Stringent Specificity in the Construction of a GABAergic Presynaptic Inhibitory Circuit

Cell

Volumn 139, Issue 1, 2009, Pages 161-174

  Betley, J Nicholas ^a   Wright, Christopher V E ^b   Kawaguchi, Yoshiya ^c   Erdélyi, Ferenc ^d   Szabó, Gábor ^d   Jessell, Thomas M ^a   Kaltschmidt, Julia A ^a,e  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

MOLNEURO; SYSNEURO

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMATE DECARBOXYLASE 65;

ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; INTERNEURON; MAMMAL; MOLECULAR RECOGNITION; MOUSE; NERVE FIBER; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROPRIOCEPTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENSORY NERVE; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SPINAL CORD;

MAMMALIA;

EID: 70349459260     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.08.027     Document Type: Article

References (52)

1. Arber S., Ladle D.R., Lin J.H., Frank E., and Jessell T.M. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101 (2000) 485-498
2. Asada H., Kawamura Y., Maruyama K., Kume H., Ding R.G., Kanbara N., Kuzume H., Sanbo M., Yagi T., and Obata K. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA 94 (1997) 6496-6499
3. Ascoli G.A., Alonso-Nanclares L., Anderson S.A., Barrionuevo G., Benavides-Piccione R., Burkhalter A., Buzsaki G., Cauli B., Defelipe J., Fairen A., et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9 (2008) 557-568
4. Burry R.W. Development of apparent presynaptic elements formed in response to polylysine coated surfaces. Brain Res. 247 (1982) 1-16
5. Cash S., Chiba A., and Keshishian H. Alternate neuromuscular target selection following the loss of single muscle fibers in Drosophila. J. Neurosci. 12 (1992) 2051-2064
6. Chalasani S.H., Chronis N., Tsunozaki M., Gray J.M., Ramot D., Goodman M.B., and Bargmann C.I. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450 (2007) 63-70
7. Chen H.H., Tourtellotte W.G., and Frank E. Muscle spindle-derived neurotrophin 3 regulates synaptic connectivity between muscle sensory and motor neurons. J. Neurosci. 22 (2002) 3512-3519
8. Conradi S. Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat. Acta Physiol. Scand. Suppl. 332 (1969) 5-48
9. Eccles J.C., Eccles R.M., and Magni F. Central inhibitory action attributable to presynaptic depolarization produced by muscle afferent volleys. J. Physiol. 159 (1961) 147-166
10. Esclapez M., Tillakaratne N.J., Kaufman D.L., Tobin A.J., and Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14 (1994) 1834-1855
11. Glasgow S.M., Henke R.M., Macdonald R.J., Wright C.V., and Johnson J.E. Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 132 (2005) 5461-5469
12. Glickfeld L.L., and Scanziani M. Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat. Neurosci. 9 (2006) 807-815
13. Gupta A., Wang Y., and Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287 (2000) 273-278
14. Hartman K.N., Pal S.K., Burrone J., and Murthy V.N. Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat. Neurosci. 9 (2006) 642-649
15. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6 (2005) 877-888
16. Holstein G.R., Martinelli G.P., and Cohen B. Ultrastructural features of non-commissural GABAergic neurons in the medial vestibular nucleus of the monkey. Neuroscience 93 (1999) 183-193
17. Hong E.J., McCord A.E., and Greenberg M.E. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60 (2008) 610-624
18. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., and Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98 (1999) 739-755
19. Huang Z.J., and Scheiffele P. GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development. Curr. Opin. Neurobiol. 18 (2008) 77-83
20. Hughes D.I., Mackie M., Nagy G.G., Riddell J.S., Maxwell D.J., Szabo G., Erdelyi F., Veress G., Szucs P., Antal M., et al. P boutons in lamina IX of the rodent spinal cord express high levels of glutamic acid decarboxylase-65 and originate from cells in deep medial dorsal horn. Proc. Natl. Acad. Sci. USA 102 (2005) 9038-9043
21. Jankowska E., and Puczynska A. Interneuronal activity in reflex pathways from group II muscle afferents is monitored by dorsal spinocerebellar tract neurons in the cat. J. Neurosci. 28 (2008) 3615-3622
22. Jin H., Wu H., Osterhaus G., Wei J., Davis K., Sha D., Floor E., Hsu C.C., Kopke R.D., and Wu J.Y. Demonstration of functional coupling between gamma -aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc. Natl. Acad. Sci. USA 100 (2003) 4293-4298
23. Jin Y., and Garner C.C. Molecular mechanisms of presynaptic differentiation. Annu. Rev. Cell Dev. Biol. 24 (2008) 237-262
24. Jonas P., Bischofberger J., Fricker D., and Miles R. Interneuron Diversity series: Fast in, fast out-temporal and spatial signal processing in hippocampal interneurons. Trends Neurosci. 27 (2004) 30-40
25. Kanaani J., el-Husseini Ael D., Aguilera-Moreno A., Diacovo J.M., Bredt D.S., and Baekkeskov S. A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J. Cell Biol. 158 (2002) 1229-1238
26. Kang R., Wan J., Arstikaitis P., Takahashi H., Huang K., Bailey A.O., Thompson J.X., Roth A.F., Drisdel R.C., Mastro R., et al. Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456 (2008) 904-909
27. Kidd M. Electron microscopy of the inner plexiform layer of the retina in the cat and the pigeon. J. Anat. 96 (1962) 179-187
28. Kubota Y., and Kawaguchi Y. Dependence of GABAergic synaptic areas on the interneuron type and target size. J. Neurosci. 20 (2000) 375-386
29. Li W.C., Cooke T., Sautois B., Soffe S.R., Borisyuk R., and Roberts A. Axon and dendrite geography predict the specificity of synaptic connections in a functioning spinal cord network. Neural Dev. 2 (2007) 17
30. Marmigere F., and Ernfors P. Specification and connectivity of neuronal subtypes in the sensory lineage. Nat. Rev. Neurosci. 8 (2007) 114-127
31. Maximov A., and Sudhof T.C. Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron 48 (2005) 547-554
32. Monyer H., and Markram H. Interneuron Diversity series: Molecular and genetic tools to study GABAergic interneuron diversity and function. Trends Neurosci. 27 (2004) 90-97
33. Ohba S., Ikeda T., Ikegaya Y., Nishiyama N., Matsuki N., and Yamada M.K. BDNF locally potentiates GABAergic presynaptic machineries: target-selective circuit inhibition. Cereb. Cortex 15 (2005) 291-298
34. Olsen S.R., and Wilson R.I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452 (2008) 956-960
35. Peng H.B., Cheng P.C., and Luther P.W. Formation of ACh receptor clusters induced by positively charged latex beads. Nature 292 (1981) 831-834
36. Prokop A., Landgraf M., Rushton E., Broadie K., and Bate M. Presynaptic development at the Drosophila neuromuscular junction: assembly and localization of presynaptic active zones. Neuron 17 (1996) 617-626
37. Rico B., Xu B., and Reichardt L.F. TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat. Neurosci. 5 (2002) 225-233
38. Rudomin P. In search of lost presynaptic inhibition. Exp. Brain Res. 196 (2009) 139-151
39. Sanes D.H., and Poo M.M. In vitro analysis of position- and lineage-dependent selectivity in the formation of neuromuscular synapses. Neuron 2 (1989) 1237-1244
40. Shen K. Molecular mechanisms of target specificity during synapse formation. Curr. Opin. Neurobiol. 14 (2004) 83-88
41. Shen K., Fetter R.D., and Bargmann C.I. Synaptic specificity is generated by the guidepost protein SYG-2 and its receptor, SYG-1. Cell 116 (2004) 869-881
42. Shen K., and Bargmann C.I. The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112 (2003) 619-630
43. Smith T.C., and Jahr C.E. Self-inhibition of olfactory bulb neurons. Nat. Neurosci. 5 (2002) 760-766
44. Sotelo C. Cerebellar synaptogenesis: what we can learn from mutant mice. J. Exp. Biol. 153 (1990) 225-249
45. Stepanyants A., Tamas G., and Chklovskii D.B. Class-specific features of neuronal wiring. Neuron 43 (2004) 251-259
46. Stepien A.E., and Arber S. Probing the locomotor conundrum: descending the 'V' interneuron ladder. Neuron 60 (2008) 1-4
47. Stevens C.F., and Williams J.H. Discharge of the readily releasable pool with action potentials at hippocampal synapses. J. Neurophysiol. 98 (2007) 3221-3229
48. Thomson A.M., and Morris O.T. Selectivity in the inter-laminar connections made by neocortical neurones. J. Neurocytol. 31 (2002) 239-246
49. Tian N., Petersen C., Kash S., Baekkeskov S., Copenhagen D., and Nicoll R. The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release. Proc. Natl. Acad. Sci. USA 96 (1999) 12911-12916
50. Vrieseling E., and Arber S. Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 127 (2006) 1439-1452
51. Walberg F. Axoaxonic contacts in the cuneate nucleus, probable basis for presynaptic depolarization. Exp. Neurol. 13 (1965) 218-231
52. Windhorst U. On the role of recurrent inhibitory feedback in motor control. Prog. Neurobiol. 49 (1996) 517-587