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Neural Plasticity
Volume 2011 (2011), Article ID 254724, 9 pages
http://dx.doi.org/10.1155/2011/254724
Review Article

The Many Forms and Functions of Long Term Plasticity at GABAergic Synapses

Department of Neurobiology and Behavior, State University of New York (SUNY), Life Science Building Rm 546, Stony Brook, NY 11794, USA

Received 11 February 2011; Revised 22 March 2011; Accepted 23 May 2011

Academic Editor: Bjorn Kampa

Copyright © 2011 Arianna Maffei. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. Komatsu and M. Iwakiri, “Long-term modification of inhibitory synaptic transmission in developing visual cortex,” NeuroReport, vol. 4, no. 7, pp. 907–910, 1993. View at Google Scholar · View at Scopus
  2. H. A. McLean, O. Caillard, Y. Ben-Ari, and J. L. Gaiarsa, “Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus,” Journal of Physiology, vol. 496, no. 2, pp. 471–477, 1996. View at Google Scholar · View at Scopus
  3. M. Ouardouz and B. R. Sastry, “Mechanisms underlying LTP of inhibitory synaptic transmission in the deep cerebellar nuclei,” Journal of Neurophysiology, vol. 84, no. 3, pp. 1414–1421, 2000. View at Google Scholar · View at Scopus
  4. W. Morishita and B. R. Sastry, “Postsynaptic mechanisms underlying long-term depression of GABAergic transmission in neurons of the deep cerebellar nuclei,” Journal of Neurophysiology, vol. 76, no. 1, pp. 59–68, 1996. View at Google Scholar · View at Scopus
  5. V. C. Kotak and D. H. Sanes, “Long-lasting inhibitory synaptic depression is age- and calcium-dependent,” Journal of Neuroscience, vol. 20, no. 15, pp. 5820–5826, 2000. View at Google Scholar · View at Scopus
  6. S. R. Glaum and P. A. Brooks, “Tetanus-induced sustained potentiation of monosynaptic inhibitory transmission in the rat medulla: evidence for a presynaptic locus,” Journal of Neurophysiology, vol. 76, no. 1, pp. 30–38, 1996. View at Google Scholar · View at Scopus
  7. A. Madhavan, A. Bonci, and J. L. Whistler, “Opioid-induced GABA potentiation after chronic morphine attenuates the rewarding effects of opioids in the ventral tegmental area,” Journal of Neuroscience, vol. 30, no. 42, pp. 14029–14035, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. F. S. Nugent, E. C. Penick, and J. A. Kauer, “Opioids block long-term potentiation of inhibitory synapses,” Nature, vol. 446, no. 7139, pp. 1086–1090, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. O. Caillard, Y. Ben-Ari, and J. L. Gaiarsa, “Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus,” Journal of Physiology, vol. 518, no. 1, pp. 109–119, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Kang, L. Jiang, S. A. Goldman, and M. Nedergaard, “Astrocyte-mediated potentiation of inhibitory synaptic transmission,” Nature Neuroscience, vol. 1, no. 8, pp. 683–692, 1998. View at Google Scholar · View at Scopus
  11. Y. Komatsu, “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, vol. 16, no. 20, pp. 6342–6352, 1996. View at Google Scholar · View at Scopus
  12. Y. Yoshimura, M. Inaba, K. Yamada et al., “Involvement of T-type Ca2+ channels in the potentiation of synaptic and visual responses during the critical period in rat visual cortex,” European Journal of Neuroscience, vol. 28, no. 4, pp. 730–743, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Komatsu and Y. Yoshimura, “Long-term modification at inhibitory synapses in developing visual cortex,” in Inhibitory Synaptic Plasticity, M. Woodin and A. Maffei, Eds., pp. 17–27, Springer, New York, NY, USA, 2011. View at Google Scholar
  14. T. Inagaki, T. Begum, F. Reza et al., “Brain-derived neurotrophic factor-mediated retrograde signaling required for the induction of long-term potentiation at inhibitory synapses of visual cortical pyramidal neurons,” Neuroscience Research, vol. 61, no. 2, pp. 192–200, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Kuczewski, C. Porcher, N. Ferrand et al., “Backpropagating action potentials trigger dendritic release of BDNF during spontaneous network activity,” Journal of Neuroscience, vol. 28, no. 27, pp. 7013–7023, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Komatsu and Y. Yoshimura, “Activity-dependent maintenance of long-term potentiation at visual cortical inhibitory synapses,” Journal of Neuroscience, vol. 20, no. 20, pp. 7539–7546, 2000. View at Google Scholar · View at Scopus
  17. F. S. Nugent, J. L. Niehaus, and J. A. Kauer, “PKG and PKA signaling in LTP at GABAergic synapses,” Neuropsychopharmacology, vol. 34, no. 7, pp. 1829–1842, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Sivakumaran, M. H. Mohajerani, and E. Cherubini, “At immature mossy-fiber-CA3 synapses, correlated Presynaptic and postsynaptic activity persistently enhances GABA release and network excitability via BDNF and cAMP-dependent PKA,” Journal of Neuroscience, vol. 29, no. 8, pp. 2637–2647, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Wood and J. Garthwaite, “Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties,” Neuropharmacology, vol. 33, no. 11, pp. 1235–1244, 1994. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Kurotani, Y. Yoshimura, and Y. Komatsu, “Postsynaptic firing produces long-term depression at inhibitory synapses of rat visual cortex,” Neuroscience Letters, vol. 337, no. 1, pp. 1–4, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Jiang, S. Huang, R. de Pasquale et al., “The maturation of GABAergic transmission in visual cortex requires endocannabinoid-mediated LTD of inhibitory inputs during a critical period,” Neuron, vol. 66, no. 2, pp. 248–259, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. V. Chevaleyre and P. E. Castillo, “Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability,” Neuron, vol. 38, no. 3, pp. 461–472, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. B. D. Heifets and P. E. Castillo, “Endocannabinoid signaling and long-term synaptic plasticity,” Annual Review of Physiology, vol. 71, pp. 283–306, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Pan, C. J. Hillard, and Q. S. Liu, “D2 dopamine receptor activation facilitates endocannabinoid- mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signaling,” Journal of Neuroscience, vol. 28, no. 52, pp. 14018–14030, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Marsicano, C. T. Wotjak, S. C. Azad et al., “The endogenous cannabinoid system controls extinction of aversive memories,” Nature, vol. 418, no. 6897, pp. 530–534, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Adermark, G. Talani, and D. M. Lovinger, “Endocannabinoid-dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity,” European Journal of Neuroscience, vol. 29, no. 1, pp. 32–41, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Q. Chiu, N. Puente, P. Grandes, and P. E. Castillo, “Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex,” Journal of Neuroscience, vol. 30, no. 21, pp. 7236–7248, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Henneberger, S. J. Redman, and R. Grantyn, “Cortical efferent control of subcortical sensory neurons by synaptic disinhibition,” Cerebral Cortex, vol. 17, no. 9, pp. 2039–2049, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. B. D. Heifets, V. Chevaleyre, and P. E. Castillo, “Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 29, pp. 10250–10255, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. S. C. Azad, K. Monory, G. Marsicano et al., “Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling,” Journal of Neuroscience, vol. 24, no. 44, pp. 9953–9961, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. R. I. Wilson and R. A. Nicoll, “Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses,” Nature, vol. 410, no. 6828, pp. 588–592, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Maejima, K. Hashimoto, T. Yoshida, A. Aiba, and M. Kano, “Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors,” Neuron, vol. 31, no. 3, pp. 463–475, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. M. A. Woodin, K. Ganguly, and M. M. Poo, “Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity,” Neuron, vol. 39, no. 5, pp. 807–820, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Maffei, K. Nataraj, S. B. Nelson, and G. G. Turrigiano, “Potentiation of cortical inhibition by visual deprivation,” Nature, vol. 443, no. 7107, pp. 81–84, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. C. D. Holmgren and Y. Zilberter, “Coincident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells,” Journal of Neuroscience, vol. 21, no. 20, pp. 8270–8277, 2001. View at Google Scholar · View at Scopus
  36. Y. X. Li, Y. Zhang, H. A. Lester, E. M. Schuman, and N. Davidson, “Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons,” Journal of Neuroscience, vol. 18, no. 24, pp. 10231–10240, 1998. View at Google Scholar · View at Scopus
  37. P. Gubellini, Y. Ben-Ari, and J. L. Gaïarsa, “Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus,” European Journal of Neuroscience, vol. 14, no. 12, pp. 1937–1946, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. J. L. Gaiarsa, O. Caillard, and Y. Ben-Ari, “Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance,” Trends in Neurosciences, vol. 25, no. 11, pp. 564–570, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Ormond and M. A. Woodin, “Disinhibition mediates a form of hippocampal long-term potentiation in area CA1,” PLoS ONE, vol. 4, no. 9, Article ID e7224, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Fiumelli and M. A. Woodin, “Role of activity-dependent regulation of neuronal chloride homeostasis in development,” Current Opinion in Neurobiology, vol. 17, no. 1, pp. 81–86, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Balena, B. Acton, and M. Woodin, “Activity-dependent inhibitory synaptic plasticity mediated by chloride regulation,” in Inhibitory Synaptic Plasticity, M. Woodin and A. Maffei, Eds., pp. 137–146, Springer, New York, NY, USA, 2011. View at Google Scholar
  42. R. A. Wardle and M. M. Poo, “Brain-derived neurotrophic factor modulation of GABAergic synapses by postsynaptic regulation of chloride transport,” Journal of Neuroscience, vol. 23, no. 25, pp. 8722–8732, 2003. View at Google Scholar · View at Scopus
  43. T. Kurotani, K. Yamada, Y. Yoshimura, M. C. Crair, and Y. Komatsu, “State-dependent bidirectional modification of somatic inhibition in neocortical pyramidal cells,” Neuron, vol. 57, no. 6, pp. 905–916, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Heuschneider and R. D. Schwartz, “cAMP and forskolin decrease γ-aminobutyric acid-gated chloride flux in rat brain synaptoneurosomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 8, pp. 2938–2942, 1989. View at Google Scholar · View at Scopus
  45. N. J. Brandon, P. Delmas, J. T. Kittler et al., “GABAA receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway,” Journal of Biological Chemistry, vol. 275, no. 49, pp. 38856–38862, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Kumar, R. T. Khisti, and A. L. Morrow, “Regulation of native GABAA receptors by PKC and protein phosphatase activity,” Psychopharmacology, vol. 183, no. 2, pp. 241–247, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Bogdanov, G. Michels, C. Armstrong-Gold et al., “Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts,” EMBO Journal, vol. 25, no. 18, pp. 4381–4389, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. A. F. Bartley, Z. J. Huang, K. M. Huber, and J. R. Gibson, “Differential activity-dependent, homeostatic plasticity of two neocortical inhibitory circuits,” Journal of Neurophysiology, vol. 100, no. 4, pp. 1983–1994, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Maffei, S. B. Nelson, and G. G. Turrigiano, “Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation,” Nature Neuroscience, vol. 7, no. 12, pp. 1353–1359, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. Q. Q. Sun, “Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV,” Journal of Neurophysiology, vol. 102, no. 5, pp. 2955–2973, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. A. L. Dorrn, K. Yuan, A. J. Barker, C. E. Schreiner, and R. C. Froemke, “Developmental sensory experience balances cortical excitation and inhibition,” Nature, vol. 465, no. 7300, pp. 932–936, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Represa and Y. Ben-Ari, “Trophic actions of GABA on neuronal development,” Trends in Neurosciences, vol. 28, no. 6, pp. 278–283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. V. C. Kotak, A. E. Takesian, and D. H. Sanes, “Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex,” Cerebral Cortex, vol. 18, no. 9, pp. 2098–2108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. V. Kilman, M. C. W. van Rossum, and G. G. Turrigiano, “Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses,” Journal of Neuroscience, vol. 22, no. 4, pp. 1328–1337, 2002. View at Google Scholar · View at Scopus
  55. Y. Ben-Ari, “Seizures beget seizures: the quest for GABA as a key player,” Critical Reviews in Neurobiology, vol. 18, no. 1-2, pp. 135–144, 2006. View at Google Scholar · View at Scopus
  56. S. Oláh, M. Füle, G. Komlósi et al., “Regulation of cortical microcircuits by unitary GABA-mediated volume transmission,” Nature, vol. 461, no. 7268, pp. 1278–1281, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. V. F. Safiulina, G. Fattorini, F. Conti, and E. Cherubini, “GABAergic signaling at mossy fiber synapses in neonatal rat hippocampus,” Journal of Neuroscience, vol. 26, no. 2, pp. 597–608, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. L. Gabernet, S. P. Jadhav, D. E. Feldman, M. Carandini, and M. Scanziani, “Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition,” Neuron, vol. 48, no. 2, pp. 315–327, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Howard, G. Tamas, and I. Soltesz, “Lighting the chandelier: new vistas for axo-axonic cells,” Trends in Neurosciences, vol. 28, no. 6, pp. 310–316, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. B. A. Richards, O. P. Voss, and C. J. Akerman, “GABAergic circuits control stimulus-instructed receptive field development in the optic tectum,” Nature Neuroscience, vol. 13, no. 9, pp. 1098–1106, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. H. J. Alitto and Y. Dan, “Function of inhibition in visual cortical processing,” Current Opinion in Neurobiology, vol. 20, no. 3, pp. 340–346, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Fritschy, “Epilepsy, E/I balance and GABAA receptor plasticity,” Frontiers in Molecular Neuroscience, vol. 1, no. 5, 2008. View at Publisher · View at Google Scholar
  63. H. Ozeki, I. M. Finn, E. S. Schaffer, K. D. Miller, and D. Ferster, “Inhibitory stabilization of the cortical network underlies visual surround suppression,” Neuron, vol. 62, no. 4, pp. 578–592, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. F. Saraga, T. Balena, T. Wolansky, C. T. Dickson, and M. A. Woodin, “Inhibitory synaptic plasticity regulates pyramidal neuron spiking in the rodent hippocampus,” Neuroscience, vol. 155, no. 1, pp. 64–75, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Maffei and A. Fontanini, “Network homeostasis: a matter of coordination,” Current Opinion in Neurobiology, vol. 19, no. 2, pp. 168–173, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. S. B. Nelson and G. G. Turrigiano, “Strength through diversity,” Neuron, vol. 60, no. 3, pp. 477–482, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Fagiolini, J. M. Fritschy, K. Löw, H. Möhler, U. Rudolph, and T. K. Hensch, “Specific GABAA circuits for visual cortical plasticity,” Science, vol. 303, no. 5664, pp. 1681–1683, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. Yazaki-Sugiyama, S. Kang, H. Câteau, T. Fukai, and T. K. Hensch, “Bidirectional plasticity in fast-spiking GABA circuits by visual experience,” Nature, vol. 462, no. 7270, pp. 218–221, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. D. G. Southwell, R. C. Froemke, A. Alvarez-Buylla, M. P. Stryker, and S. P. Gandhi, “Cortical plasticity induced by inhibitory neuron transplantation,” Science, vol. 327, no. 5969, pp. 1145–1148, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. A. E. Takesian, V. C. Kotak, and D. H. Sanes, “Presynaptic GABAB receptors regulate experience-dependent development of inhibitory short-term plasticity,” Journal of Neuroscience, vol. 30, no. 7, pp. 2716–2727, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. J. de la Rocha, C. Marchetti, M. Schiff, and A. D. Reyes, “Linking the response properties of cells in auditory cortex with network architecture: cotuning versus lateral inhibition,” Journal of Neuroscience, vol. 28, no. 37, pp. 9151–9163, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. J. Sun, G. K. Wu, B. H. Liu et al., “Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development,” Nature, vol. 465, no. 7300, pp. 927–931, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. M. M. Carrasco, Y. T. Mao, T. S. Balmer, and S. L. Pallas, “Inhibitory plasticity underlies visual deprivation-induced loss of receptive field refinement in the adult superior colliculus,” European Journal of Neuroscience, vol. 33, no. 1, pp. 58–68, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. S. J. Cruikshank, H. Urabe, A. V. Nurmikko, and B. W. Connors, “Pathway-Specific Feedforward Circuits between Thalamus and Neocortex Revealed by Selective Optical Stimulation of Axons,” Neuron, vol. 65, no. 2, pp. 230–245, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. S. J. Cruikshank, T. J. Lewis, and B. W. Connors, “Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex,” Nature Neuroscience, vol. 10, no. 4, pp. 462–468, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Fagiolini, T. Pizzorusso, N. Berardi, L. Domenici, and L. Maffei, “Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation,” Vision Research, vol. 34, no. 6, pp. 709–720, 1994. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Maffei, M. E. Lambo, and G. G. Turrigiano, “Critical period for inhibitory plasticity in rodent binocular V1,” Journal of Neuroscience, vol. 30, no. 9, pp. 3304–3309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Thomson and C. Lamy, “Functional maps of neocortical local circuitry,” Frontiers in Neuroscience, vol. 1, no. 1, pp. 19–42, 2007. View at Publisher · View at Google Scholar
  79. J. W. Theile, H. Morikawa, R. A. Gonzales, and R. A. Morrisett, “Ethanol enhances GABAergic transmission onto dopamine neurons in the ventral tegmental area of the rat,” Alcoholism, vol. 32, no. 6, pp. 1040–1048, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Melis, R. Camarini, M. A. Ungless, and A. Bonci, “Long-lasting potentiation of GABAergic synapses in dopamine neurons after a single in vivo ethanol exposure,” Journal of Neuroscience, vol. 22, no. 6, pp. 2074–2082, 2002. View at Google Scholar · View at Scopus
  81. F. S. Nugent and J. A. Kauer, “LTP of GABAergic synapses in the ventral tegmental area and beyond,” Journal of Physiology, vol. 586, no. 6, pp. 1487–1493, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. J. W. Theile, H. Morikawa, R. A. Gonzales, and R. A. Morrisett, “Role of 5-hydroxytryptamine2C receptors in Ca2+-dependent ethanol potentiation of GABA release onto ventral tegmental area dopamine neurons,” Journal of Pharmacology and Experimental Therapeutics, vol. 329, no. 2, pp. 625–633, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Madhavan, A. Bonci, and J. L. Whistler, “Opioid-induced GABA potentiation after chronic morphine attenuates the rewarding effects of opioids in the ventral tegmental area,” Journal of Neuroscience, vol. 30, no. 42, pp. 14029–14035, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. W. C. Abraham and M. F. Bear, “Metaplasticity: the plasticity of synaptic plasticity,” Trends in Neurosciences, vol. 19, no. 4, pp. 126–130, 1996. View at Publisher · View at Google Scholar · View at Scopus
  85. Y. Ben-Ari, J. L. Gaiarsa, R. Tyzio, and R. Khazipov, “GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations,” Physiological Reviews, vol. 87, no. 4, pp. 1215–1284, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. N. Kuczewski, A. Langlois, H. Fiorentino et al., “Spontaneous glutamatergic activity induces a BDNF-dependent potentiation of GABAergic synapses in the newborn rat hippocampus,” Journal of Physiology, vol. 586, no. 21, pp. 5119–5128, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. E. E. Galindo-Leon, F. G. Lin, and R. C. Liu, “Inhibitory plasticity in a lateral band improves cortical detection of natural vocalizations,” Neuron, vol. 62, no. 5, pp. 705–716, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. S. A. Prescott, T. J. Sejnowski, and Y. De Koninck, “Reduction of anion reversal potential subverts the inhibitory control of firing rate in spinal lamina I neurons: towards a biophysical basis for neuropathic pain,” Molecular Pain, vol. 2, article 32, 2006. View at Publisher · View at Google Scholar · View at Scopus
  89. A. N. Clarkson, B. S. Huang, S. E. MacIsaac, I. Mody, and S. T. Carmichael, “Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke,” Nature, vol. 468, no. 7321, pp. 305–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Shulga, J. Thomas-Crusells, T. Sigl et al., “Posttraumatic GABAA-mediated [Ca2+]i increase is essential for the induction of brain-derived neurotrophic factor-dependent survival of mature central neurons,” Journal of Neuroscience, vol. 28, no. 27, pp. 6996–7005, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Maguire and I. Mody, “GABAAR plasticity during pregnancy: relevance to postpartum depression,” Neuron, vol. 59, no. 2, pp. 207–213, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. Y. Kawaguchi and Y. Kubota, “GABAergic cell subtypes and their synaptic connections in rat frontal cortex,” Cerebral Cortex, vol. 7, no. 6, pp. 476–486, 1997. View at Publisher · View at Google Scholar · View at Scopus
  93. G. Tamás, P. Somogyi, and E. H. Buhl, “Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat,” Journal of Neuroscience, vol. 18, no. 11, pp. 4255–4270, 1998. View at Google Scholar · View at Scopus
  94. A. B. Ali and A. M. Thomson, “Synaptic α5 subunit-containing GABAA receptors mediate ipsps elicited by dendrite-preferring cells in rat neocortex,” Cerebral Cortex, vol. 18, no. 6, pp. 1260–1271, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. Z. Nusser, W. Sieghart, D. Benke, J. M. Fritschy, and P. Somogyi, “Differential synaptic localization of two major γ-aminobutyric acid type A receptor α subunits on hippocampal pyramidal cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 21, pp. 11939–11944, 1996. View at Publisher · View at Google Scholar · View at Scopus
  96. T. Klausberger, J. D. B. Roberts, and P. Somogyi, “Cell type- and input-specific differences in the number and subtypes of synaptic GABAA receptors in the hippocampus,” Journal of Neuroscience, vol. 22, no. 7, pp. 2513–2521, 2002. View at Google Scholar · View at Scopus
  97. J. M. Fritschy, O. Weinmann, A. Wenzel, and D. Benke, “Synapse-specific localization of NMDA and GABAA receptor subunits revealed by antigen-retrieval immunohistochemistry,” Journal of Comparative Neurology, vol. 390, no. 2, pp. 194–210, 1998. View at Publisher · View at Google Scholar · View at Scopus