The GABAB1b Isoform Mediates Long-Lasting Inhibition of Dendritic Ca2+ Spikes in Layer 5 Somatosensory Pyramidal Neurons

Neuron

Volumn 50, Issue 4, 2006, Pages 603-616

  Pérez Garci, Enrique ^a   Gassmann, Martin ^b   Bettler, Bernhard ^b   Larkum, Matthew E ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b Pharmazentrum   (Switzerland)

Author keywords

CELLBIO; MOLNEURO; SYSNEURO

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B1A RECEPTOR; 4 AMINOBUTYRIC ACID B1B RECEPTOR; CALCIUM CHANNEL; CALCIUM ION; GLUTAMIC ACID; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG; CALCIUM; ISOPROTEIN;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITE; INHIBITION KINETICS; INHIBITORY POSTSYNAPTIC POTENTIAL; KNOCKOUT MOUSE; MALE; MOUSE; NEOCORTEX; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY SYSTEM; SPIKE WAVE; SYNAPTIC INHIBITION; ANIMAL; CELL MEMBRANE POTENTIAL; METABOLISM; MOUSE MUTANT; NERVE CELL INHIBITION; PATCH CLAMP; PHYSIOLOGY; RAT; SOMATOSENSORY CORTEX;

ANIMALS; CALCIUM; DENDRITES; GAMMA-AMINOBUTYRIC ACID; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PROTEIN ISOFORMS; PYRAMIDAL CELLS; RATS; RECEPTORS, GABA-B; SOMATOSENSORY CORTEX;

EID: 33646405443     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.04.019     Document Type: Article

References (76)

1. Amitai Y., Friedman A., Connors B.W., and Gutnick M.J. Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cereb. Cortex 3 (1993) 26-38
2. Beaulieu C., and Somogyi P. Targets and quantitative distribution of GABAergic synapses in the visual cortex of the cat. Eur. J. Neurosci. 2 (1990) 296-303
3. Beaulieu C., Kisvarday Z., Somogyi P., Cynader M., and Cowey A. Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb. Cortex 2 (1992) 295-309
4. Benardo L.S. Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro. J. Physiol. 476 (1994) 203-215
5. Benke D., Honer M., Michel C., Bettler B., and Mohler H. gamma-aminobutyric acid type B receptor splice variant proteins GBR1a and GBR1b are both associated with GBR2 in situ and display differential regional and subcellular distribution. J. Biol. Chem. 274 (1999) 27323-27330
6. Bettler B., Kaupmann K., Mosbacher J., and Gassmann M. Molecular structure and physiological functions of GABA(B) receptors. Physiol. Rev. 84 (2004) 835-867
7. Binzegger T., Douglas R.J., and Martin K.A. A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24 (2004) 8441-8453
8. Bischoff S., Leonhard S., Reymann N., Schuler V., Shigemoto R., Kaupmann K., and Bettler B. Spatial distribution of GABA(B)R1 receptor mRNA and binding sites in the rat brain. J. Comp. Neurol. 412 (1999) 1-16
9. Buzsaki G., Penttonen M., Nadasdy Z., and Bragin A. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc. Natl. Acad. Sci. USA 93 (1996) 9921-9925
10. 2+ currents in rat sensory neurones by the G protein G(0): antisense oligonucleotide studies. J. Physiol. 470 (1993) 1-11
11. Cauller L. Layer I of primary sensory neocortex: where top-down converges upon bottom-up. Behav. Brain Res. 71 (1995) 163-170
12. Cauller L.J., Clancy B., and Connors B.W. Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I. J. Comp. Neurol. 390 (1998) 297-310
13. Chen H., and Lambert N.A. Inhibition of dendritic calcium influx by activation of G-protein-coupled receptors in the hippocampus. J. Neurophysiol. 78 (1997) 3484-3488
14. Chu Z., Galarreta M., and Hestrin S. Synaptic interactions of late-spiking neocortical neurons in layer 1. J. Neurosci. 23 (2003) 96-102
15. Cossart R., Dinocourt C., Hirsch J.C., Merchan-Perez A., De Felipe J., Ben Ari Y., Esclapez M., and Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 4 (2001) 52-62
16. Costa E., Auta J., Grayson D.R., Matsumoto K., Pappas G.D., Zhang X., and Guidotti A. GABAA receptors and benzodiazepines: a role for dendritic resident subunit mRNAs. Neuropharmacology 43 (2002) 925-937
17. de Blas A.L., Vitorica J., and Friedrich P. Localization of the GABAA receptor in the rat brain with a monoclonal antibody to the 57,000 Mr peptide of the GABAA receptor/benzodiazepine receptor/Cl- channel complex. J. Neurosci. 8 (1988) 602-614
18. DeFelipe J., and Jones E.G. Cajal on the cerebral cortex: an annotated translation of the complete writings (1988), Oxford University Press, Oxford, UK
19. Derer P., and Derer M. Cajal-Retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36 (1990) 839-856
20. Diamond M.E. Somatosensory thalamus of the rat. In: Jones E.G., and Diamond M.E. (Eds). Cerebral Cortex: The Barrel Cortex of Rodents (1995), Plenum, New York, NY 189-220
21. Felleman D.J., and Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1 (1991) 1-47
22. Fritschy J.M., Weinmann O., Wenzel A., and Benke D. Synapse-specific localization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry. J. Comp. Neurol. 390 (1998) 194-210
23. Fritschy J.M., Meskenaite V., Weinmann O., Honer M., Benke D., and Mohler H. GABAB-receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization. Eur. J. Neurosci. 11 (1999) 761-768
24. Gähwiler B.H., and Brown D.A. GABAb-receptor-activated K+ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures. Proc. Natl. Acad. Sci. USA 82 (1985) 1558-1562
25. Gonchar Y., and Burkhalter A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7 (1997) 347-358
26. Gonchar Y., and Burkhalter A. Differential subcellular localization of forward and feedback interareal inputs to parvalbumin expressing GABAergic neurons in rat visual cortex. J. Comp. Neurol. 406 (1999) 346-360
27. Gonchar Y., and Burkhalter A. Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J. Neurosci. 23 (2003) 10904-10912
28. Gonchar Y., Pang L.Y., Malitschek B., Bettler B., and Burkhalter A. Subcellular localization of GABA(B) receptor subunits in rat visual cortex. J. Comp. Neurol. 431 (2001) 182-197
29. Gulledge A.T., and Stuart G.J. Excitatory actions of GABA in the cortex. Neuron 37 (2003) 299-309
30. Helmchen F. Calibration of fluorescent calcium indicators. In: Yuste R., and Konnerth A. (Eds). Imaging Neurons: A Laboratory Manual (2005), Cold Spring Harbor Laboratory, New York 253-263
31. Helmchen F., Svoboda K., Denk W., and Tank D.W. In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat. Neurosci. 2 (1999) 989-996
32. Hestrin S., and Armstrong W.E. Morphology and physiology of cortical neurons in layer I. J. Neurosci. 16 (1996) 5290-5300
33. Houser C.R., Hendry S.H., Jones E.G., and Vaughn J.E. Morphological diversity of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. J. Neurocytol. 12 (1983) 617-638
34. 2+ channels characterized by recordings from isolated hippocampal dendritic segments. Neuron 18 (1997) 651-663
35. Kim H.G., Beierlein M., and Connors B.W. Inhibitory control of excitable dendrites in neocortex. J. Neurophysiol. 74 (1995) 1810-1814
36. Kim U., Sanchez-Vives M.V., and McCormick D.A. Functional dynamics of GABAergic inhibition in the thalamus. Science 278 (1997) 130-134
37. Lamme V.A.F., Super H., and Spekreijse H. Feedforward, horizontal, and feedback processing in the visual cortex. Curr. Opin. Neurobiol. 8 (1998) 529-535
38. + action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons in vitro and in vivo. J. Neurosci. 22 (2002) 6991-7005
39. Larkum M.E., Kaiser K.M., and Sakmann B. Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc. Natl. Acad. Sci. USA 96 (1999) 14600-14604
40. Larkum M.E., Zhu J.J., and Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398 (1999) 338-341
41. Lavenex P., and Amaral D.G. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10 (2000) 420-430
42. Liang F., Hatanaka Y., Saito H., Yamamori T., and Hashikawa T. Differential expression of gamma-aminobutyric acid type B receptor-1a and -1b mRNA variants in GABA and non-GABAergic neurons of the rat brain. J. Comp. Neurol. 416 (2000) 475-495
43. Llinas R.R., Leznik E., and Urbano F.J. Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc. Natl. Acad. Sci. USA 99 (2002) 449-454
44. López-Bendito G., Shigemoto R., Kulik A., Paulsen O., Fairen A., and Lujan R. Expression and distribution of metabotropic GABA receptor subtypes GABABR1 and GABABR2 during rat neocortical development. Eur. J. Neurosci. 15 (2002) 1766-1778
45. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., and Wu C. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5 (2004) 793-807
46. Migliore M., and Shepherd G.M. Emerging rules for the distributions of active dendritic conductances. Nat. Rev. Neurosci. 3 (2002) 362-370
47. Miles R., Toth K., Gulyas A.I., Hajos N., and Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16 (1996) 815-823
48. 2+ channels in central neurons. Neuron 10 (1993) 889-898
49. Newberry N.R., and Nicoll R.A. Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells. Nature 308 (1984) 450-452
50. Olson I.R., Chun M.M., and Allison T. Contextual guidance of attention: human intracranial event-related potential evidence for feedback modulation in anatomically early, temporally late stages of visual processing. Brain 124 (2001) 1417-1425
51. Poorkhalkali N., Juneblad K., Jonsson A.C., Lindberg M., Karlsson O., Wallbrandt P., Ekstrand J., and Lehmann A. Immunocytochemical distribution of the GABA(B) receptor splice variants GABA(B) R1a and R1b in the rat CNS and dorsal root ganglia. Anat. Embryol. (Berl.) 201 (2000) 1-13
52. Princivalle A.P., Pangalos M.N., Bowery N.G., and Spreafico R. Distribution of GABA(B(1a)), GABA(B(1b)) and GABA(B2) receptor protein in cerebral cortex and thalamus of adult rats. Neuroreport 12 (2001) 591-595
53. Radnikow G., Feldmeyer D., and Lubke J. Axonal projection, input and output synapses, and synaptic physiology of Cajal-Retzius cells in the developing rat neocortex. J. Neurosci. 22 (2002) 6908-6919
54. Rockland K.S., and Pandya D.N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus-monkey. Brain Res. 179 (1979) 3-20
55. Scanziani M. GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25 (2000) 673-681
56. Schaefer A.T., Larkum M.E., Sakmann B., and Roth A. Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J. Neurophysiol. 89 (2003) 3143-3154
57. Schiller J., Schiller Y., Stuart G., and Sakmann B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 505 (1997) 605-616
58. Schiller Y. Activation of a calcium-activated cation current during epileptiform discharges and its possible role in sustaining seizure-like events in neocortical slices. J. Neurophysiol. 92 (2004) 862-872
59. 2+ currents and synaptic transmission in cultured rat hippocampal neurones. J. Physiol. 444 (1991) 669-686
60. Shao Z.W., and Burkhalter A. Role of GABA(B) receptor-mediated inhibition in reciprocal interareal pathways of rat visual cortex. J. Neurophysiol. 81 (1999) 1014-1024
61. Shlosberg D., Patrick S.L., Buskila Y., and Amitai Y. Inhibitory effect of mouse neocortex layer I on the underlying cellular network. Eur. J. Neurosci. 18 (2003) 2751-2759
62. Simon A., Olah S., Molnar G., Szabadics J., and Tamas G. Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J. Neurosci. 25 (2005) 6278-6285
63. Somogyi P., Tamas G., Lujan R., and Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26 (1998) 113-135
64. Staley K.J., and Mody I. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J. Neurophysiol. 68 (1992) 197-212
65. Stuart G., and Spruston N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18 (1998) 3501-3510
66. Stuart G., Spruston N., Sakmann B., and Häusser M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20 (1997) 125-131
67. + (GIRK) currents in dendrites of rat neocortical pyramidal cells. J. Physiol. 517 (1999) 385-390
68. Tamas G., Lorincz A., Simon A., and Szabadics J. Identified sources and targets of slow inhibition in the neocortex. Science 299 (2003) 1902-1905
69. Thomson A.M., and Bannister A.P. Interlaminar connections in the neocortex. Cereb. Cortex 13 (2003) 5-14
70. 2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 76 (1996) 2896-2906
71. B receptor variants. Neuron 50 (2006) 589-601 this issue
72. Wang Y., Toledo-Rodriguez M., Gupta A., Wu C., Silberberg G., Luo J., and Markram H. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J. Physiol. 561 (2004) 65-90
73. Williams S.R. Encoding and decoding of dendritic excitation during active states in pyramidal neurons. J. Neurosci. 25 (2005) 5894-5902
74. Williams S.R., and Stuart G.J. Backpropagation of physiological spike trains in neocortical pyramidal neurons: implications for temporal coding in dendrites. J. Neurosci. 20 (2000) 8238-8246
75. Wong R.K., and Prince D.A. Dendritic mechanisms underlying penicillin-induced epileptiform activity. Science 204 (1979) 1228-1231
76. Zhu Y., Stornetta R.L., and Zhu J.J. Chandelier cells control excessive cortical excitation: characteristics of whisker-evoked synaptic responses of layer 2/3 nonpyramidal and pyramidal neurons. J. Neurosci. 24 (2004) 5101-5108