Assortment of GABAergic plasticity in the cortical interneuron melting pot

Neural Plasticity

Volumn 2011, Issue , 2011, Pages

  Méndez, Pablo ^a   Bacci, Alberto ^a  

^a EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; AMPA RECEPTOR; ANADAMIDE; CALCINEURIN; CALCIUM; CALCIUM BINDING PROTEIN; CHOLINERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE; ENDOCANNABINOID; GLUTAMATE DECARBOXYLASE 67; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROPEPTIDE; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID RELEASE; ANATOMICAL VARIATION; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; CELL HETEROGENEITY; CELL POLARITY; DENDRITE; DENTATE GYRUS; EXCITABILITY; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HUMAN; INTERNEURON; MOLECULAR BIOLOGY; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; POSTSYNAPTIC INHIBITION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPIKE WAVE; STRENGTH; SYNAPSE; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION;

EID: 80052687198     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2011/976856     Document Type: Review

References (161)

1. Wang X. J., Neurophysiological and computational principles of cortical rhythms in cognition Physiological Reviews 2010 90 3 1195 1268
2. Buzski G., Draguhn A., Neuronal olscillations in cortical networks Science 2004 304 5679 1926 1929 (Pubitemid 38822177)
3. Klausberger T., Somogyi P., Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations Science 2008 321 5885 53 57 (Pubitemid 351956237)
4. Bragin A., Jando G., Nadasdy Z., Hetke J., Wise K., Buzsaki G., Gamma (40100Hz) oscillation in the hippocampus of the behaving rat Journal of Neuroscience 1995 15 1 47 60
5. Sohal V. S., Zhang F., Yizhar O., Deisseroth K., Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 2009 459 7247 698 702
6. Cardin J. A., Carlen M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L. H., Moore C. I., Driving fast-spiking cells induces gamma rhythm and controls sensory responses Nature 2009 459 7247 663 667
7. Bartos M., Vida I., Jonas P., Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks Nature Reviews. Neuroscience 2007 8 1 45 56 (Pubitemid 46011998)
8. Vida I., Bartos M., Jonas P., Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates Neuron 2006 49 1 107 117 (Pubitemid 43017189)
9. Bartos M., Vida I., Frotscher M., Meyer A., Monyer H., Geiger J. R. P., Jonas P., Heidelberg., Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks Proceedings of the National Academy of Sciences of the United States of America 2002 99 20 13222 13227
10. Freund T. F., Katona I., Perisomatic inhibition Neuron 2007 56 1 33 42 (Pubitemid 47484182)
11. Hjos N., Plhalini J., Mann E. O., Nmeth B., Paulsen O., Freund T. F., Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro Journal of Neuroscience 2004 24 41 9127 9137 (Pubitemid 39372256)
12. Somogyi P., Klausberger T., Defined types of cortical interneurone structure space and spike timing in the hippocampus Journal of Physiology 2005 562 1 9 26 (Pubitemid 40207780)
13. Klausberger T., Magill P. J., Mrton L. F., Roberts J. D. B., Cobden P. M., Buzski G., Somogyi P., Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo Nature 2003 421 6925 844 848 (Pubitemid 36254143)
14. Benes F. M., Berretta S., GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder Neuropsychopharmacology 2001 25 1 1 27 (Pubitemid 32493819)
15. Gogolla N., Leblanc J. J., Quast K. B., Sudhof T., Fagiolini M., Hensch T. K., Common circuit defect of excitatory-inhibitory balance in mouse models of autism Journal of Neurodevelopmental Disorders 2009 1 1 172 181
16. Orekhova E. V., Stroganova T. A., Nygren G., Tsetlin M. M., Posikera I. N., Gillberg C., Elam M., Excess of high frequency electroencephalogram oscillations in boys with autism Biological Psychiatry 2007 62 9 1022 1029 (Pubitemid 47562364)
17. Levitt P., Eagleson K. L., Powell E. M., Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders Trends in Neurosciences 2004 27 7 400 406 (Pubitemid 38829255)
18. Lewis D. A., Hashimoto T., Volk D. W., Cortical inhibitory neurons and schizophrenia Nature Reviews. Neuroscience 2005 6 4 312 324 (Pubitemid 40469985)
19. Morris R. G., Anderson E., Lynch G. S., Baudry M., Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5 Nature 1986 319 6056 774 776 (Pubitemid 16145031)
20. Malenka R. C., The long-term potential of LTP Nature Reviews. Neuroscience 2003 4 11 923 926 (Pubitemid 37351431)
21. McHugh T. J., Blum K. I., Tsien J. Z., Tonegawa S., Wilson M. A., Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice Cell 1996 87 7 1339 1349 (Pubitemid 27010116)
22. Gaiarsa J. L., Caillard O., Ari Y. B., Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance Trends in Neurosciences 2002 25 11 564 570 (Pubitemid 35254180)
23. Freund T. F., Buzsaki G., Interneurons of the hippocampus Hippocampus 1996 6 4 347 470 (Pubitemid 126682925)
24. Bartos M., Vida I., Frotscher M., Geiger J. R., Jonas P., Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network Journal of Neurophysiology 2001 21 8 2687 2698 (Pubitemid 32298211)
25. Bartos M., Alle H., Vida I., Role of microcircuit structure and input integration in hippocampal interneuron recruitment and plasticity Neuropharmacology 2010 60 5 730 737
26. Kullmann D. M., Lamsa K. P., LTP and LTD in cortical GABAergic interneurons: emerging rules and roles Neuropharmacology 2011 60 5 712 719
27. Kullmann D. M., Lamsa K. P., Long-term synaptic plasticity in hippocampal interneurons Nature Reviews. Neuroscience 2007 8 9 687 699 (Pubitemid 47283146)
28. Wang Y., Toledo-Rodriguez M., Gupta A., Wu C., Silberberg G., Luo J., Markram H., Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat Journal of Physiology 2004 561 1 65 90 (Pubitemid 39549467)
29. Wang Y., Gupta A., Toledo-Rodriguez M., Wu C. Z., Markram H., Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex Cerebral Cortex 2002 12 4 395 410 (Pubitemid 34226064)
30. Hefft S., Jonas P., Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse Nature Neuroscience 2005 8 1319 1328 (Pubitemid 41630419)
31. Daw M. I., Tricoire L., Erdelyi F., Szabo G., McBain C. J., Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent The Journal of Neuroscience 2009 29 36 11112 11122
32. Maccaferri G., Roberts J. D., Szucs P., Cottingham C. A., Somogyi P., Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro Nature 2000 524 6993 91 116 (Pubitemid 30195308)
33. Reyes A., Lujan R., Rozov A., Burnashev N., Somogyi P., Sakmann B., Target-cell-specific facilitation and depression in neocortical circuits Nature Neuroscience 1998 1 4 279 285 (Pubitemid 128712317)
34. Kawaguchi Y., Kubota Y., Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex Neuroscience 1998 85 3 677 701 (Pubitemid 28223633)
35. Kawaguchi Y, Kubota Y., GABAergic cell subtypes and their synaptic connections in rat frontal cortex Cerebral Cortex 1997 7 6 476 486 (Pubitemid 27353633)
36. Ascoli G. A., Alonso-Nanclares L., Anderson S. A., Barrionuevo G., Benavides-Piccione R., Burkhalter A., Buzski G., Cauli B., DeFelipe J., Fairén A., Feldmeyer D., Fishell G., Fregnac Y., Freund T. F., Gardner D., Gardner E. P., Goldberg J. H., Helmstaedter M., Hestrin S., Karube F., Kisvrday Z. F., Lambolez B., Lewis D. A., Marin O., Markram H., Moz A., Packer A., Petersen C. C. H., Rockland K. S., Rossier J., Rudy B., Somogyi P., Staiger J. F., Tamas G., Thomson A. M., Toledo-Rodriguez M., Wang Y., West D. C., Yuste R., Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex Nature Reviews. Neuroscience 2008 9 7 557 568 (Pubitemid 351873463)
37. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C., Interneurons of the neocortical inhibitory system Nature Reviews. Neuroscience 2004 5 10 793 807 (Pubitemid 39336216)
38. McBain C. J., Fisahn A., Interneurons unbound Nature Reviews. Neuroscience 2001 2 1 11 23 (Pubitemid 33673345)
39. Castillo P. E., Chiu C. Q., Carroll R. C., Long-term plasticity at inhibitory synapses Current Opinion in Neurobiology 2011 21 2 328 338
40. Marinelli S., Pacioni S., Cannich A., Marsicano G., Bacci A., Self-modulation of neocortical pyramidal neurons by endocannabinoids Nature Neuroscience 2009 12 12 1488 1490
41. DeFelipe J., Farinas I., The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs Progress in Neurobiology 1992 39 6 563 607
42. Connors B. W., Gutnick M. J., Intrinsic firing patterns of diverse neocortical neurons Trends in Neurosciences 1990 13 3 99 104 (Pubitemid 20062535)
43. Le Bé J. V., Silberberg G., Wang Y., Markram H., Morphological, electrophysiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex Cerebral Cortex 2007 17 9 2204 2213 (Pubitemid 47283691)
44. McCormick D. A., Connors B. W., Lighthall J. W., Prince D. A., Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex Journal of Neurophysiology 1985 54 4 782 806 (Pubitemid 16253719)
45. Brown S. P., Hestrin S., Intracortical circuits of pyramidal neurons reflect their long-range axonal targets Nature 2009 457 7233 1133 1136
46. Spruston N., Pyramidal neurons: dendritic structure and synaptic integration Nature Reviews. Neuroscience 2008 9 3 206 221 (Pubitemid 351272663)
47. Kubota Y., Shigematsu N., Karube F., Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cerebral Cortex. In press
48. Douglas R., Markram H., Martin K., Shepherd G., Neocortex The Synaptic Organization of the Brain 2004 New York, NY, USA Oxford University Press 499 558
49. Bacci A., Rudolph U., Huguenard J. R., Prince D. A., Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses Journal of Neuroscience 2003 23 29 9664 9674 (Pubitemid 37352066)
50. Beierlein M., Gibson J. R., Connors B. W., Two dynamically distinct inhibitory networks in layer 4 of the neocortex Journal of Neurophysiology 2003 90 5 2987 3000 (Pubitemid 37430000)
51. Karube F., Kubota Y., Kawaguchi Y., Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes Journal of Neuroscience 2004 24 12 2853 2865 (Pubitemid 38405734)
52. Maccaferri G., Stratum oriens horizontal interneurone diversity and hippocampal network dynamics Journal of Physiology 2005 562 1 73 80
53. Pouille F., Scanziani M., Routing of spike series by dynamic circuits in the hippocampus Nature 2004 429 6993 717 723 (Pubitemid 38833116)
54. Szabadics J., Tams G., Soltesz I., Different transmitter transients underlie presynaptic cell type specificity of GABA and GABA, fast Proceedings of the National Academy of Sciences of the United States of America 2007 104 37 14831 14836 (Pubitemid 350003228)
55. Capogna M., Neurogliaform cells and other interneurons of stratum lacunosum moleculare gate entorhinal-hippocampal dialogue Journal of Physiological 2010 15 589 1875 1883
56. Karayannis T., Elfant D., Huerta-Ocampo I., Slow GABA transient and receptor desensitization shape synaptic responses evoked by hippocampal neurogliaform cells Journal of Neuroscience 2010 30 29 9898 9909
57. Olah S., Komlosi G., Szabadics J., Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex Frontiers in Neural Circuits 2007 1, article 4
58. Johnston D., Amaral D., Shepherd G., Hippocampus Synaptic Organization of the Brain 2004 New York, NY, USA Oxford University Press
59. Fuentealba P., Begum R., Capogna M., Jinno S., Mrton L. F., Csicsvari J., Thomson A., Somogyi P., Klausberger T., Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity Neuron 2008 57 6 917 929 (Pubitemid 351400638)
60. Williams S. R., Stuart G. J., Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons Science 2002 295 5561 1907 1910 (Pubitemid 34214130)
61. Somogyi P., A specific axo-axonal interneuron in the visual cortex of the rat Brain Research 1977 136 2 345 350 (Pubitemid 8205709)
62. Szabadics J., Varga C., Molnr G., Olh S., Barz P., Tams G., Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits Science 2006 311 5758 233 235 (Pubitemid 43108189)
63. Khirug S., Yamada J., Afzalov R., Voipio J., Khiroug L., Kaila K., GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1 Journal of Neuroscience 2008 28 18 4635 4639
64. Woodruff A. R., Anderson S. A., Yuste R, The enigmatic function of chandelier cells Frontiers in Neuroscience 2010 4, article 201
65. Glickfeld L. L., Roberts J. D., Somogyi P., Scanziani M., Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis Nature Neuroscience 2009 12 1 21 23
66. Geiger J. R., Lbke J., Roth A., Frotscher M., Jonas P., Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse Neuron 1997 18 6 1009 1023 (Pubitemid 27274618)
67. Gabernet L., Jadhav S. P., Feldman D. E., Carandini M., Scanziani M., Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition Neuron 2005 48 2 315 327 (Pubitemid 41476364)
68. Hartig W., Brauer K., Bruckner G., Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons NeuroReport 1992 3 10 869 872
69. Berardi N., Pizzorusso T., Maffei L., Extracellular matrix and visual cortical plasticity: freeing the synapse Neuron 2004 44 6 905 908 (Pubitemid 39643086)
70. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J. W., Maffei L., Reactivation of ocular dominance plasticity in the adult visual cortex Science 2002 298 5596 1248 1251 (Pubitemid 35285495)
71. Gogolla N., Caroni P., Lthi A., Herry C., Perineuronal nets protect fear memories from erasure Science 2009 325 5945 1258 1261
72. Bucurenciu I., Kulik A., Schwaller B., Frotscher M., Jonas P., Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse Neuron 2008 57 4 536 545 (Pubitemid 351273992)
73. Tottene A., Conti R., Fabbro A., Vecchia D., Shapovalova M., Santello M., van den Maagdenberg A. M. J. M., Ferrari M. D., Pietrobon D., Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice Neuron 2009 61 5 762 773
74. Gibson J. R., Belerlein M., Connors B. W., Two networks of electrically coupled inhibitory neurons in neocortex Nature 1999 402 6757 75 79
75. Galarreta M., Hestrin S., A network of fast-spiking cells in the neocortex connected by electrical synapses Nature 1999 402 6757 72 75
76. Tams G., Buhl E. H., Lrincz A., Somogyi P., Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons Nature Neuroscience 2000 3 4 366 371 (Pubitemid 30185487)
77. Connors B. W., Long M. A., Electrical synapses in the mammalian brain Annual Review of Neuroscience 2004 27 393 418 (Pubitemid 39050408)
78. Hestrin S., Galarreta M., Electrical synapses define networks of neocortical GABAergic neurons Trends in Neurosciences 2005 28 6 304 309 (Pubitemid 40775775)
79. Tams G., Buhl E. H., Somogyi P., Massive autaptic self-innervation of GABAergic neurons in cat visual cortex Journal of Neuroscience 1997 17 16 6352 6364 (Pubitemid 27329908)
80. Connelly W. M., Lees G., Modulation and function of the autaptic connections of layer V fast spiking interneurons in the rat neocortex Journal of Physiological 2010 588 2047 2063
81. Bacci A., Huguenard J. R., Prince D. A., Functional autaptic neurotransmission in fast-spiking interneurons: a novel form of feedback inhibition in the neocortex Journal of Neuroscience 2003 23 3 859 866 (Pubitemid 36206176)
82. Manseau F., Marinelli S., Mendez P., Desynchronization of neocortical networks by asynchronous release of GABA at autaptic and synaptic vontacts from fast-spiking interneurons PLoS Biology 2010 28 8
83. Bacci A., Huguenard J. R., Enhancement of spike-timing precision by autaptic transmission in neocortical inhibitory interneurons Neuron 2006 49 1 119 130 (Pubitemid 43017190)
84. Wilson R. I., Kunos G., Nicoll R. A., Presynaptic specificity of endocannabinoid signaling in the hippocampus Neuron 2001 31 3 453 462 (Pubitemid 32778563)
85. Freund T. F., Katona I., Piomelli D., Role of endogenous cannabinoids in synaptic signaling Physiological Reviews 2003 83 3 1017 1066 (Pubitemid 36828930)
86. Chevaleyre V., Castillo P. E., Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability Neuron 2003 38 3 461 472 (Pubitemid 36579147)
87. Sanacora G., Gueorguieva R., Epperson C. N., Wu YU. T., Appel M., Rothman D. L., Krystal J. H., Mason G. F., Subtype-specific alterations of γ-aminobutyric acid and glutamate in patients with major depression Archives of General Psychiatry 2004 61 7 705 713 (Pubitemid 38890805)
88. Croarkin P. E., Levinson A. J., Daskalakis Z. J., Evidence for GABAergic inhibitory deficits in major depressive disorder Neuroscience and Biobehavioral Reviews 2010 35 3 818 825
89. Sanacora G., Mason G. F., Rothman D. L., Behar K. L., Hyder F., Petroff O. A. C., Berman R. M., Charney D. S., Krystal J. H., Reduced cortical γ-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy Archives of General Psychiatry 1999 56 11 1043 1047 (Pubitemid 29526389)
90. Ben-Ari Y., Holmes G. L., The multiple facets of γ-aminobutyric acid dysfunction in epilepsy Current Opinion in Neurology 2005 18 2 141 145 (Pubitemid 40477489)
91. Chao H. T., Chen H., Samaco R. C., Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes Nature 2010 468 7321 263 269
92. Cunningham M. O., Hunt J., Middleton S., LeBeau F. E. N., Gillies M. G., Davies C. H., Maycox P. R., Whittington M. A., Racca C., Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness Journal of Neuroscience 2006 26 10 2767 2776 (Pubitemid 43357860)
93. Reynolds G. P., Beasley C. L., GABAergic neuronal subtypes in the human frontal cortexdevelopment and deficits in schizophrenia Journal of Chemical Neuroanatomy 2001 22 1-2 95 100 (Pubitemid 32695512)
94. Nakazawa K., Zsiros V., Jiang Z., GABAergic interneuron origin of schizophrenia pathophysiology. Neuropharmacology. In press
95. Uhlhaas P. J., Singer W., Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology Neuron 2006 52 1 155 168 (Pubitemid 44466360)
96. Uhlhaas P. J., Singer W., Abnormal neural oscillations and synchrony in schizophrenia Nature Reviews. Neuroscience 2010 11 2 100 113
97. Varga V., Losonczy A., Zemelman B. V., Borhegyi Z., Nyiri G., Domonkos A., Hangya B., Holderith N., Magee J. C., Freund T. F., Fast synaptic subcortical control of hippocampal circuits Science 2009 326 5951 449 453
98. Freund T. F., Gulyas A. I., Acsady L., Gorcs T., Toth K., Serotonergic control of the hippocampus via local inhibitory interneurons Proceedings of the National Academy of Sciences of the United States of America 1990 87 21 8501 8505
99. Fldy C., Lee S. Y., Szabadics J., Neu A., Soltesz I., Cell type-specific gating of perisomatic inhibition by cholecystokinin Nature Neuroscience 2007 10 9 1128 1130 (Pubitemid 47339951)
100. Puig M. V., Watakabe A., Ushimaru M., Yamamori T., Kawaguchi Y., Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT and 5-HT receptors Journal of Neuroscience 2010 30 6 2211 2222
101. Glickfeld L. L., Atallah B. V., Scanziani M., Complementary modulation of somatic inhibition by opioids and cannabinoids Journal of Neuroscience 2008 28 8 1824 1832 (Pubitemid 351302663)
102. Hu W., Zhang M., Czéh B., Flgge G., Zhang W., Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin- expressing neuronal network Neuropsychopharmacology 2010 35 8 1693 1707
103. Czeh B., Simon M., van der Hart M. G., Schmelting B., Hesselink M. B., Fuchs E., Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: prevention by treatment with a substance P receptor (NK1) antagonist Neuropsychopharmacology 2005 30 1 67 79 (Pubitemid 40024401)
104. Bliss T. V. P., Lomo T., Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path Journal of Physiology 1973 232 2 331 356
105. Ohno-Shosaku T., Maejima T., Kano M., Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals Neuron 2001 29 3 729 738 (Pubitemid 32323945)
106. Kano M., Ohno-Shosaku T., Hashimotodani Y., Uchigashima M., Watanabe M., Endocannabinoid-mediated control of synaptic transmission Physiological Reviews 2009 89 1 309 380
107. Chevaleyre V., Takahashi K. A., Castillo P. E., Endocannabinoid-mediated synaptic plasticity in the CNS Annual Review of Neuroscience 2006 29 37 76 (Pubitemid 44476839)
108. Llano I., Leresche N., Marty A., Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents Neuron 1991 6 4 565 574
109. A responses in hippocampal pyramidal cells Journal of Neuroscience 1992 12 10 4122 4132
110. Wilson R. I., Nicoll R. A., Endogenous cannabinoids mediate retrograde signalling at hippocampal synapsess Nature 2001 410 588 592
111. Heifets B. D., Castillo P. E., Endocannabinoid signaling and long-term synaptic plasticity Annual Review of Physiology 2009 71 283 306
112. Wilson R. I., Nicoll R. A., Endocannabinoid signaling in the brain Science 2002 296 5568 678 682
113. Kreitzer A. C., Regehr W. G., Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells Neuron 2001 29 3 717 727 (Pubitemid 32323944)
114. Piomelli D., The molecular logic of endocannabinoid signalling Nature Reviews. Neuroscience 2003 4 11 873 884 (Pubitemid 37351427)
115. Stella N., Schweitzer P., Plomelli D., A second endogenous cannabinoid that modulates long-term potentiation Nature 1997 388 6644 773 778 (Pubitemid 27375156)
116. Di Marzo V., Fontana A., Cadas H., Schinelli S., Cimino G., Schwartz J. C., Piomelli D., Formation and inactivation of endogenous cannabinoid anandamide in central neurons Nature 1994 372 6507 686 691
117. Heifets B. D., Chevaleyre V., Castillo P. E., Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin Proceedings of the National Academy of Sciences of the United States of America 2008 105 29 10250 10255
118. Chevaleyre V., Heifets B. D., Kaeser P. S., Sdhof T. C., Purpura D. P., Castillo P. E., Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1 Neuron 2007 54 5 801 812 (Pubitemid 46843526)
119. Harkany T., Holmgren C., Hrtig W., Qureshi T., Chaudhry F. A., Storm-Mathisen J., Dobszay M. B., Berghuis P., Schulte G., Sousa K. M., Fremeau R. T., Edwards R. H., Mackie K., Ernfors P., Zilberter Y., Endocannabinoid- independent retrograde signaling at inhibitory synapses in layer 2/3 of neocortex: involvement of vesicular glutamate transporter 3 Journal of Neuroscience 2004 24 21 4978 4988 (Pubitemid 38697831)
120. Zilberter Y., Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex Journal of Physiology 2000 528 3 489 496
121. Holmgren C. D., Zilberter Y., Coincident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells Journal of Neuroscience 2001 21 20 8270 8277 (Pubitemid 32952781)
122. Markram H., Lbke J., Frotscher M., Sakmann B., Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs Science 1997 275 5297 213 215 (Pubitemid 27034762)
123. Magee J. C., Johnston D., A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons Science 1997 275 5297 209 213 (Pubitemid 27034761)
124. Dan Y., Poo M. M., Spike timing-dependent plasticity: from synapse to perception Physiological Reviews 2006 86 3 1033 1048 (Pubitemid 44033388)
125. Lu J. T., Li C. Y., Zhao J. P., Poo M. M., Zhang X. H., Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type Journal of Neuroscience 2007 27 36 9711 9720
126. Woodin M. A., Ganguly K., Poo M. M., Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl-transporter activity Neuron 2003 39 5 807 820 (Pubitemid 37088092)
127. Haas J. S., Nowotny T., Abarbanel H. D. I., Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex Journal of Neurophysiology 2006 96 6 3305 3313 (Pubitemid 44837874)
128. Kurotani T., Yamada K., Yoshimura Y., Crair M. C., Komatsu Y., State-dependent bidirectional modification of somatic inhibition in neocortical pyramidal cells Neuron 2008 57 6 905 916 (Pubitemid 351400635)
129. Lu Y. M., Mansuy I. M., Kandel E. R., Roder J., Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP Neuron 2000 26 1 197 205
130. Komatsu Y., Yoshimura Y., Activity-dependent maintenance of long-term potentiation at visual cortical inhibitory synapses Journal of Neuroscience 2000 20 20 7539 7546
131. Komatsu Y., GABAB receptors, monoamine receptors, and postsynaptic inositol trisphosphate-induced Ca2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses Journal of Neuroscience 1996 16 20 6342 6352 (Pubitemid 26337358)
132. A synaptic transmission Journal of Physiological 2003 553 155 167 (Pubitemid 37483924)
133. Losonczy A., Biro A. A., Nusser Z., Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons Proceedings of the National Academy of Sciences of the United States of America 2004 101 5 1362 1367 (Pubitemid 38182694)
134. Neu A., Foldy C., Soltesz I., 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 Journal of Physiology 2007 578 1 233 247 (Pubitemid 44971121)
135. Loureno J., Cannich A., Carta M., Coussen F., Mulle C., Marsicano G., Synaptic activation of kainate receptors gates presynaptic CB(1) signaling at GABAergic synapses Nature Neuroscience 2010 13 2 197 204
136. Fldy C., Neu A., Jones M. V., Soltesz I., Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release Journal of Neuroscience 2006 26 5 1465 1469 (Pubitemid 43237017)
137. Kang J., Jiang L., Goldman S. A., Nedergaard M., Astrocyte-mediated potentiation of inhibitory synaptic transmission Nature Neuroscience 1998 1 8 683 692 (Pubitemid 128406379)
138. Maffei A., Nataraj K., Nelson S. B., Turrigiano G. G., Potentiation of cortical inhibition by visual deprivation Nature 2006 443 7107 81 84 (Pubitemid 44344051)
139. Patz S., Wirth M. J., Gorba T., Klostermann O., Wahle P., Neuronal activity and neurotrophic factors regulate GAD-65/67 mRNA and protein expression in organotypic cultures of rat visual cortex European Journal of Neuroscience 2003 18 1 1 12 (Pubitemid 36920840)
140. Gierdalski M., Jablonska B., Siucinska E., Lech E., Skibinska A., Kossut M., Rapid regulation of GAD67 mRNA and protein level in cortical neurons after sensory learning Cerebral Cortex 2001 11 9 806 815 (Pubitemid 32800548)
141. Asada H., Kawamura Y., Maruyama K., Kume H., Ding R. G., Kanbara N., Kuzume H., Sanbo M., Yagi T., Obata K., Cleft palate and decreased brain γ-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase Proceedings of the National Academy of Sciences of the United States of America 1997 94 12 6496 6499 (Pubitemid 27270713)
142. Chattopadhyaya B., Di Cristo G., Wu C. Z., Knott G., Kuhlman S., Fu YU., Palmiter R. D., Huang Z. J., GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex Neuron 2007 54 6 889 903 (Pubitemid 46907499)
143. Huang Z. J., Di Cristo G., Ango F., Development of GABA innervation in the cerebral and cerebellar cortices Nature Reviews. Neuroscience 2007 8 9 673 686 (Pubitemid 47283143)
144. Doischer D., Hosp J. A., Yanagawa Y., Obata K., Jonas P., Vida I., Bartos M., Postnatal differentiation of basket cells from slow to fast signaling devices Journal of Neuroscience 2008 28 48 12956 12968
145. Jonas P., Bischofberger J., Fricker D., Miles R., Interneuron diversity series: fast in, fast outtemporal and spatial signal processing in hippocampal interneurons Trends in Neurosciences 2004 27 1 30 40 (Pubitemid 38036976)
146. Glickfeld L. L., Scanziani M., Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells Nature Neuroscience 2006 9 6 807 815
147. Li P., Rudolph U., Huntsman M. M., Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex Proceedings of the National Academy of Sciences of the United States of America 2009 106 29 12156 12161
148. Micheva K. D., Beaulieu C., An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex Proceedings of the National Academy of Sciences of the United States of America 1995 92 25 11834 11838 (Pubitemid 26014204)
149. Jiao Y., Zhang C., Yanagawa Y., Sun Q. Q., Major effects of sensory experiences on the neocortical inhibitory circuits Journal of Neuroscience 2006 26 34 8691 8701 (Pubitemid 44319404)
150. A receptor-mediated unitary IPSPs by cannabinoid receptors at synapses between CCK-positive interneurons in rat hippocampus Journal of Neurophysiology 2007 98 2 861 869 (Pubitemid 47236037)
151. Robbe D., Montgomery S. M., Thome A., Rueda-Orozco P. E., McNaughton B. L., Buzsaki G., Cannabinoids reveal importance of spike timing coordination in hippocampal function Nature Neuroscience 2006 9 12 1526 1533 (Pubitemid 44862661)
152. Hajos N., Katona I., Naiem S. S., Mackie K., Ledent C., Mody I., Freund T. F., Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations European Journal of Neuroscience 2000 12 9 3239 3249
153. Galarreta M., Erdélyi F., Szab G., Hestrin S., Cannabinoid sensitivity and synaptic properties of 2 GABAergic networks in the neocortex Cerebral Cortex 2008 18 10 2296 2305
154. Lemtiri-Chlieh F., Levine E. S., Lack of Depolarization-induced Suppression of Inhibition (DSI) in layer 2/3 interneurons that receive cannabinoid-sensitive inhibitory inputs Journal of Neurophysiology 2007 98 5 2517 2524 (Pubitemid 350127917)
155. Bodor A. L., Katona I., Nyiri G., Mackie K., Ledent C., Hjos N., Freund T. F., Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types Journal of Neuroscience 2005 25 29 6845 6856 (Pubitemid 41023152)
156. Fortin D. A., Levine E. S., Differential effects of endocannabinoids on glutamatergic and GABAergic inputs to layer 5 pyramidal neurons Cerebral Cortex 2007 17 1 163 174 (Pubitemid 44973905)
157. Kapfer C., Glickfeld L. L., Atallah B. V., Scanziani M., Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex Nature Neuroscience 2007 10 6 743 753 (Pubitemid 46828515)
158. Berger T. K., Perin R., Silberberg G., Markram H., Frequency-dependent
159. Silberberg G., Markram H., Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells Neuron 2007 53 5 735 746
160. Murayama M., Pérez-Garci E., Nevian T., Bock T., Senn W., Larkum M. E., Dendritic encoding of sensory stimuli controlled by deep cortical interneurons Nature 2009 457 7233 1137 1141
161. Sjstrm P. J., Husser M., A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons Neuron 2006 51 2 227 238