GABA transporter GAT1 prevents spillover at proximal and distal GABA synapses onto primate prefrontal cortex neurons

Journal of Neurophysiology

Volumn 101, Issue 2, 2009, Pages 533-547

  Gonzalez Burgos, Guillermo ^a   Rotaru, Diana C ^a   Zaitsev, Aleksey V ^a,c   Povysheva, Nadezhda V ^a   Lewis, David A ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

1 [2 (BENZHYDRYLIDENEAMINOOXY)ETHYL] 1,2,5,6 TETRAHYDRO 3 PYRIDINECARBOXYLIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID CARRIER GAT1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CONTROLLED STUDY; DENDRITIC CELL; EVOKED RESPONSE; EXPERIMENTAL MONKEY; FEMALE; GABAERGIC TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION;

ANIMALS; ELECTRIC STIMULATION; FEMALE; GABA AGONISTS; GABA ANTAGONISTS; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MACACA FASCICULARIS; MACACA MULATTA; MALE; MODELS, NEUROLOGICAL; NEURONS; NIPECOTIC ACIDS; ORGANOPHOSPHORUS COMPOUNDS; OXIMES; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; PYRIDAZINES; SYNAPSES;

EID: 61349115539     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.91161.2008     Document Type: Article

References (85)

1. Andrasfalvy BK, Mody I. Differences between the scaling of miniature IPSCs and EPSCs recorded in the dendrites of CA1 mouse pyramidal neurons. J Physiol 576: 191-196, 2006.
2. Barbour B. An evaluation of synapse independence. J Neurosci 21: 7969-7984, 2001.
3. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8: 45-56, 2007.
4. Bernstein EM, Quick MW. Regulation of gamma-aminobutyric acid (GABA) transporters by extracellular GABA. J Biol Chem 274: 889-895, 1999.
5. Bicho A, Grewer C. Rapid substrate-induced charge movements of the GABA transporter GAT1. Biophys J 89: 211-231, 2005.
6. Borden LA. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int 29: 335-356, 1996.
7. Bragina L, Marchionni I, Omrani A, Cozzi A, Pellegrini-Giampietro DE, Cherubini E, Conti F. GAT-1 regulates both tonic and phasic GABA(A) receptor-mediated inhibition in the cerebral cortex. J Neurochem 105: 1781-1793, 2008.
8. Buhl EH, Cobb SR, Halasy K, Somogyi P. Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7: 1989-2004, 1995.
9. Chang YM, Luebke JI. Electrophysiological diversity of layer 5 pyramidal cells in the prefrontal cortex of the rhesus monkey: in vitro slice studies. J Neurophysiol 98: 2622-2632, 2007.
10. Constantinidis C, Goldman-Rakic PS. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J Neurophysiol 88: 3487-3497, 2002.
11. Conti F, Melone M, De Biasi S, Minelli A, Brecha NC, Ducati A. Neuronal and glial localization of GAT-1, a high-affinity gamma-aminobutyric acid plasma membrane transporter, in human cerebral cortex: with a note on its distribution in monkey cortex. J Comp Neurol 396: 51-63, 1998.
12. Conti F, Minelli A, Melone M. GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications. Brain Res Brain Res Rev 45: 196-212, 2004.
13. Cruz DA, Eggan SM, Lewis DA. Postnatal development of pre- and postsynaptic GABA markers at chandelier cell connections with pyramidal neurons in monkey prefrontal cortex. J Comp Neurol 465: 385-400, 2003.
14. DeFelipe J, Alonso-Nanclares L, Arellano JI. Microstructure of the neocortex: comparative aspects. J Neurocytol 31: 299-316, 2002.
15. Edwards RH. The neurotransmitter cycle and quantal size. Neuron 55: 835-858, 2007.
16. Erickson SL, Lewis DA. Postnatal development of parvalbumin- and GABA transporter-immunoreactive axon terminals in monkey prefrontal cortex. J Comp Neurol 448: 186-202, 2002.
17. Farrant M, Kaila K. The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog Brain Res 160: 59-87, 2007.
18. Farrant M, Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6: 215-229, 2005.
19. Freund TF, Katona I. Perisomatic inhibition. Neuron 56: 33-42, 2007.
20. Gonzalez-Burgos G, Barrionuevo G, Lewis DA. Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. Cereb Cortex 10: 82-92, 2000.
21. Gonzalez-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA. Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93: 942-953, 2005.
22. Gonzalez-Burgos G, Krimer LS, Urban NN, Barrionuevo G, Lewis DA. Synaptic efficacy during repetitive activation of excitatory inputs in primate dorsolateral prefrontal cortex. Cereb Cortex 14: 530-542, 2004.
23. Gonzalez-Burgos G, Kroener S, Zaitsev AV, Povysheva NV, Krimer LS, Barrionuevo G, Lewis DA. Functional maturation of excitatory synapses in layer 3 pyramidal neurons during postnatal development of the primate prefrontal cortex. Cereb Cortex 18: 626-637, 2008.
24. Guastella J, Nelson N, Nelson H, Czyzyk L, Keynan S, Miedel MC, Davidson N, Lester HA, Kanner BI. Cloning and expression of a rat brain GABA transporter. Science 249: 1303-1306, 1990.
25. Gulledge AT, Stuart GJ. Excitatory actions of GABA in the cortex. Neuron 37: 299-309, 2003.
26. Hajos N, Nusser Z, Rancz EA, Freund TF, Mody I. Cell type- and synapse-specific variability in synaptic GABAA receptor occupancy. Eur J Neurosci 12: 810-818, 2000.
27. Hashimoto T, Arion D, Unger T, Maldonado-Aviles JG, Morris HM, Volk DW, Mirnics K, Lewis DA. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 13: 147-161, 2008.
28. Hefft S, Kraushaar U, Geiger JR, Jonas P. Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus. J Physiol 539: 201-208, 2002.
29. Herculano-Houzel S, Collins CE, Wong P, Kaas JH. Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104: 3562-3567, 2007.
30. Herculano-Houzel S, Mota B, Lent R. Cellular scaling rules for rodent brains. Proc Natl Acad Sci USA 103: 12138-12143, 2006.
31. Isaacson JS, Solis JM, Nicoll RA. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10: 165-175, 1993.
32. B receptors in the hippocampus. J Neurophysiol 90: 2690-2701, 2003.
33. Jin H, Wu H, Osterhaus G, Wei J, Davis K, Sha D, Floor E, Hsu CC, Kopke RD, Wu JY. Demonstration of functional coupling between gamma -aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc Natl Acad Sci USA 100: 4293-4298, 2003.
34. Kampa BM, Letzkus JJ, Stuart GJ. Dendritic mechanisms controlling spike-timing-dependent synaptic plasticity. Trends Neurosci 30: 456-463, 2007.
35. A conductances in rat neocortex. J Neurophysiol 94: 2073-2085, 2005.
36. Khirug S, Yamada J, Afzalov R, Voipio J, Khirough R, Kaila K. GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl- contransporter NKCC1. J Neurosci 28: 4635-4639, 2008.
37. Kisvarday ZF, Gulyas A, Beroukas D, North JB, Chubb IW, Somogyi P. Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. Brain 113: 793-812, 1990.
38. Klausberger T, Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321: 53-57, 2008.
39. Koch C, Rapp M, Segev I. A brief history of time (constants). Cereb Cortex 6: 93-101, 1996.
40. Kramer MA, Roopun AK, Carracedo LM, Traub RD, Whittington MA and Kopell NJ. Rhythm generation through period concatenation in rat somatosensory cortex. PLoS Comput Biol 4: e1000169, 2008.
41. B receptors in hippocampal pyramidal cells. J Neurosci 26: 4289-4297, 2006.
42. A receptor microscopic affinity. Neuropharmacology 35: 1383-1392, 1996.
43. Lei S, McBain CJ. GABA B receptor modulation of excitatory and inhibitory synaptic transmission onto rat CA3 hippocampal interneurons. J Physiol 546: 439-453, 2003.
44. Leung LS, Peloquin P. GABA(B) receptors inhibit backpropagating dendritic spikes in hippocampal CA1 pyramidal cells in vivo. Hippocampus 16: 388-407, 2006.
45. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6: 312-324, 2005.
46. Lopez-Bendito G, Shigemoto R, Kulik A, Paulsen O, Fairen A, Lujan R. Expression and distribution of metabotropic GABA receptor subtypes GABABR1 and GABABR2 during rat neocortical development. Eur J Neurosci 15: 1766 -1778, 2002.
47. + channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19: 687-695, 1997.
48. Mager S, Kleinberger-Doron N, Keshet GI, Davidson N, Kanner BI, Lester HA. Ion binding and permeation at the GABA transporter GAT1. J Neurosci 16: 5405-5414, 1996.
49. McCormick DA. GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 62: 1018-1027, 1989.
50. Megias M, Emri Z, Freund TF, Gulyas AI. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102: 527-540, 2001.
51. Minelli A, Brecha NC, Karschin C, DeBiasi S, Conti F. GAT-1, a highaffinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J Neurosci 15: 7734-7746, 1995.
52. Mitchell JF, Sundberg KA, Reynolds JH. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55: 131-141, 2007.
53. Mozrzymas JW. Dynamism of GABA(A) receptor activation shapes the "personality" of inhibitory synapses. Neuropharmacology 47: 945-960, 2004.
54. 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. J Physiol 578: 233-247, 2007.
55. Olah S, Komlosi G, Szabadics J, Varga C, Toth E, Barzo P, Tamas G. Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex. Front Neural Circuits 1: 4, 2007.
56. Ortinski PI, Turner JR, Barberis A, Motamedi G, Yasuda RP, Wolfe BB, Kellar KJ, Vicini S. Deletion of the GABA(A) receptor alpha1 subunit increases tonic GABA(A) receptor current: a role for GABA uptake transporters. J Neurosci 26: 9323-9331, 2006.
57. Overstreet LS, Jones MV, Westbrook GL. Slow desensitization regulates the availability of synaptic GABA(A) receptors. J Neurosci 20: 7914-7921, 2000.
58. Overstreet LS, Westbrook GL. Synapse density regulates independence at unitary inhibitory synapses. J Neurosci 23: 2618-2626, 2003.
59. Papp E, Leinekugel X, Henze DA, Lee J, Buzsaki G. The apical shaft of CA1 pyramidal cells is under GABAergic interneuronal control. Neuroscience 102: 715-721, 2001.
60. 2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 50: 603-616, 2006.
61. Perrais D, Ropert N. Effect of zolpidem on miniature IPSCs and occupancy of postsynaptic GABAA receptors in central synapses. J Neurosci 19: 578-588, 1999.
62. Pierri JN, Chaudry AS, Woo TU, Lewis DA. Alterations in chandelier neuron axon terminals in the prefrontal cortex of schizophrenic subjects. Am J Psychiatry 156: 1709-1719, 1999.
63. Pouille F, Scanziani M. Routing of spike series by dynamic circuits in the hippocampus. Nature 429: 717-723, 2004.
64. Povysheva NV, Zaitsev AV, Kroener S, Krimer OA, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS. Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. J Neurophysiol 97: 1030-1039, 2007.
65. Price CJ, Scott R, Rusakov DA, Capogna M. GABA(B) receptor modulation of feedforward inhibition through hippocampal neurogliaform cells. J Neurosci 28: 6974-6982, 2008.
66. Quick MW, Hu J, Wang D, Zhang HY. Regulation of a gamma-aminobutyric acid transporter by reciprocal tyrosine and serine phosphorylation. J Biol Chem 279: 15961-15967, 2004.
67. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232: 232-235, 1986.
68. Scanziani M. GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25: 673-681, 2000.
69. Sherwood CC, Stimpson CD, Raghanti MA, Wildman DE, Uddin M, Grossman LI, Goodman M, Redmond JC, Bonar CJ, Erwin JM, Hof PR. Evolution of increased glia-neuron ratios in the human frontal cortex. Proc Natl Acad Sci USA 103: 13606-13611, 2006.
70. Somogyi P, Tamas G, Lujan R, Buhl EH. Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26: 113-135, 1998.
71. Szabadics J, Tamas G, Soltesz I. Different transmitter transients underlie presynaptic cell type specificity of GABAA,slow and GABAA,fast. Proc Natl Acad Sci USA 104: 14831-14836, 2007.
72. Szabadics J, Varga C, Molnar G, Olah S, Barzo P, Tamas G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311: 233-235, 2006.
73. Tamas G, Lorincz A, Simon A, Szabadics J. Identified sources and targets of slow inhibition in the neocortex. Science 299: 1902-1905, 2003.
74. Thompson SM, Gahwiler BH. Effects of the GABA uptake inhibitor tiagabine on inhibitory synaptic potentials in rat hippocampal slice cultures. J Neurophysiol 67: 1698-1701, 1992.
75. Thomson AM, Destexhe A. Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices. Neuroscience 92: 1193-1215, 1999.
76. Traub RD, Whittington MA, Colling SB, Buzsaki G, Jefferys JG. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 493: 471-484, 1996.
77. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH. Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506: 755-773, 1998.
78. Vierling-Claassen D, Siekmeier P, Stufflebeam S, Kopell N. Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. J Neurophysiol 99: 2656-2671, 2008.
79. Vittellaro-Zuccarello L, Calvaresi N, DeBiasi S. Expression of GABA transporters, GAT-1 and GAT-3, in the cerebral cortex and thalamus of the rat during postnatal development. Cell Tissue Res 313: 245-257, 2003.
80. Volk DW, Austin MC, Pierri JN, Sampson AR, Lewis DA. GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: decreased expression in a subset of neurons. Am J Psychiatry 158: 256-265, 2001.
81. Wang XJ, Tegner J, Constantinidis C, Goldman-Rakic PS. Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. Proc Natl Acad Sci USA 101: 1368-1373, 2004.
82. Whittington MA, Traub RD, Jefferys JG. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612-615, 1995.
83. Williams SR, Stuart GJ. Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J Neurosci 23: 7358-7367, 2003.
84. Wu Y, Wang W, Diez-Sampedro A, Richerson GB. Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56: 851-865, 2007.
85. Zaitsev AV, Povysheva NV, Gonzalez-Burgos G, Rotaru D, Fish KN, Krimer LS, Lewis DA. Interneuron diversity in layers 2-3 of monkey prefrontal cortex. Cereb Cortex doi:10.1093/cercor/bhn198.2008.