–191.PubMedCrossRefGoogle Scholar
  36. Bijak M, Misgeld U (1995) Adrenergic modulation of hilar neuron activity and granule cell inhibition in the guinea-pig hippocampal slice. Neuroscience 67:541–550.PubMedCrossRefGoogle Scholar
  37. Blackshaw S, Eliasson MJ, Sawa A, Watkins CC, Krug D, Gupta A, Arai T, Ferrante RJ, Snyder SH (2003) Species, strain and developmental variations in hippocampal neuronal and endothelial nitric oxide synthase clarify discrepancies in nitric oxide-dependent synaptic plasticity. Neuroscience 119:979–990.PubMedCrossRefGoogle Scholar
  38. Boden PR, Hill RG (1988) Effects of cholecystokinin and pentagastrin on rat hippocampal neurones maintained in vitro. Neuropeptides 12:95–103.PubMedCrossRefGoogle Scholar
  39. Boehm S (1999) Presynaptic alpha2-adrenoceptors control excitatory, but not inhibitory, transmission at rat hippocampal synapses. J Physiol 519(Pt 2):439–449.PubMedCrossRefGoogle Scholar
  40. Bohme GA, Stutzmann JM, Blanchard JC (1988) Excitatory effects of cholecystokinin in rat hippocampus: pharmacological response compatible with ‘central’- or B-type CCK receptors. Brain Res 451:309–318.PubMedCrossRefGoogle Scholar
  41. Bon CL, Garthwaite J (2001) Exogenous nitric oxide causes potentiation of hippocampal synaptic transmission during low-frequency stimulation via the endogenous nitric oxide-cGMP pathway. Eur J Neurosci 14:585–594.PubMedCrossRefGoogle Scholar
  42. Bonaventure P, Nepomuceno D, Kwok A, Chai W, Langlois X, Hen R, Stark K, Carruthers N, Lovenberg TW (2002) Reconsideration of 5-hydroxytryptamine (5-HT)(7) receptor distribution using [(3)H]5-carboxamidotryptamine and [(3)H]8-hydroxy-2-(di-n-propylamino)tetraline: analysis in brain of 5-HT(1A) knockout and 5-HT(1A/1B) double-knockout mice. J Pharmacol Exp Ther 302:240–248.PubMedCrossRefGoogle Scholar
  43. Borhegyi Z, Leranth C (1997) Substance P innervation of the rat hippocampal formation. J Comp Neurol 384:41–58.PubMedCrossRefGoogle Scholar
  44. Boulton CL, Irving AJ, Southam E, Potier B, Garthwaite J, Collingridge GL (1994) The nitric oxide – cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur J Neurosci 6:1528–1535.PubMedCrossRefGoogle Scholar
  45. Bouthenet ML, Ruat M, Sales N, Garbarg M, Schwartz JC (1988) A detailed mapping of histamine H1-receptors in guinea-pig central nervous system established by autoradiography with [125I]iodobolpyramine. Neuroscience 26:553–600.PubMedCrossRefGoogle Scholar
  46. Bowser DN, Khakh BS (2004) ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J Neurosci 24:8606–8620.PubMedCrossRefGoogle Scholar
  47. Brazhnik ES, Fox SE (1999) Action potentials and relations to the theta rhythm of medial septal neurons in vivo. Exp Brain Res 127:244–258.PubMedCrossRefGoogle Scholar
  48. Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283:673–676.PubMedCrossRefGoogle Scholar
  49. Brown RE, Haas HL (1999) On the mechanism of histaminergic inhibition of glutamate release in the rat dentate gyrus. J Physiol 515(Pt 3):777–786.PubMedCrossRefGoogle Scholar
  50. Brown RE, Stevens DR, Haas HL (2001) The physiology of brain histamine. Prog Neurobiol 63:637–672.PubMedCrossRefGoogle Scholar
  51. Brown RE, Fedorov NB, Haas HL, Reymann KG (1995) Histaminergic modulation of synaptic plasticity in area CA1 of rat hippocampal slices. Neuropharmacology 34:181–190.PubMedCrossRefGoogle Scholar
  52. Buckley NJ, Bonner TI, Brann MR (1988) Localization of a family of muscarinic receptor mRNAs in rat brain. J Neurosci 8:4646–4652.PubMedGoogle Scholar
  53. Buhler AV, Dunwiddie TV (2001) Regulation of the activity of hippocampal stratum oriens interneurons by alpha7 nicotinic acetylcholine receptors. Neuroscience 106:55–67.PubMedCrossRefGoogle Scholar
  54. Burke SP, Nadler JV (1988) Regulation of glutamate and aspartate release from slices of the hippocampal CA1 area: effects of adenosine and baclofen. J Neurochem 51:1541–1551.PubMedCrossRefGoogle Scholar
  55. Bushell TJ, Plevin R, Cobb S, Irving AJ (2006) Characterization of proteinase-activated receptor 2 signalling and expression in rat hippocampal neurons and astrocytes. Neuropharmacology 50:714–725.PubMedCrossRefGoogle Scholar
  56. Cea del Rio CA, Erdelyi F, Szabo G, Mcbain CJ, Lawrence JJ (2008) Neurochemical identity governs cholinergic phenotype across hippocampal basket cell networks. Society for Neuroscience Abstracts Online 532.12.Google Scholar
  57. Chameau P, van Hooft JA (2006) Serotonin 5-HT(3) receptors in the central nervous system. Cell Tissue Res 326:573–581.PubMedCrossRefGoogle Scholar
  58. Chang M, Saito H, Abe K (1998) Histamine H3 receptor-mediated inhibition of excitatory synaptic transmission in the rat dentate gyrus in vivo. Jpn J Pharmacol 77:251–255.PubMedCrossRefGoogle Scholar
  59. Chang Q, Fischbach GD (2006) An acute effect of neuregulin 1 beta to suppress alpha 7-containing nicotinic acetylcholine receptors in hippocampal interneurons. J Neurosci 26:11295–11303.PubMedCrossRefGoogle Scholar
  60. Chapman CA, Lacaille JC (1999) Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J Neurosci 19:\break8637–8645.PubMedGoogle Scholar
  61. Chen C, Diaz Brinton RD, Shors TJ, Thompson RF (1993) Vasopressin induction of long-lasting potentiation of synaptic transmission in the dentate gyrus. Hippocampus 3:193–203.PubMedCrossRefGoogle Scholar
  62. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461–472.PubMedCrossRefGoogle Scholar
  63. Chevaleyre V, Takahashi KA, Castillo PE (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29:37–76.PubMedCrossRefGoogle Scholar
  64. Clemett DA, Punhani T, Duxon MS, Blackburn TP, Fone KC (2000) Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS. Neuropharmacology 39:123–132.PubMedCrossRefGoogle Scholar
  65. Cobb SR, Davies CH (2005) Cholinergic modulation of hippocampal cells and circuits. J Physiol 562:81–88.PubMedCrossRefGoogle Scholar
  66. Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221:1299–1301.PubMedCrossRefGoogle Scholar
  67. Cole AE, Nicoll RA (1984a) Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol 352:173–188.PubMedGoogle Scholar
  68. Cole AE, Nicoll RA (1984b) The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells. Brain Res 305:283–290.PubMedCrossRefGoogle Scholar
  69. Colino A, Halliwell JV (1987) Differential modulation of three separate K-conductances in hippocampal CA1 neurons by serotonin. Nature 328:73–77.PubMedCrossRefGoogle Scholar
  70. Colino A, Halliwell JV (1993) Carbachol potentiates Q current and activates a calcium-dependent non-specific conductance in rat hippocampus in vitro. Eur J Neurosci 5:1198–1209.PubMedCrossRefGoogle Scholar
  71. Corradetti R, Ballerini L, Pugliese AM, Pepeu G (1992) Serotonin blocks the long-term potentiation induced by primed burst stimulation in the CA1 region of rat hippocampal slices. Neuroscience 46:511–518.PubMedCrossRefGoogle Scholar
  72. Couey JJ, Meredith RM, Spijker S, Poorthuis RB, Smit AB, Brussaard AB, Mansvelder HD (2007) Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54:73–87.PubMedCrossRefGoogle Scholar
  73. Cox DJ, Racca C, LeBeau FE (2008) Beta-adrenergic receptors are differentially expressed in distinct interneuron subtypes in the rat hippocampus. J Comp Neurol 509:551–565.PubMedCrossRefGoogle Scholar
  74. Cunha RA, Milusheva E, Vizi ES, Ribeiro JA, Sebastiao AM (1994) Excitatory and inhibitory effects of A1 and A2A adenosine receptor activation on the electrically evoked [3H]acetylcholine release from different areas of the rat hippocampus. J Neurochem 63:207–214.PubMedGoogle Scholar
  75. Cunha-Reis D, Ribeiro JA, Sebastiao AM (2005) VIP enhances synaptic transmission to hippocampal CA1 pyramidal cells through activation of both VPAC1 and VPAC2 receptors. Brain Res 1049:52–60.PubMedCrossRefGoogle Scholar
  76. Cunha-Reis D, Sebastiao AM, Wirkner K, Illes P, Ribeiro JA (2004) VIP enhances both pre- and postsynaptic GABAergic transmission to hippocampal interneurones leading to increased excitatory synaptic transmission to CA1 pyramidal cells. Br J Pharmacol 143:733–744.PubMedCrossRefGoogle Scholar
  77. Davies S, Kohler C (1985) The substance P innervation of the rat hippocampal region. Anat Embryol (Berl) 173:45–52.CrossRefGoogle Scholar
  78. Day HE, Campeau S, Watson Jr SJ, Akil H (1997) Distribution of alpha 1a-, alpha 1b- and alpha 1d-adrenergic receptor mRNA in the rat brain and spinal cord. J Chem Neuroanat 13:115–139.PubMedCrossRefGoogle Scholar
  79. de Lecea L, Sutcliffe JG (1996) Peptides, sleep and cortistatin. Mol Psychiatry 1:349–351.PubMedGoogle Scholar
  80. de Lecea L, del Rio JA, Criado JR, Alcantara S, Morales M, Danielson PE, Henriksen SJ, Soriano E, Sutcliffe JG (1997) Cortistatin is expressed in a distinct subset of cortical interneurons. J Neurosci 17:5868–5880.PubMedGoogle Scholar
  81. Deisseroth K, Feng G, Majewska AK, Miesenbock G, Ting A, Schnitzer MJ (2006) Next-generation optical technologies for illuminating genetically targeted brain circuits. J Neurosci 26:10380–10386.PubMedCrossRefGoogle Scholar
  82. Deller T, Katona I, Cozzari C, Frotscher M, Freund TF (1999) Cholinergic innervation of mossy cells in the rat fascia dentata. Hippocampus 9:314–320.PubMedCrossRefGoogle Scholar
  83. Deng PY, Lei S (2008) Serotonin increases GABA release in rat entorhinal cortex by inhibiting interneuron TASK-3 K$+$ channels. Mol Cell Neurosci 39:273–284.PubMedCrossRefGoogle Scholar
  84. Deng PY, Porter JE, Shin HS, Lei S (2006) Thyrotropin-releasing hormone increases GABA release in rat hippocampus. J Physiol 577:497–511.PubMedCrossRefGoogle Scholar
  85. Dinerman JL, Dawson TM, Schell MJ, Snowman A, Snyder SH (1994) Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc Natl Acad Sci U S A 91:4214–4218.PubMedCrossRefGoogle Scholar
  86. Dodd J, Kelly JS (1979) Excitation of CA1 pyramidal neurones of the hippocampus by the tetra- and octapeptide C-terminal fragments of cholecystokinin [proceedings]. J Physiol 295:61P–62P.Google Scholar
  87. Dodd J, Dingledine R, Kelly JS (1981) The excitatory action of acetylcholine on hippocampal neurones of the guinea pig and rat maintained in vitro. Brain Res 207:109–127.PubMedCrossRefGoogle Scholar
  88. Dorostkar MM, Boehm S (2007) Opposite effects of presynaptic 5-HT3 receptor activation on spontaneous and action potential-evoked GABA release at hippocampal synapses. J Neurochem 100:395–405.PubMedCrossRefGoogle Scholar
  89. Dougherty KD, Milner TA (1999) Cholinergic septal afferent terminals preferentially contact neuropeptide Y-containing interneurons compared to parvalbumin-containing interneurons in the rat dentate gyrus. J Neurosci 19:10140–10152.PubMedGoogle Scholar
  90. Doze VA, Cohen GA, Madison DV (1991) Synaptic localization of adrenergic disinhibition in the rat hippocampus. Neuron 6:889–900.PubMedCrossRefGoogle Scholar
  91. Dreifuss JJ, Raggenbass M (1986) Tachykinins and bombesin excite non-pyramidal neurones in rat hippocampus. J Physiol 379:417–428.PubMedGoogle Scholar
  92. Dubrovsky B, Harris J, Gijsbers K, Tatarinov A (2002) Oxytocin induces long-term depression on the rat dentate gyrus: possible ATPase and ectoprotein kinase mediation. Brain Res Bull 58:141–147.PubMedCrossRefGoogle Scholar
  93. Dunwiddie TV, Hoffer BJ (1980) Adenine nucleotides and synaptic transmission in the in vitro rat hippocampus. Br J Pharmacol 69:59–68.PubMedGoogle Scholar
  94. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31–55.PubMedCrossRefGoogle Scholar
  95. Dutar P, Bassant MH, Senut MC, Lamour Y (1995) The septohippocampal pathway: structure and function of a central cholinergic system. Physiol Rev 75:393–427.PubMedGoogle Scholar
  96. Ebihara S, Akaike N (1993) Potassium currents operated by thyrotrophin-releasing hormone in dissociated CA1 pyramidal neurones of rat hippocampus. J Physiol 472:689–710.PubMedGoogle Scholar
  97. El-Ghundi M, Fletcher PJ, Drago J, Sibley DR, O’Dowd BF, George SR (1999) Spatial learning deficit in dopamine D(1) receptor knockout mice. Eur J Pharmacol 383:95–106.PubMedCrossRefGoogle Scholar
  98. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG, Fine A (2001) Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21:7993–8003.PubMedGoogle Scholar
  99. Fanselow EE, Richardson KA, Connors BW (2008) Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100:2640–2652.PubMedCrossRefGoogle Scholar
  100. Feil R, Kleppisch T (2008) NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol 184:529–560.PubMedCrossRefGoogle Scholar
  101. Ferezou I, Cauli B, Hill EL, Rossier J, Hamel E, Lambolez B (2002) 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J Neurosci 22:7389–7397.PubMedGoogle Scholar
  102. Fernandez de Sevilla D, Nunez A, Borde M, Malinow R, Buno W (2008) Cholinergic-mediated IP3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons. J Neurosci 28:1469–1478.CrossRefGoogle Scholar
  103. Ferraguti F, Klausberger T, Cobden P, Baude A, Roberts JD, Szucs P, Kinoshita A, Shigemoto R, Somogyi P, Dalezios Y (2005) Metabotropic glutamate receptor 8-expressing nerve terminals target subsets of GABAergic neurons in the hippocampus. J Neurosci 25:10520–10536.PubMedCrossRefGoogle Scholar
  104. Ferster D, Jagadeesh B (1992) EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. J Neurosci 12:1262–1274.PubMedGoogle Scholar
  105. Filippov AK, Choi RC, Simon J, Barnard EA, Brown DA (2006) Activation of P2Y1 nucleotide receptors induces inhibition of the M-type K+ current in rat hippocampal pyramidal neurons. J Neurosci 26:9340–9348.PubMedCrossRefGoogle Scholar
  106. Fink KB, Gothert M (2007) 5-HT receptor regulation of neurotransmitter release. Pharmacol Rev 59:360–417.PubMedGoogle Scholar
  107. Foldy C, Neu A, Jones MV, Soltesz I (2006) Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release. J Neurosci 26:1465–1469.PubMedCrossRefGoogle Scholar
  108. Foldy C, Lee SY, Szabadics J, Neu A, Soltesz I (2007) Cell type-specific gating of perisomatic inhibition by cholecystokinin. Nat Neurosci 10:1128–1130.PubMedCrossRefGoogle Scholar
  109. Frade JG, Barbosa RM, Laranjinha J (2008) Stimulation of NMDA and AMPA glutamate receptors elicits distinct concentration dynamics of nitric oxide in rat hippocampal slices. Hippocampus 19:603–611.CrossRefGoogle Scholar
  110. Fraser DD, MacVicar BA (1996) Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 16:4113–4128.PubMedGoogle Scholar
  111. Frazier CJ, Strowbridge BW, Papke RL (2003) Nicotinic receptors on local circuit neurons in dentate gyrus: a potential role in regulation of granule cell excitability. J Neurophysiol 89:3018–3028.PubMedCrossRefGoogle Scholar
  112. Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV (1998a) Synaptic potentials mediated via alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 18:8228–8235.PubMedGoogle Scholar
  113. Frazier CJ, Rollins YD, Breese CR, Leonard S, Freedman R, Dunwiddie TV (1998b) Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J Neurosci 18:1187–1195.PubMedGoogle Scholar
  114. Fredholm BB, Dunwiddie TV (1988) How does adenosine inhibit transmitter release? Trends Pharmacol Sci 9:130–134.PubMedCrossRefGoogle Scholar
  115. Fredholm BB, Chen JF, Cunha RA, Svenningsson P, Vaugeois JM (2005) Adenosine and brain function. Int Rev Neurobiol 63:191–270.PubMedCrossRefGoogle Scholar
  116. Freedman R, Wetmore C, Stromberg I, Leonard S, Olson L (1993) Alpha-bungarotoxin binding to hippocampal interneurons: immunocytochemical characterization and effects on growth factor expression. J Neurosci 13:1965–1975.PubMedGoogle Scholar
  117. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470.PubMedCrossRefGoogle Scholar
  118. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33–42.PubMedCrossRefGoogle Scholar
  119. Freund TF, Gulyas AI, Acsady L, Gorcs T, Toth K (1990) Serotonergic control of the hippocampus via local inhibitory interneurons. Proc Natl Acad Sci U S A 87:8501–8505.PubMedCrossRefGoogle Scholar
  120. Freund TF, Hajos N, Acsady L, Gorcs TJ, Katona I (1997) Mossy cells of the rat dentate gyrus are immunoreactive for calcitonin gene-related peptide (CGRP). Eur J Neurosci 9:1815–1830.PubMedCrossRefGoogle Scholar
  121. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661–1664.PubMedCrossRefGoogle Scholar
  122. Frotscher M, Leranth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239:237–246.PubMedCrossRefGoogle Scholar
  123. Frotscher M, Schlander M, Leranth C (1986) Cholinergic neurons in the hippocampus. A combined light- and electron-microscopic immunocytochemical study in the rat. Cell Tissue Res 246:293–301.PubMedCrossRefGoogle Scholar
  124. Frotscher M, Vida I, Bender R (2000) Evidence for the existence of non-GABAergic, cholinergic interneurons in the rodent hippocampus. Neuroscience 96:27–31.PubMedCrossRefGoogle Scholar
  125. Fukudome Y, Ohno-Shosaku T, Matsui M, Omori Y, Fukaya M, Tsubokawa H, Taketo MM, Watanabe M, Manabe T, Kano M (2004) Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur J Neurosci 19:2682–2692.PubMedCrossRefGoogle Scholar
  126. Gao C, Sun X, Wolf ME (2006) Activation of D1 dopamine receptors increases surface expression of AMPA receptors and facilitates their synaptic incorporation in cultured hippocampal neurons. J Neurochem 98:1664–1677.PubMedCrossRefGoogle Scholar
  127. Gao WJ, Goldman-Rakic PS (2003) Selective modulation of excitatory and inhibitory microcircuits by dopamine. Proc Natl Acad Sci U S A 100:2836–2841.PubMedCrossRefGoogle Scholar
  128. Gao WJ, Wang Y, Goldman-Rakic PS (2003) Dopamine modulation of perisomatic and peridendritic inhibition in prefrontal cortex. J Neurosci 23:1622–1630.PubMedGoogle Scholar
  129. Garthwaite J (2008) Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27:2783–2802.PubMedCrossRefGoogle Scholar
  130. Garthwaite J, Boulton CL (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683–706.PubMedCrossRefGoogle Scholar
  131. Gasbarri A, Sulli A, Packard MG (1997) The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21:1–22.PubMedCrossRefGoogle Scholar
  132. Gasbarri A, Packard MG, Campana E, Pacitti C (1994) Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33:445–452.PubMedCrossRefGoogle Scholar
  133. Gasbarri A, Sulli A, Innocenzi R, Pacitti C, Brioni JD (1996) Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat. Neuroscience 74:1037–1044.PubMedGoogle Scholar
  134. Ge S, Dani JA (2005) Nicotinic acetylcholine receptors at glutamate synapses facilitate long-term depression or potentiation. J Neurosci 25:6084–6091.PubMedCrossRefGoogle Scholar
  135. Gibbs ME, Summers RJ (2002) Role of adrenoceptor subtypes in memory consolidation. Prog Neurobiol 67:345–391.PubMedCrossRefGoogle Scholar
  136. Gingrich MB, Junge CE, Lyuboslavsky P, Traynelis SF (2000) Potentiation of NMDA receptor function by the serine protease thrombin. J Neurosci 20:4582–4595.PubMedGoogle Scholar
  137. Giocomo LM, Hasselmo ME (2005) Nicotinic modulation of glutamatergic synaptic transmission in region CA3 of the hippocampus. Eur J Neurosci 22:1349–1356.PubMedCrossRefGoogle Scholar
  138. Giocomo LM, Hasselmo ME (2007) Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Mol Neurobiol 36:184–200.PubMedCrossRefGoogle Scholar
  139. Glickfeld LL, Scanziani M (2006) Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat Neurosci 9:807–815.PubMedCrossRefGoogle Scholar
  140. Glickfeld LL, Atallah BV, Scanziani M (2008) Complementary modulation of somatic inhibition by opioids and cannabinoids. J Neurosci 28:1824–1832.PubMedCrossRefGoogle Scholar
  141. Goldsmith SK, Joyce JN (1994) Dopamine D2 receptor expression in hippocampus and parahippocampal cortex of rat, cat, and human in relation to tyrosine hydroxylase-immunoreactive fibers. Hippocampus 4:354–373.PubMedCrossRefGoogle Scholar
  142. Gong S, Doughty M, Harbaugh CR, Cummins A, Hatten ME, Heintz N, Gerfen CR (2007) Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci 27:9817–9823.PubMedCrossRefGoogle Scholar
  143. Gonzalez-Burgos G, Kroener S, Seamans JK, Lewis DA, Barrionuevo G (2005) Dopaminergic modulation of short-term synaptic plasticity in fast-spiking interneurons of primate dorsolateral prefrontal cortex. J Neurophysiol 94:4168–4177.PubMedCrossRefGoogle Scholar
  144. Gorelova N, Seamans JK, Yang CR (2002) Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J Neurophysiol 88:3150–3166.PubMedCrossRefGoogle Scholar
  145. Gray R, Johnston D (1987) Noradrenaline and beta-adrenoceptor agonists increase activity of voltage-dependent calcium channels in hippocampal neurons. Nature 327:620–622.PubMedCrossRefGoogle Scholar
  146. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713–716.PubMedCrossRefGoogle Scholar
  147. Greene RW, Haas HL (1990) Effects of histamine on dentate granule cells in vitro. Neuroscience 34:299–303.PubMedCrossRefGoogle Scholar
  148. Gribkoff VK, Ashe JH (1984) Modulation by dopamine of population responses and cell membrane properties of hippocampal CA1 neurons in vitro. Brain Res 292:327–338.PubMedCrossRefGoogle Scholar
  149. Gulledge AT, Kawaguchi Y (2007) Phasic cholinergic signaling in the hippocampus: functional homology with the neocortex? Hippocampus 17:327–332.PubMedCrossRefGoogle Scholar
  150. Gulledge AT, Park SB, Kawaguchi Y, Stuart GJ (2007) Heterogeneity of phasic cholinergic signaling in neocortical neurons. J Neurophysiol 97:2215–2229.PubMedCrossRefGoogle Scholar
  151. Gulyas AI, Acsady L, Freund TF (1999) Structural basis of the cholinergic and serotonergic modulation of GABAergic neurons in the hippocampus. Neurochem Int 34:359–372.PubMedCrossRefGoogle Scholar
  152. Gustafson EL, Durkin MM, Bard JA, Zgombick J, Branchek TA (1996) A receptor autoradiographic and in situ hybridization analysis of the distribution of the 5-ht7 receptor in rat brain. Br J Pharmacol 117:657–666.PubMedGoogle Scholar
  153. Haas H, Panula P (2003) The role of histamine and the tuberomamillary nucleus in the nervous system. Nat Rev Neurosci 4:121–130.PubMedCrossRefGoogle Scholar
  154. Haas HL, Konnerth A (1983) Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature 302:432–434.PubMedCrossRefGoogle Scholar
  155. Haas HL, Greene RW (1986) Effects of histamine on hippocampal pyramidal cells of the rat in vitro. Exp Brain Res 62:123–130.PubMedCrossRefGoogle Scholar
  156. Haas HL, Rose GM (1987) Noradrenaline blocks potassium conductance in rat dentate granule cells in vitro. Neurosci Lett 78:171–174.PubMedCrossRefGoogle Scholar
  157. Haas HL, Gahwiler BH (1992) Vasoactive intestinal polypeptide modulates neuronal excitability in hippocampal slices of the rat. Neuroscience 47:273–277.PubMedCrossRefGoogle Scholar
  158. Haas HL, Sergeeva OA, Selbach O (2008) Histamine in the nervous system. Physiol Rev 88:1183–1241.PubMedCrossRefGoogle Scholar
  159. Haas HL, Hermann A, Greene RW, Chan-Palay V (1987) Action and location of neuropeptide tyrosine (Y) on hippocampal neurons of the rat in slice preparations. J Comp Neurol 257:208–215.PubMedCrossRefGoogle Scholar
  160. Habib D, Dringenberg HC (2009) Alternating low frequency stimulation of medial septal and commissural fibers induces NMDA-dependent, long-lasting potentiation of hippocampal synapses in urethane-anesthetized rats. Hippocampus 19:299–307.PubMedCrossRefGoogle Scholar
  161. Hajos N, Papp EC, Acsady L, Levey AI, Freund TF (1998) Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 82:355–376.PubMedCrossRefGoogle Scholar
  162. Haley JE, Schaible E, Pavlidis P, Murdock A, Madison DV (1996) Basal and apical synapses of CA1 pyramidal cells employ different LTP induction mechanisms. Learn Mem 3:289–295.PubMedCrossRefGoogle Scholar
  163. Hallbeck M, Hermanson O, Blomqvist A (1999) Distribution of preprovasopressin mRNA in the rat central nervous system. J Comp Neurol 411:181–200.PubMedCrossRefGoogle Scholar
  164. Halliwell JV (1990) Physiological mechanisms of cholinergic action in the hippocampus. Prog Brain Res 84:255–272.PubMedCrossRefGoogle Scholar
  165. Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71–92.PubMedCrossRefGoogle Scholar
  166. Hammad H, Wagner JJ (2006) Dopamine-mediated disinhibition in the CA1 region of rat hippocampus via D3 receptor activation. J Pharmacol Exp Ther 316:113–120.PubMedCrossRefGoogle Scholar
  167. Harley CW (2007) Norepinephrine and the dentate gyrus. Prog Brain Res 163:299–318.PubMedCrossRefGoogle Scholar
  168. Harvey J (2007) Leptin: a diverse regulator of neuronal function. J Neurochem 100:307–313.PubMedCrossRefGoogle Scholar
  169. Hasselmo ME (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16:710–715.PubMedCrossRefGoogle Scholar
  170. Hasselmo ME, Schnell E (1994) Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14:3898–3914.PubMedGoogle Scholar
  171. Haug T, Storm JF (2000) Protein kinase A mediates the modulation of the slow Ca(2+)-dependent K(+) current, I(sAHP), by the neuropeptides CRF, VIP, and CGRP in hippocampal pyramidal neurons. J Neurophysiol 83:2071–2079.PubMedGoogle Scholar
  172. Hefft S, Hulo S, Bertrand D, Muller D (1999) Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol 515(Pt 3):769–776.PubMedCrossRefGoogle Scholar
  173. Henny P, Jones BE (2008) Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci 27:654–670.PubMedCrossRefGoogle Scholar
  174. Henstridge CM, Balenga NA, Ford LA, Ross RA, Waldhoer M, Irving AJ (2009) The GPR55 ligand L-alpha-lysophosphatidylinositol promotes RhoA-dependent Ca2+ signaling and NFAT activation. Faseb J 23:183–193.PubMedCrossRefGoogle Scholar
  175. Hillman KL, Lei S, Doze VA, Porter JE (2009) Alpha-1A adrenergic receptor activation increases inhibitory tone in CA1 hippocampus. Epilepsy Res 84:97–109.PubMedCrossRefGoogle Scholar
  176. Hillman KL, Knudson CA, Carr PA, Doze VA, Porter JE (2005) Adrenergic receptor characterization of CA1 hippocampal neurons using real time single cell RT-PCR. Brain Res Mol Brain Res 139:267–276.PubMedCrossRefGoogle Scholar
  177. Hollins C, Stone TW (1980) Adenosine inhibition of gamma-aminobutyric acid release from slices of rat cerebral cortex. Br J Pharmacol 69:107–112.PubMedGoogle Scholar
  178. Holscher C, Anwyl R, Rowan MJ (1997) Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can Be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 17:6470–6477.PubMedGoogle Scholar
  179. Hsu KS (1996) Characterization of dopamine receptors mediating inhibition of excitatory synaptic transmission in the rat hippocampal slice. J Neurophysiol 76:1887–1895.PubMedGoogle Scholar
  180. Huang YY, Kandel ER (1995) D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A 92:2446–2450.PubMedCrossRefGoogle Scholar
  181. Huerta PT, Lisman JE (1993) Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723–725.PubMedCrossRefGoogle Scholar
  182. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (2003) Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725–11731.PubMedGoogle Scholar
  183. Ihalainen JA, Riekkinen P, Jr., Feenstra MG (1999) Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neurosci Lett 277:71–74.PubMedCrossRefGoogle Scholar
  184. Ikeuchi Y, Nishizaki T, Okada Y (1996) Repetitive applications of ATP potentiate potassium current by Ca2+/calmodulin kinase in cultured rat hippocampal neurons. Neurosci Lett 203:115–118.PubMedCrossRefGoogle Scholar
  185. Illes P, Nieber K, Norenberg W (1996) Electrophysiological effects of ATP on brain neurones. J Auton Pharmacol 16:407–411.PubMedCrossRefGoogle Scholar
  186. Inagaki N, Yamatodani A, Ando-Yamamoto M, Tohyama M, Watanabe T, Wada H (1988) Organization of histaminergic fibers in the rat brain. J Comp Neurol 273:283–300.PubMedCrossRefGoogle Scholar
  187. Inoue K, Koizumi S, Ueno S, Kita A, Tsuda M (1999) The functions of ATP receptors in the synaptic transmission in the hippocampus. Prog Brain Res 120:193–206.PubMedCrossRefGoogle Scholar
  188. Ishihara K, Katsuki H, Sugimura M, Satoh M (1992) YM-14673, a new thyrotropin-releasing hormone analog, augments long-term potentiation in the mossy fiber-CA3 system of guinea pig hippocampal slices. J Pharmacobiodyn 15:75–78.PubMedGoogle Scholar
  189. Ito HT, Schuman EM (2007) Frequency-dependent gating of synaptic transmission and plasticity by dopamine. Front Neural Circuits 1:1.PubMedCrossRefGoogle Scholar
  190. Jagadeesh B, Gray CM, Ferster D (1992) Visually evoked oscillations of membrane potential in cells of cat visual cortex. Science 257:552–554.PubMedCrossRefGoogle Scholar
  191. Jahnsen H (1980) The action of 5-hydroxytryptamine on neuronal membranes and synaptic transmission in area CA1 of the hippocampus in vitro. Brain Res 197:83–94.PubMedCrossRefGoogle Scholar
  192. Jia Y, Yamazaki Y, Nakauchi S, Sumikawa K (2009) Alpha2 nicotine receptors function as a molecular switch to continuously excite a subset of interneurons in rat hippocampal circuits. Eur J Neurosci 29:1588–1603.PubMedCrossRefGoogle Scholar
  193. Jones BE (2004) Activity, modulation and role of basal forebrain cholinergic neurons innervating the cerebral cortex. Prog Brain Res 145:157–169.PubMedCrossRefGoogle Scholar
  194. Jones JD, Carney ST, Vrana KE, Norford DC, Howlett AC (2008) Cannabinoid receptor-mediated translocation of NO-sensitive guanylyl cyclase and production of cyclic GMP in neuronal cells. Neuropharmacology 54:23–30.PubMedCrossRefGoogle Scholar
  195. Jones S, Yakel JL (1997) Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J Physiol 504(Pt 3):603–610.PubMedCrossRefGoogle Scholar
  196. Kahle JS, Cotman CW (1989) Carbachol depresses synaptic responses in the medial but not the lateral perforant path. Brain Res 482:159–163.PubMedCrossRefGoogle Scholar
  197. Kajimoto T, Okada T, Yu H, Goparaju SK, Jahangeer S, Nakamura S (2007) Involvement of sphingosine-1-phosphate in glutamate secretion in hippocampal neurons. Mol Cell Biol 27:3429–3440.PubMedCrossRefGoogle Scholar
  198. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380.PubMedCrossRefGoogle Scholar
  199. Karson MA, Whittington KC, Alger BE (2008) Cholecystokinin inhibits endocannabinoid-sensitive hippocampal IPSPs and stimulates others. Neuropharmacology 54:117–128.PubMedCrossRefGoogle Scholar
  200. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544–4558.PubMedGoogle Scholar
  201. Katona I, Urban GM, Wallace M, Ledent C, Jung KM, Piomelli D, Mackie K, Freund TF (2006) Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26:5628–5637.PubMedCrossRefGoogle Scholar
  202. Katsurabayashi S, Kubota H, Tokutomi N, Akaike N (2003) A distinct distribution of functional presynaptic 5-HT receptor subtypes on GABAergic nerve terminals projecting to single hippocampal CA1 pyramidal neurons. Neuropharmacology 44:1022–1030.PubMedCrossRefGoogle Scholar
  203. Katz PS, Frost WN (1996) Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19:54–61.PubMedCrossRefGoogle Scholar
  204. Kawa K (1994) Distribution and functional properties of 5-HT3 receptors in the rat hippocampal dentate gyrus: a patch-clamp study. J Neurophysiol 71:1935–1947.PubMedGoogle Scholar
  205. Kawaguchi Y (1997) Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 78:1743–1747.PubMedGoogle Scholar
  206. Kawamura M, Gachet C, Inoue K, Kato F (2004) Direct excitation of inhibitory interneurons by extracellular ATP mediated by P2Y1 receptors in the hippocampal slice. J Neurosci 24:10835–10845.PubMedCrossRefGoogle Scholar
  207. Kearns IR, Morton RA, Bulters DO, Davies CH (2001) Opioid receptor regulation of muscarinic acetylcholine receptor-mediated synaptic responses in the hippocampus. Neuropharmacology 41:565–573.PubMedCrossRefGoogle Scholar
  208. Khakh BS (2009) ATP-gated P2X receptors on excitatory nerve terminals onto interneurons initiate a form of asynchronous glutamate release. Neuropharmacology 56:216–222.PubMedCrossRefGoogle Scholar
  209. Khakh BS, Gittermann D, Cockayne DA, Jones A (2003) ATP modulation of excitatory synapses onto interneurons. J Neurosci 23:7426–7437.PubMedGoogle Scholar
  210. Kim J, Isokawa M, Ledent C, Alger BE (2002) Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:10182–10191.PubMedGoogle Scholar
  211. Kirby MT, Hampson RE, Deadwyler SA (2000) Cannabinoid receptor activation in CA1 pyramidal cells in adult rat hippocampus. Brain Res 863:120–131.PubMedCrossRefGoogle Scholar
  212. Kitamura K, Judkewitz B, Kano M, Denk W, Hausser M (2008) Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat Methods 5:61–67.PubMedCrossRefGoogle Scholar
  213. Klapstein GJ, Colmers WF (1993) On the sites of presynaptic inhibition by neuropeptide Y in rat hippocampus in vitro. Hippocampus 3:103–111.PubMedCrossRefGoogle Scholar
  214. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57.PubMedCrossRefGoogle Scholar
  215. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsaki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844–848.PubMedCrossRefGoogle Scholar
  216. Kobayashi K, Suzuki H (2007) Dopamine selectively potentiates hippocampal mossy fiber to CA3 synaptic transmission. Neuropharmacology 52:552–561.PubMedCrossRefGoogle Scholar
  217. 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 103:1059–1064.PubMedCrossRefGoogle Scholar
  218. Kojima T, Matsumoto M, Togashi H, Tachibana K, Kemmotsu O, Yoshioka M (2003) Fluvoxamine suppresses the long-term potentiation in the hippocampal CA1 field of anesthetized rats: an effect mediated via 5-HT1A receptors. Brain Res 959:165–168.PubMedCrossRefGoogle Scholar
  219. Kouznetsova M, Nistri A (1998) Modulation by substance P of synaptic transmission in the mouse hippocampal slice. Eur J Neurosci 10:3076–3084.PubMedCrossRefGoogle Scholar
  220. Kremin T, Hasselmo ME (2007) Cholinergic suppression of glutamatergic synaptic transmission in hippocampal region CA3 exhibits laminar selectivity: implication for hippocampal network dynamics. Neuroscience 149:760–767.PubMedCrossRefGoogle Scholar
  221. Kremin T, Gerber D, Giocomo LM, Huang SY, Tonegawa S, Hasselmo ME (2006) Muscarinic suppression in stratum radiatum of CA1 shows dependence on presynaptic M1 receptors and is not dependent on effects at GABA(B) receptors. Neurobiol Learn Mem 85:153–163.PubMedCrossRefGoogle Scholar
  222. Kroner S, Krimer LS, Lewis DA, Barrionuevo G (2007) Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons. Cereb Cortex 17:1020–1032.PubMedCrossRefGoogle Scholar
  223. Kulik A, Vida I, Fukazawa Y, Guetg N, Kasugai Y, Marker CL, Rigato F, Bettler B, Wickman K, Frotscher M, Shigemoto R (2006) Compartment-dependent colocalization of Kir3.2-containing K+ channels and GABAB receptors in hippocampal pyramidal cells. J Neurosci 26:4289–4297.PubMedCrossRefGoogle Scholar
  224. Lacaille JC, Schwartzkroin PA (1988) Intracellular responses of rat hippocampal granule cells in vitro to discrete applications of norepinephrine. Neurosci Lett 89:176–181.PubMedCrossRefGoogle Scholar
  225. Lauckner JE, Jensen JB, Chen HY, Lu HC, Hille B, Mackie K (2008) GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proc Natl Acad Sci U S A 105:2699–2704.PubMedCrossRefGoogle Scholar
  226. Lawrence JJ (2007) Homosynaptic and heterosynaptic modes of endocannabinoid action at hippocampal CCK$+$ basket cell synapses. J Physiol 578:3–4.PubMedCrossRefGoogle Scholar
  227. Lawrence JJ (2008) Cholinergic control of GABA release: emerging parallels between neocortex and hippocampus. Trends Neurosci 31:317–327.PubMedCrossRefGoogle Scholar
  228. Lawrence JJ, Mcbain CJ (2007) Pre- and postsynaptic cholinergic neuromodulation of parvalbumin positive (PV+) CA1 basket cells. Society for Neuroscience Abstracts Online 144.13.Google Scholar
  229. Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ (2006a) Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J Physiol 570:595–610.PubMedCrossRefGoogle Scholar
  230. Lawrence JJ, Grinspan ZM, Statland JM, McBain CJ (2006b) Muscarinic receptor activation tunes mouse stratum oriens interneurones to amplify spike reliability. J Physiol 571:555–562.PubMedCrossRefGoogle Scholar
  231. Lawrence JJ, Saraga F, Churchill JF, Statland JM, Travis KE, Skinner FK, McBain CJ (2006c) Somatodendritic Kv7/KCNQ/M channels control interspike interval in hippocampal interneurons. J Neurosci 26:12325–12338.PubMedCrossRefGoogle Scholar
  232. Lawrence JJ, Tricoire L, Cea del Rio CA, Cauli B, Erdelyi F, Szabo G, Mcbain CJ (2008) Hippocampal interneuron subtypes are associated with distinct muscarinic receptor mRNA expression profiles. Society for Neuroscience Abstracts Online 532.11.Google Scholar
  233. Lee K, Dixon AK, Gonzalez I, Stevens EB, McNulty S, Oles R, Richardson PJ, Pinnock RD, Singh L (1999) Bombesin-like peptides depolarize rat hippocampal interneurones through interaction with subtype 2 bombesin receptors. J Physiol 518(Pt 3):791–802.PubMedCrossRefGoogle Scholar
  234. Lee MG, Hassani OK, Alonso A, Jones BE (2005) Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci 25:4365–4369.PubMedCrossRefGoogle Scholar
  235. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsaki G (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033–1047.PubMedCrossRefGoogle Scholar
  236. Leranth C, Frotscher M (1987) Cholinergic innervation of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J Comp Neurol 261:33–47.PubMedCrossRefGoogle Scholar
  237. Levey AI, Edmunds SM, Koliatsos V, Wiley RG, Heilman CJ (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15:4077–4092.PubMedGoogle Scholar
  238. Levkovitz Y, Segal M (1997) Serotonin 5-HT1A receptors modulate hippocampal reactivity to afferent stimulation. J Neurosci 17:5591–5598.PubMedGoogle Scholar
  239. Li S, Cullen WK, Anwyl R, Rowan MJ (2003) Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci 6:526–531.PubMedGoogle Scholar
  240. Lisman JE, Grace AA (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46:703–713.PubMedCrossRefGoogle Scholar
  241. Lopes LV, Cunha RA, Kull B, Fredholm BB, Ribeiro JA (2002) Adenosine A(2A) receptor facilitation of hippocampal synaptic transmission is dependent on tonic A(1) receptor inhibition. Neuroscience 112:319–329.PubMedCrossRefGoogle Scholar
  242. Lopez-Bendito G, Sturgess K, Erdelyi F, Szabo G, Molnar Z, Paulsen O (2004) Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb Cortex 14:1122–1133.PubMedCrossRefGoogle Scholar
  243. Loy R, Koziell DA, Lindsey JD, Moore RY (1980) Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189:699–710.PubMedCrossRefGoogle Scholar
  244. Lucas-Meunier E, Fossier P, Baux G, Amar M (2003) Cholinergic modulation of the cortical neuronal network. Pflugers Arch 446:17–29.PubMedGoogle Scholar
  245. Maccaferri G (2005) Stratum oriens horizontal interneurone diversity and hippocampal network dynamics. J Physiol 562:73–80.PubMedCrossRefGoogle Scholar
  246. 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(Pt 1):119–130.PubMedGoogle Scholar
  247. Maccaferri G, Lacaille JC (2003) Interneuron Diversity series: hippocampal interneuron classifications – making things as simple as possible, not simpler. Trends Neurosci 26:564–571.PubMedCrossRefGoogle Scholar
  248. MacVicar BA, Kerrin JP, Davison JS (1987) Inhibition of synaptic transmission in the hippocampus by cholecystokinin (CCK) and its antagonism by a CCK analog (CCK27-33). Brain Res 406:130–135.PubMedCrossRefGoogle Scholar
  249. Madison DV, Nicoll RA (1982) Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299:636–638.PubMedCrossRefGoogle Scholar
  250. Madison DV, Nicoll RA (1986) Actions of noradrenaline recorded intracellularly in rat hippocampal CA1 pyramidal neurones, in vitro. J Physiol 372:221–244.PubMedGoogle Scholar
  251. Madison DV, Nicoll RA (1988a) Norepinephrine decreases synaptic inhibition in the rat hippocampus. Brain Res 442:131–138.PubMedCrossRefGoogle Scholar
  252. Madison DV, Nicoll RA (1988b) Enkephalin hyperpolarizes interneurones in the rat hippocampus. J Physiol 398:123–130.PubMedGoogle Scholar
  253. Madison DV, McQuiston AR (2006) Toward a unified hypothesis of interneuronal modulation. J Physiol 570:435.PubMedCrossRefGoogle Scholar
  254. Madison DV, Lancaster B, Nicoll RA (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7:733–741.PubMedGoogle Scholar
  255. Maeda T, Kaneko S, Satoh M (1994) Inhibitory influence via 5-HT3 receptors on the induction of LTP in mossy fiber-CA3 system of guinea-pig hippocampal slices. Neurosci Res 18:277–282.PubMedCrossRefGoogle Scholar
  256. Makara JK, Katona I, Nyiri G, Nemeth B, Ledent C, Watanabe M, de Vente J, Freund TF, Hajos N (2007) Involvement of nitric oxide in depolarization-induced suppression of inhibition in hippocampal pyramidal cells during activation of cholinergic receptors. J Neurosci 27:10211–10222.PubMedCrossRefGoogle Scholar
  257. Malenka RC, Nicoll RA (1986) Dopamine decreases the calcium-activated afterhyperpolarization in hippocampal CA1 pyramidal cells. Brain Res 379:210–215.PubMedCrossRefGoogle Scholar
  258. Manaker S, Winokur A, Rostene WH, Rainbow TC (1985) Autoradiographic localization of thyrotropin-releasing hormone receptors in the rat central nervous system. J Neurosci 5:167–174.PubMedGoogle Scholar
  259. Manseau F, Goutagny R, Danik M, Williams S (2008) The hippocamposeptal pathway generates rhythmic firing of GABAergic neurons in the medial septum and diagonal bands: an investigation using a complete septohippocampal preparation in vitro. J Neurosci 28:4096–4107.PubMedCrossRefGoogle Scholar
  260. Markram H, Segal M (1990a) Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J Physiol 427:381–393.PubMedGoogle Scholar
  261. Markram H, Segal M (1990b) Acetylcholine potentiates responses to N-methyl-D-aspartate in the rat hippocampus. Neurosci Lett 113:62–65.PubMedCrossRefGoogle Scholar
  262. Marsicano G, Lutz B (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11:4213–4225.PubMedCrossRefGoogle Scholar
  263. Martin LA, Wei DS, Alger BE (2001) Heterogeneous susceptibility of GABA(A) receptor-mediated IPSCs to depolarization-induced suppression of inhibition in rat hippocampus. J Physiol 532:685–700.PubMedCrossRefGoogle Scholar
  264. Martinez-Mir MI, Pollard H, Moreau J, Arrang JM, Ruat M, Traiffort E, Schwartz JC, Palacios JM (1990) Three histamine receptors (H1, H2 and H3) visualized in the brain of human and non-human primates. Brain Res 526:322–327.PubMedCrossRefGoogle Scholar
  265. Matsumoto M, Kojima T, Togashi H, Mori K, Ohashi S, Ueno K, Yoshioka M (2002) Differential characteristics of endogenous serotonin-mediated synaptic transmission in the hippocampal CA1 and CA3 fields of anaesthetized rats. Naunyn Schmiedebergs Arch Pharmacol 366:570–577.PubMedCrossRefGoogle Scholar
  266. Matthes H, Boschert U, Amlaiky N, Grailhe R, Plassat JL, Muscatelli F, Mattei MG, Hen R (1993) Mouse 5-hydroxytryptamine5A and 5-hydroxytryptamine5B receptors define a new family of serotonin receptors: cloning, functional expression, and chromosomal localization. Mol Pharmacol 43:313–319.PubMedGoogle Scholar
  267. McBain CJ (2008) Differential mechanisms of transmission and plasticity at mossy fiber synapses. Prog Brain Res 169:225–240.PubMedCrossRefGoogle Scholar
  268. McMahon LL, Kauer JA (1997) Hippocampal interneurons are excited via serotonin-gated ion channels. J Neurophysiol 78:2493–2502.PubMedGoogle Scholar
  269. McQuiston AR, Madison DV (1999a) Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 19:2887–2896.PubMedGoogle Scholar
  270. McQuiston AR, Madison DV (1999b) Muscarinic receptor activity induces an afterdepolarization in a subpopulation of hippocampal CA1 interneurons. J Neurosci 19:5703–5710.PubMedGoogle Scholar
  271. McQuiston AR, Madison DV (1999c) Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons. J Neurosci 19:5693–5702.PubMedGoogle Scholar
  272. McQuiston AR, Petrozzino JJ, Connor JA, Colmers WF (1996) Neuropeptide Y1 receptors inhibit N-type calcium currents and reduce transient calcium increases in rat dentate granule cells. J Neurosci 16:1422–1429.PubMedGoogle Scholar
  273. Mercer JG, Hoggard N, Williams LM, Lawrence CB, Hannah LT, Trayhurn P (1996) Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization. FEBS Lett 387:113–116.PubMedCrossRefGoogle Scholar
  274. Miller KK, Hoffer A, Svoboda KR, Lupica CR (1997) Cholecystokinin increases GABA release by inhibiting a resting K+ conductance in hippocampal interneurons. J Neurosci 17:4994–5003.PubMedGoogle Scholar
  275. Milligan G (2007) G protein-coupled receptor dimerisation: molecular basis and relevance to function. Biochim Biophys Acta 1768:825–835.PubMedCrossRefGoogle Scholar
  276. Milner TA, Bacon CE (1989a) GABAergic neurons in the rat hippocampal formation: ultrastructure and synaptic relationships with catecholaminergic terminals. J Neurosci 9:3410–3427.PubMedGoogle Scholar
  277. Milner TA, Bacon CE (1989b) Ultrastructural localization of tyrosine hydroxylase-like immunoreactivity in the rat hippocampal formation. J Comp Neurol 281:479–495.PubMedCrossRefGoogle Scholar
  278. Milner TA, Shah P, Pierce JP (2000) Beta-adrenergic receptors primarily are located on the dendrites of granule cells and interneurons but also are found on astrocytes and a few presynaptic profiles in the rat dentate gyrus. Synapse 36:178–193.PubMedCrossRefGoogle Scholar
  279. Milner TA, Lee A, Aicher SA, Rosin DL (1998) Hippocampal alpha2a-adrenergic receptors are located predominantly presynaptically but are also found postsynaptically and in selective astrocytes. J Comp Neurol 395:310–327.PubMedCrossRefGoogle Scholar
  280. Mitchell JB, Miller K, Dunwiddie TV (1993) Adenosine-induced suppression of synaptic responses and the initiation and expression of long-term potentiation in the CA1 region of the hippocampus. Hippocampus 3:77–86.PubMedCrossRefGoogle Scholar
  281. Miyoshi G, Fishell G (2006) Directing neuron-specific transgene expression in the mouse CNS. Curr Opin Neurobiol 16:577–584.PubMedCrossRefGoogle Scholar
  282. Monyer H, Markram H (2004) Interneuron Diversity series: molecular and genetic tools to study GABAergic interneuron diversity and function. Trends Neurosci 27:90–97.PubMedCrossRefGoogle Scholar
  283. Moore SD, Madamba SG, Joels M, Siggins GR (1988) Somatostatin augments the M-current in hippocampal neurons. Science 239:278–280.PubMedCrossRefGoogle Scholar
  284. Moore SD, Madamba SG, Schweitzer P, Siggins GR (1994) Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro. J Neurosci 14:809–820.PubMedGoogle Scholar
  285. Morales M, Hein K, Vogel Z (2007) Hippocampal interneurons co-express transcripts encoding the alpha7 nicotinic receptor subunit and the cannabinoid receptor 1. Neuroscience 152:70–81.CrossRefGoogle Scholar
  286. Mori M, Heuss C, Gahwiler BH, Gerber U (2001) Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J Physiol 535:115–123.PubMedCrossRefGoogle Scholar
  287. Morton RA, Davies CH (1997) Regulation of muscarinic acetylcholine receptor-mediated synaptic responses by adenosine receptors in the rat hippocampus. J Physiol 502(Pt 1):75–90.PubMedCrossRefGoogle Scholar
  288. Morton RA, Manuel NA, Bulters DO, Cobb SR, Davies CH (2001) Regulation of muscarinic acetylcholine receptor-mediated synaptic responses by GABA(B) receptors in the rat hippocampus. J Physiol 535:757–766.PubMedCrossRefGoogle Scholar
  289. Mrzljak L, Bergson C, Pappy M, Huff R, Levenson R, Goldman-Rakic PS (1996) Localization of dopamine D4 receptors in GABAergic neurons of the primate brain. Nature 381:245–248.PubMedCrossRefGoogle Scholar
  290. Muhlethaler M, Charpak S, Dreifuss JJ (1984) Contrasting effects of neurohypophysial peptides on pyramidal and non-pyramidal neurones in the rat hippocampus. Brain Res 308:97–107.PubMedCrossRefGoogle Scholar
  291. Murchison CF, Zhang XY, Zhang WP, Ouyang M, Lee A, Thomas SA (2004) A distinct role for norepinephrine in memory retrieval. Cell 117:131–143.PubMedCrossRefGoogle Scholar
  292. Muzzio IA, Kentros C, Kandel E (2009) What is remembered? Role of attention on the encoding and retrieval of hippocampal representations. J Physiol 587:2837–2854.PubMedCrossRefGoogle Scholar
  293. Neu A, Foldy C, Soltesz I (2007) Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus. J Physiol 578:233–247.PubMedCrossRefGoogle Scholar
  294. Nicholas AP, Hokfelt T, Pieribone VA (1996) The distribution and significance of CNS adrenoceptors examined with in situ hybridization. Trends Pharmacol Sci 17:245–255.PubMedCrossRefGoogle Scholar
  295. Nicoll RA, Malenka RC, Kauer JA (1990) Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol Rev 70:513–565.PubMedGoogle Scholar
  296. Noriyama Y, Ogawa Y, Yoshino H, Yamashita M, Kishimoto T (2006) Dopamine profoundly suppresses excitatory transmission in neonatal rat hippocampus via phosphatidylinositol-linked D1-like receptor. Neuroscience 138:475–485.PubMedCrossRefGoogle Scholar
  297. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729–738.PubMedCrossRefGoogle Scholar
  298. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M (2002) Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864–3872.PubMedGoogle Scholar
  299. Oleskevich S, Descarries L, Lacaille JC (1989) Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J Neurosci 9:3803–3815.PubMedGoogle Scholar
  300. Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, Myers L, Mora Z, Tagliaferro P, Gardner E, Brusco A, Akinshola BE, Liu QR, Hope B, Iwasaki S, Arinami T, Teasenfitz L, Uhl GR (2006) Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann N Y Acad Sci 1074:514–536.PubMedCrossRefGoogle Scholar
  301. Otmakhova NA, Lisman JE (1996) D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16:7478–7486.PubMedGoogle Scholar
  302. Otmakhova NA, Lisman JE (1998) D1/D5 dopamine receptors inhibit depotentiation at CA1 synapses via cAMP-dependent mechanism. J Neurosci 18:1270–1279.PubMedGoogle Scholar
  303. Otmakhova NA, Lisman JE (1999) Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region. J Neurosci 19:1437–1445.PubMedGoogle Scholar
  304. Otmakhova NA, Lisman JE (2000) Dopamine, serotonin, and noradrenaline strongly inhibit the direct perforant path-CA1 synaptic input, but have little effect on the Schaffer collateral input. Ann N Y Acad Sci 911:462–464.PubMedCrossRefGoogle Scholar
  305. Otmakhova NA, Lewey J, Asrican B, Lisman JE (2005) Inhibition of perforant path input to the CA1 region by serotonin and noradrenaline. J Neurophysiol 94:1413–1422.PubMedCrossRefGoogle Scholar
  306. Packard MG, Cahill L, McGaugh JL (1994) Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc Natl Acad Sci U S A 91:8477–8481.PubMedCrossRefGoogle Scholar
  307. Pagotto U, Marsicano G, Cota D, Lutz B, Pasquali R (2006) The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr Rev 27:73–100.PubMedCrossRefGoogle Scholar
  308. Pankratov Y, Castro E, Miras-Portugal MT, Krishtal O (1998) A purinergic component of the excitatory postsynaptic current mediated by P2X receptors in the CA1 neurons of the rat hippocampus. Eur J Neurosci 10:3898–3902.PubMedCrossRefGoogle Scholar
  309. Pankratov Y, Lalo U, Verkhratsky A, North RA (2006) Vesicular release of ATP at central synapses. Pflugers Arch 452:589–597.PubMedCrossRefGoogle Scholar
  310. Pankratov Y, Lalo U, Krishtal OA, Verkhratsky A (2009) P2X receptors and synaptic plasticity. Neuroscience 158:137–148.PubMedCrossRefGoogle Scholar
  311. Pankratov YV, Lalo UV, Krishtal OA (2002) Role for P2X receptors in long-term potentiation. J Neurosci 22:8363–8369.PubMedGoogle Scholar
  312. Panula P, Pirvola U, Auvinen S, Airaksinen MS (1989) Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience 28:585–610.PubMedCrossRefGoogle Scholar
  313. Papay R, Gaivin R, Jha A, McCune DF, McGrath JC, Rodrigo MC, Simpson PC, Doze VA, Perez DM (2006) Localization of the mouse alpha1A-adrenergic receptor (AR) in the brain: alpha1AAR is expressed in neurons, GABAergic interneurons, and NG2 oligodendrocyte progenitors. J Comp Neurol 497:209–222.PubMedCrossRefGoogle Scholar
  314. Parra P, Gulyas AI, Miles R (1998) How many subtypes of inhibitory cells in the hippocampus? Neuron 20:983–993.PubMedCrossRefGoogle Scholar
  315. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113–116.PubMedCrossRefGoogle Scholar
  316. Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383–387.PubMedCrossRefGoogle Scholar
  317. Pedarzani P, Storm JF (1993) PKA mediates the effects of monoamine transmitters on the K$+$ current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11:1023–1035.PubMedCrossRefGoogle Scholar
  318. Pedarzani P, Storm JF (1995) Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons. J Neurophysiol 74:2749–2753.PubMedGoogle Scholar
  319. Pedarzani P, Storm JF (1996) Interaction between alpha- and beta-adrenergic receptor agonists modulating the slow Ca(2+)-activated K+ current IAHP in hippocampal neurons. Eur J Neurosci 8:2098–2110.PubMedCrossRefGoogle Scholar
  320. Pillot C, Heron A, Cochois V, Tardivel-Lacombe J, Ligneau X, Schwartz JC, Arrang JM (2002) A detailed mapping of the histamine H(3) receptor and its gene transcripts in rat brain. Neuroscience 114:173–193.PubMedCrossRefGoogle Scholar
  321. Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Methods 65:113–136.PubMedCrossRefGoogle Scholar
  322. Pitler TA, Alger BE (1992a) Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12:4122–4132.PubMedGoogle Scholar
  323. Pitler TA, Alger BE (1992b) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450:127–142.PubMedGoogle Scholar
  324. Pittman QJ, Siggins GR (1981) Somatostatin hyperpolarizes hippocampal pyramidal cells in vitro. Brain Res 221:402–408.PubMedCrossRefGoogle Scholar
  325. Pollard H, Moreau J, Arrang JM, Schwartz JC (1993) A detailed autoradiographic mapping of histamine H3 receptors in rat brain areas. Neuroscience 52:169–189.PubMedCrossRefGoogle Scholar
  326. Pompeiano M, Palacios JM, Mengod G (1994) Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res Mol Brain Res 23:163–178.PubMedCrossRefGoogle Scholar
  327. Porter JT, Cauli B, Tsuzuki K, Lambolez B, Rossier J, Audinat E (1999) Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J Neurosci 19:5228–5235.PubMedGoogle Scholar
  328. Power JM, Sah P (2002) Nuclear calcium signaling evoked by cholinergic stimulation in hippocampal CA1 pyramidal neurons. J Neurosci 22:3454–3462.PubMedGoogle Scholar
  329. Pugliese AM, Passani MB, Corradetti R (1998) Effect of the selective 5-HT1A receptor antagonist WAY 100635 on the inhibition of e.p.s.ps produced by 5-HT in the CA1 region of rat hippocampal slices. Br J Pharmacol 124:93–100.PubMedCrossRefGoogle Scholar
  330. Qian J, Saggau P (1997) Presynaptic inhibition of synaptic transmission in the rat hippocampus by activation of muscarinic receptors: involvement of presynaptic calcium influx. Br J Pharmacol 122:511–519.PubMedCrossRefGoogle Scholar
  331. Qiu C, Zeyda T, Johnson B, Hochgeschwender U, de Lecea L, Tallent MK (2008) Somatostatin receptor subtype 4 couples to the M-current to regulate seizures. J Neurosci 28:3567–3576.PubMedCrossRefGoogle Scholar
  332. Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18:7075–7083.PubMedGoogle Scholar
  333. Raggenbass M (2001) Vasopressin- and oxytocin-induced activity in the central nervous system: electrophysiological studies using in-vitro systems. Prog Neurobiol 64:307–326.PubMedCrossRefGoogle Scholar
  334. Rancz EA, Ishikawa T, Duguid I, Chadderton P, Mahon S, Hausser M (2007) High-fidelity transmission of sensory information by single cerebellar mossy fiber boutons. Nature 450:1245–1248.PubMedCrossRefGoogle Scholar
  335. Reece LJ, Schwartzkroin PA (1991) Effects of cholinergic agonists on two non-pyramidal cell types in rat hippocampal slices. Brain Res 566:115–126.PubMedCrossRefGoogle Scholar
  336. Richter-Levin G, Segal M (1996) Serotonin, aging and cognitive functions of the hippocampus. Rev Neurosci 7:103–113.PubMedGoogle Scholar
  337. Romo-Parra H, Aceves J, Gutierrez R (2005) Tonic modulation of inhibition by dopamine D4 receptors in the rat hippocampus. Hippocampus 15:254–259.PubMedCrossRefGoogle Scholar
  338. Ropert N, Guy N (1991) Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampus in vitro. J Physiol 441:121–136.PubMedGoogle Scholar
  339. Rouse ST, Marino MJ, Potter LT, Conn PJ, Levey AI (1999) Muscarinic receptor subtypes involved in hippocampal circuits. Life Sci 64:501–509.PubMedCrossRefGoogle Scholar
  340. Ruat M, Traiffort E, Arrang JM, Tardivel-Lacombe J, Diaz J, Leurs R, Schwartz JC (1993) A novel rat serotonin (5-HT6) receptor: molecular cloning, localization and stimulation of cAMP accumulation. Biochem Biophys Res Commun 193:268–276.PubMedCrossRefGoogle Scholar
  341. Ryberg E, Larsson N, Sjogren S, Hjorth S, Hermansson NO, Leonova J, Elebring T, Nilsson K, Drmota T, Greasley PJ (2007) The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 152:1092–1101.PubMedCrossRefGoogle Scholar
  342. Sakurai O, Kosaka T (2007) Nonprincipal neurons and CA2 pyramidal cells, but not mossy cells are immunoreactive for calcitonin gene-related peptide in the mouse hippocampus. Brain Res 1186:129–143.PubMedCrossRefGoogle Scholar
  343. Sanchez G, Alvares Lde O, Oberholzer MV, Genro B, Quillfeldt J, da Costa JC, Cervenansky C, Jerusalinsky D, Kornisiuk E (2009) M4 muscarinic receptors are involved in modulation of neurotransmission at synapses of Schaffer collaterals on CA1 hippocampal neurons in rats. J Neurosci Res 87:691–700.PubMedCrossRefGoogle Scholar
  344. Sarter M, Hasselmo ME, Bruno JP, Givens B (2005) Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain research 48:98–111.CrossRefGoogle Scholar
  345. Scanziani M, Gahwiler BH, Thompson SM (1993) Presynaptic inhibition of excitatory synaptic transmission mediated by alpha adrenergic receptors in area CA3 of the rat hippocampus in vitro. J Neurosci 13:5393–5401.PubMedGoogle Scholar
  346. Scatton B, Simon H, Le Moal M, Bischoff S (1980) Origin of dopaminergic innervation of the rat hippocampal formation. Neurosci Lett 18:125–131.PubMedCrossRefGoogle Scholar
  347. Scheiderer CL, Smith CC, McCutchen E, McCoy PA, Thacker EE, Kolasa K, Dobrunz LE, McMahon LL (2008) Coactivation of M(1) muscarinic and alpha1 adrenergic receptors stimulates extracellular signal-regulated protein kinase and induces long-term depression at CA3-CA1 synapses in rat hippocampus. J Neurosci 28:5350–5358.PubMedCrossRefGoogle Scholar
  348. Scheiderer CL, McCutchen E, Thacker EE, Kolasa K, Ward MK, Parsons D, Harrell LE, Dobrunz LE, McMahon LL (2006) Sympathetic sprouting drives hippocampal cholinergic reinnervation that prevents loss of a muscarinic receptor-dependent long-term depression at CA3-CA1 synapses. J Neurosci 26:3745–3756.PubMedCrossRefGoogle Scholar
  349. Schmitz D, Empson RM, Heinemann U (1995) Serotonin and 8-OH-DPAT reduce excitatory transmission in rat hippocampal area CA1 via reduction in presumed presynaptic Ca2+ entry. Brain Res 701:249–254.PubMedCrossRefGoogle Scholar
  350. Schuman EM, Madison DV (1991) A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254:1503–1506.PubMedCrossRefGoogle Scholar
  351. Schuman EM, Madison DV (1994) Nitric oxide and synaptic function. Annu Rev Neurosci 17:153–183.PubMedCrossRefGoogle Scholar
  352. Schweitzer P (2000) Cannabinoids decrease the K(+) M-current in hippocampal CA1 neurons. J Neurosci 20:51–58.PubMedGoogle Scholar
  353. Schweitzer P, Madamba S, Siggins GR (1990) Arachidonic acid metabolites as mediators of somatostatin-induced increase of neuronal M-current. Nature 346:464–467.PubMedCrossRefGoogle Scholar
  354. Schweitzer P, Madamba SG, Siggins GR (2003) The sleep-modulating peptide cortistatin augments the h-current in hippocampal neurons. J Neurosci 23:10884–10891.PubMedGoogle Scholar
  355. Seeger T, Alzheimer C (2001) Muscarinic activation of inwardly rectifying K(+) conductance reduces EPSPs in rat hippocampal CA1 pyramidal cells. J Physiol 535:383–396.PubMedCrossRefGoogle Scholar
  356. Seeger T, Fedorova I, Zheng F, Miyakawa T, Koustova E, Gomeza J, Basile AS, Alzheimer C, Wess J (2004) M2 muscarinic acetylcholine receptor knock-out mice show deficits in behavioral flexibility, working memory, and hippocampal plasticity. J Neurosci 24:10117–10127.PubMedCrossRefGoogle Scholar
  357. Seeman P, Van Tol HH (1994) Dopamine receptor pharmacology. Trends Pharmacol Sci 15:264–270.PubMedCrossRefGoogle Scholar
  358. Segal M (1980) The action of serotonin in the rat hippocampal slice preparation. J Physiol 303:423–439.PubMedGoogle Scholar
  359. Segal M (1981) Histamine modulates reactivity of hippocampal CA3 neurons to afferent stimulation in vitro. Brain Res 213:443–448.PubMedCrossRefGoogle Scholar
  360. Selbach O, Brown RE, Haas HL (1997) Long-term increase of hippocampal excitability by histamine and cyclic AMP. Neuropharmacology 36:1539–1548.PubMedCrossRefGoogle Scholar
  361. Shakesby AC, Anwyl R, Rowan MJ (2002) Overcoming the effects of stress on synaptic plasticity in the intact hippocampus: rapid actions of serotonergic and antidepressant agents. J Neurosci 22:3638–3644.PubMedGoogle Scholar
  362. Sharma G, Vijayaraghavan S (2003) Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38:929–939.PubMedCrossRefGoogle Scholar
  363. Sharma G, Grybko M, Vijayaraghavan S (2008) Action potential-independent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses. J Neurosci 28:2563–2575.PubMedCrossRefGoogle Scholar
  364. Shen JX, Tu B, Yakel JL (2009) Inhibition of alpha7-containing nicotinic ACh receptors by muscarinic M1 ACh receptors in rat hippocampal CA1 interneurones in slices. J Physiol 587:1033–1042.PubMedCrossRefGoogle Scholar
  365. Shen M, Piser TM, Seybold VS, Thayer SA (1996) Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 16:4322–4334.PubMedGoogle Scholar
  366. Shen RY, Andrade R (1998) 5-Hydroxytryptamine2 receptor facilitates GABAergic neurotransmission in rat hippocampus. J Pharmacol Exp Ther 285:805–812.PubMedGoogle Scholar
  367. Shigemoto R, Kulik A, Roberts JD, Ohishi H, Nusser Z, Kaneko T, Somogyi P (1996) Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381:523–525.PubMedCrossRefGoogle Scholar
  368. Shinoe T, Matsui M, Taketo MM, Manabe T (2005) Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25:11194–11200.PubMedCrossRefGoogle Scholar
  369. Shinohara S, Kawasaki K (1997) Electrophysiological changes in rat hippocampal pyramidal neurons produced by cholecystokinin octapeptide. Neuroscience 78:1005–1016.PubMedCrossRefGoogle Scholar
  370. Smith WB, Starck SR, Roberts RW, Schuman EM (2005) Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 45:765–779.PubMedCrossRefGoogle Scholar
  371. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698–702.PubMedCrossRefGoogle Scholar
  372. Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015–1023.PubMedCrossRefGoogle Scholar
  373. Sperk G, Hamilton T, Colmers WF (2007) Neuropeptide Y in the dentate gyrus. Prog Brain Res 163:285–297.PubMedCrossRefGoogle Scholar
  374. Springfield SA, Geller HM (1988) Histamine modulates local inhibition in the rat hippocampal slice. Cell Mol Neurobiol 8:431–445.PubMedCrossRefGoogle Scholar
  375. Stanzione P, Calabresi P, Mercuri N, Bernardi G (1984) Dopamine modulates CA1 hippocampal neurons by elevating the threshold for spike generation: an in vitro study. Neuroscience 13:1105–1116.PubMedCrossRefGoogle Scholar
  376. Staubli U, Xu FB (1995) Effects of 5-HT3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat. J Neurosci 15:2445–2452.PubMedGoogle Scholar
  377. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773–778.PubMedCrossRefGoogle Scholar
  378. Stocca G, Nistri A (1996) The neuropeptide thyrotropin-releasing hormone modulates GABAergic synaptic transmission on pyramidal neurones of the rat hippocampal slice. Peptides 17:1197–1202.PubMedCrossRefGoogle Scholar
  379. Sudweeks SN, Hooft JA, Yakel JL (2002) Serotonin 5-HT(3) receptors in rat CA1 hippocampal interneurons: functional and molecular characterization. J Physiol 544:715–726.PubMedCrossRefGoogle Scholar
  380. Surmeier DJ (2007) Dopamine and working memory mechanisms in prefrontal cortex. J Physiol 581:885.PubMedCrossRefGoogle Scholar
  381. Swanson LW, Köhler C, Björklund A (1987) The limbic region, I: the septohippocampal system. In: Handbook of Chemical Neuroanatomy, Integrated Systems of the CNS (Björklund A, Hökfelt T, Swanson LW, eds.), pp 125–277. Amsterdam: Elsevier.Google Scholar
  382. Swant J, Stramiello M, Wagner JJ (2008) Postsynaptic dopamine D3 receptor modulation of evoked IPSCs via GABA(A) receptor endocytosis in rat hippocampus. Hippocampus 18:492–502.PubMedCrossRefGoogle Scholar
  383. Szabadits E, Cserep C, Ludanyi A, Katona I, Gracia-Llanes J, Freund TF, Nyiri G (2007) Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling. J Neurosci 27:8101–8111.PubMedCrossRefGoogle Scholar
  384. Szabo SI, Zelles T, Vizi ES, Lendvai B (2008) The effect of nicotine on spiking activity and Ca2+ dynamics of dendritic spines in rat CA1 pyramidal neurons. Hippocampus 18:376–385.PubMedCrossRefGoogle Scholar
  385. Takagi H, Morishima Y, Matsuyama T, Hayashi H, Watanabe T, Wada H (1986) Histaminergic axons in the neostriatum and cerebral cortex of the rat: a correlated light and electron microscopic immunocytochemical study using histidine decarboxylase as a marker. Brain Res 364:114–123.PubMedCrossRefGoogle Scholar
  386. Tallent MK, Siggins GR (1997) Somatostatin depresses excitatory but not inhibitory neurotransmission in rat CA1 hippocampus. J Neurophysiol 78:3008–3018.PubMedGoogle Scholar
  387. Tallent MK, Qiu C (2008) Somatostatin: an endogenous antiepileptic. Mol Cell Endocrinol 286:96–103.PubMedCrossRefGoogle Scholar
  388. Tallent MK, Fabre V, Qiu C, Calbet M, Lamp T, Baratta MV, Suzuki C, Levy CL, Siggins GR, Henriksen SJ, Criado JR, Roberts A, de Lecea L (2005) Cortistatin overexpression in transgenic mice produces deficits in synaptic plasticity and learning. Mol Cell Neurosci 30:465–475.PubMedCrossRefGoogle Scholar
  389. Tecott LH, Maricq AV, Julius D (1993) Nervous system distribution of the serotonin 5-HT3 receptor mRNA. Proc Natl Acad Sci U S A 90:1430–1434.PubMedCrossRefGoogle Scholar
  390. Thompson AM, Swant J, Wagner JJ (2005) Cocaine-induced modulation of long-term potentiation in the CA1 region of rat hippocampus. Neuropharmacology 49:185–194.PubMedCrossRefGoogle Scholar
  391. Thompson SM, Haas HL, Gahwiler BH (1992) Comparison of the actions of adenosine at pre- and postsynaptic receptors in the rat hippocampus in vitro. J Physiol 451:347–363.PubMedGoogle Scholar
  392. Toledo-Rodriguez M, Markram H (2007) Single-cell RT-PCR, a technique to decipher the electrical, anatomical, and genetic determinants of neuronal diversity. Methods Mol Biol 403:123–139.PubMedCrossRefGoogle Scholar
  393. Torres GE, Arfken CL, Andrade R (1996) 5-Hydroxytryptamine4 receptors reduce afterhyperpolarization in hippocampus by inhibiting calcium-induced calcium release. Mol Pharmacol 50:1316–1322.PubMedGoogle Scholar
  394. Toselli M, Lang J, Costa T, Lux HD (1989) Direct modulation of voltage-dependent calcium channels by muscarinic activation of a pertussis toxin-sensitive G-protein in hippocampal neurons. Pflugers Arch 415:255–261.PubMedCrossRefGoogle Scholar
  395. Towers SK, Hestrin S (2008) D1-like dopamine receptor activation modulates GABAergic inhibition but not electrical coupling between neocortical fast-spiking interneurons. J Neurosci 28:2633–2641.PubMedCrossRefGoogle Scholar
  396. Tricoire L, Cea-Del Rio CA (2007) Illuminating cholinergic microcircuits in the neocortex. J Neurosci 27:12119–12120.PubMedCrossRefGoogle Scholar
  397. Triller A, Choquet D (2008) New concepts in synaptic biology derived from single-molecule imaging. Neuron 59:359–374.PubMedCrossRefGoogle Scholar
  398. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393–411.PubMedCrossRefGoogle Scholar
  399. Turner TJ, Mokler DJ, Luebke JI (2004) Calcium influx through presynaptic 5-HT3 receptors facilitates GABA release in the hippocampus: in vitro slice and synaptosome studies. Neuroscience 129:703–718.PubMedCrossRefGoogle Scholar
  400. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314:1788–1792.PubMedCrossRefGoogle Scholar
  401. Valentino RJ, Dingledine R (1981) Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci 1:784–792.PubMedGoogle Scholar
  402. van Hooft JA, Spier AD, Yakel JL, Lummis SC, Vijverberg HP (1998) Promiscuous coassembly of serotonin 5-HT3 and nicotinic alpha4 receptor subunits into Ca(2+)-permeable ion channels. Proc Natl Acad Sci U S A 95:11456–11461.PubMedCrossRefGoogle Scholar
  403. Varela JA, Hirsch SJ, Chapman D, Leverich LS, Greene RW (2009) D1/D5 modulation of synaptic NMDA receptor currents. J Neurosci 29:3109–3119.PubMedCrossRefGoogle Scholar
  404. Varma N, Carlson GC, Ledent C, Alger BE (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21:RC188.PubMedGoogle Scholar
  405. Vilaro MT, Cortes R, Mengod G (2005) Serotonin 5-HT4 receptors and their mRNAs in rat and guinea pig brain: distribution and effects of neurotoxic lesions. J Comp Neurol 484:418–439.PubMedCrossRefGoogle Scholar
  406. Vizi ES, Kiss JP (1998) Neurochemistry and pharmacology of the major hippocampal transmitter systems: synaptic and nonsynaptic interactions. Hippocampus 8:566–607.PubMedCrossRefGoogle Scholar
  407. Vizuete ML, Traiffort E, Bouthenet ML, Ruat M, Souil E, Tardivel-Lacombe J, Schwartz JC (1997) Detailed mapping of the histamine H2 receptor and its gene transcripts in guinea-pig brain. Neuroscience 80:321–343.PubMedCrossRefGoogle Scholar
  408. Vogt KE, Regehr WG (2001) Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21:75–83.PubMedGoogle Scholar
  409. von Engelhardt J, Eliava M, Meyer AH, Rozov A, Monyer H (2007) Functional characterization of intrinsic cholinergic interneurons in the cortex. J Neurosci 27:5633–5642.CrossRefGoogle Scholar
  410. Vorobjev VS, Sharonova IN, Walsh IB, Haas HL (1993) Histamine potentiates N-methyl-{\sc d}-aspartate responses in acutely isolated hippocampal neurons. Neuron 11:837–844.PubMedCrossRefGoogle Scholar
  411. Wagner JJ, Terman GW, Chavkin C (1993) Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 363:451–454.PubMedCrossRefGoogle Scholar
  412. Wanaverbecq N, Semyanov A, Pavlov I, Walker MC, Kullmann DM (2007) Cholinergic axons modulate GABAergic signaling among hippocampal interneurons via postsynaptic alpha 7 nicotinic receptors. J Neurosci 27:5683–5693.PubMedCrossRefGoogle Scholar
  413. Wang RY, Arvanov VL (1998) M100907, a highly selective 5-HT2A receptor antagonist and a potential atypical antipsychotic drug, facilitates induction of long-term potentiation in area CA1 of the rat hippocampal slice. Brain Res 779:309–313.PubMedCrossRefGoogle Scholar
  414. Ward RP, Hamblin MW, Lachowicz JE, Hoffman BJ, Sibley DR, Dorsa DM (1995) Localization of serotonin subtype 6 receptor messenger RNA in the rat brain by in situ hybridization histochemistry. Neuroscience 64:1105–1111.PubMedCrossRefGoogle Scholar
  415. Weiss T, Veh RW, Heinemann U (2003) Dopamine depresses cholinergic oscillatory network activity in rat hippocampus. Eur J Neurosci 18:2573–2580.PubMedCrossRefGoogle Scholar
  416. Weisskopf MG, Zalutsky RA, Nicoll RA (1993) The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fiber synapses and modulates long-term potentiation. Nature 365:188.PubMedGoogle Scholar
  417. Whittaker E, Vereker E, Lynch MA (1999) Neuropeptide Y inhibits glutamate release and long-term potentiation in rat dentate gyrus. Brain Res 827:229–233.PubMedCrossRefGoogle Scholar
  418. Widmer H, Ferrigan L, Davies CH, Cobb SR (2006) Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons. Hippocampus 16:617–628.PubMedCrossRefGoogle Scholar
  419. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588–592.PubMedCrossRefGoogle Scholar
  420. Wojtowicz AM, van den Boom L, Chakrabarty A, Maggio N, Haq RU, Behrens CJ, Heinemann U (2009) Monoamines block kainate- and carbachol-induced gamma-oscillations but augment stimulus-induced gamma-oscillations in rat hippocampus in vitro. Hippocampus 19:273–288.PubMedCrossRefGoogle Scholar
  421. Wolf ME, Mangiavacchi S, Sun X (2003) Mechanisms by which dopamine receptors may influence synaptic plasticity. Ann N Y Acad Sci 1003:241–249.PubMedCrossRefGoogle Scholar
  422. Woolf NJ (1991) Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475–524.PubMedCrossRefGoogle Scholar
  423. Wright DE, Seroogy KB, Lundgren KH, Davis BM, Jennes L (1995) Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain. J Comp Neurol 351:357–373.PubMedCrossRefGoogle Scholar
  424. Wu LG, Saggau P (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20:204–212.PubMedCrossRefGoogle Scholar
  425. Xiang Z, Huguenard JR, Prince DA (1998) Cholinergic switching within neocortical inhibitory networks. Science 281:985–988.PubMedCrossRefGoogle Scholar
  426. Yamazaki Y, Kaneko K, Fujii S, Kato H, Ito K (2003) Long-term potentiation and long-term depression induced by local application of ATP to hippocampal CA1 neurons of the guinea pig. Hippocampus 13:81–92.PubMedCrossRefGoogle Scholar
  427. Yang SN (2000) Sustained enhancement of AMPA receptor- and NMDA receptor-mediated currents induced by dopamine D1/D5 receptor activation in the hippocampus: an essential role of postsynaptic Ca2+. Hippocampus 10:57–63.PubMedCrossRefGoogle Scholar
  428. Yanovsky Y, Haas HL (1998) Histamine increases the bursting activity of pyramidal cells in the CA3 region of mouse hippocampus. Neurosci Lett 240:110–112.PubMedCrossRefGoogle Scholar
  429. Yoon KW, Rothman SM (1991) Adenosine inhibits excitatory but not inhibitory synaptic transmission in the hippocampus. J Neurosci 11:1375–1380.PubMedGoogle Scholar
  430. Zago WM, Massey KA, Berg DK (2006) Nicotinic activity stabilizes convergence of nicotinic and GABAergic synapses on filopodia of hippocampal interneurons. Mol Cell Neurosci 31:549–559.PubMedCrossRefGoogle Scholar
  431. Zaninetti M, Raggenbass M (2000) Oxytocin receptor agonists enhance inhibitory synaptic transmission in the rat hippocampus by activating interneurons in stratum pyramidale. Eur J Neurosci 12:3975–3984.PubMedCrossRefGoogle Scholar
  432. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, Watzke N, Wood PG, Bamberg E, Nagel G, Gottschalk A, Deisseroth K (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446:633–639.PubMedCrossRefGoogle Scholar
  433. Zhang J, Berg DK (2007) Reversible inhibition of GABAA receptors by alpha7-containing nicotinic receptors on the vertebrate postsynaptic neurons. J Physiol 579:753–763.PubMedCrossRefGoogle Scholar
  434. Zieglgansberger W, French ED, Siggins GR, Bloom FE (1979) Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons. Science 205:415–417.PubMedCrossRefGoogle Scholar
  435. Zsiros V, Maccaferri G (2008) Noradrenergic modulation of electrical coupling in GABAergic networks of the hippocampus. J Neurosci 28:1804–1815.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Neuroscience and Molecular Pharmacology, Faculty of Biomedical and Life Sciences, University of GlasgowGlasgowUK
  2. 2.COBRE Center for Structural and Functional Neuroscience, Department of Biomedical and Pharmaceutical SciencesUniversity of MontanaMissoulaUSA

Personalised recommendations