Untangling GABAergic wiring in the cortical microcircuit

Current Opinion in Neurobiology

Volumn 26, Issue , 2014, Pages 7-14

  Kubota, Yoshiyuki ^a,b,c  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ 2; CALBINDIN; CALRETININ; CHOLECYSTOKININ; CONNEXIN 36; CORTICOTROPIN RELEASING FACTOR; METABOTROPIC RECEPTOR; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; PARVALBUMIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV3.1; POTASSIUM CHANNEL KV3.2; SEROTONIN 3A RECEPTOR; SHAW POTASSIUM CHANNEL; SOMATOSTATIN; SUBSTANCE P RECEPTOR; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; 4 AMINOBUTYRIC ACID;

BASKET CELL; CELL STRUCTURE; CHANDELIER CELL; CONNECTOME; CORTICAL MICROCIRCUIT; DENDRITE; DENDRITIC SHAFT; DENDRITIC SPINE; DOUBLE BOUQUET CELL; ELECTRICAL SYNAPSE; GABAERGIC SYSTEM; GABAERGIC WIRING; GLIA CELL; HUMAN; INHIBITORY GABAERGIC NONPYRAMIDAL CELL; INNERVATION; MARTINOTTI CELL; NERVE CELL INHIBITION; NERVE CONDUCTION; NERVE EXCITABILITY; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SIGNAL TRANSDUCTION; SOMATA; ACTION POTENTIAL; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CORTEX; CLASSIFICATION; CYTOLOGY; METABOLISM; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; GAMMA-AMINOBUTYRIC ACID; HUMANS; NERVE NET; NEURAL INHIBITION; NEURONS;

EID: 84887597933     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.10.003     Document Type: Review

References (85)

1. Rubenstein J.L., Merzenich M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Gene Brain Behav 2003, 2:255-267.
2. Sgado P., Dunleavy M., Genovesi S., Provenzano G., Bozzi Y. The role of GABAergic system in neurodevelopmental disorders: a focus on autism and epilepsy. Int J Physiol Pathophysiol Pharmacol 2011, 3:223-235.
3. Hunt R.F., Girskis K.M., Rubenstein J.L., Alvarez-Buylla A., Baraban S.C. GABA progenitors grafted into the adult epileptic brain control seizures and abnormal behavior. Nat Neurosci 2013, 16:692-697.
4. Curley A.A., Lewis D.A. Cortical basket cell dysfunction in schizophrenia. J Physiol 2012, 590(Pt 4):715-724.
5. Gonzalez-Burgos G., Hashimoto T., Lewis D.A. Alterations of cortical GABA neurons and network oscillations in schizophrenia. Curr Psychiatry Rep 2010, 12:335-344.
6. Lewis D.A., Curley A.A., Glausier J.R., Volk D.W. Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci 2012, 35:57-67.
7. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 1997, 7:476-486.
8. Kubota Y., Karube F., Nomura M., Gulledge A.T., Mochizuki A., Schertel A., Kawaguchi Y. Conserved properties of dendritic trees in four cortical interneuron subtypes. Sci Rep 2011, 1:89.
9. Uematsu M., Hirai Y., Karube F., Ebihara S., Kato M., Abe K., Obata K., Yoshida S., Hirabayashi M., Yanagawa Y., Kawaguchi Y. Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 2008, 18:315-330.
10. Jiang X., Wang G., Lee A.J., Stornetta R.L., Zhu J.J. The organization of two new cortical interneuronal circuits. Nat Neurosci 2013, 16:210-218.
11. Kawaguchi Y., Kubota Y. Neurochemical features and synaptic connections of large physiologically identified GABAergic cells in the rat frontal cortex. Neuroscience 1998, 85:677-701.
12. Kisvarday Z.F., Gulyas A., Beroukas D., North J.B., Chubb I.W., Somogyi P. Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. Brain J Neurol 1990, 113(Pt 3):793-812.
13. Kisvarday Z.F., Martin K.A., Whitteridge D., Somogyi P. Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J Comp Neurol 1985, 241:111-137.
14. Kubota Y., Hatada S., Kondo S., Karube F., Kawaguchi Y. Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J Neurosci Official J Soc Neurosci 2007, 27:1139-1150.
15. Melchitzky D.S., Sesack S.R., Lewis D.A. Parvalbumin-immunoreactive axon terminals in macaque monkey and human prefrontal cortex: laminar, regional, and target specificity of type I and type II synapses. J Comp Neurol 1999, 408:11-22.
16. Williams S.M., Goldman-Rakic P.S., Leranth C. The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J Comp Neurol 1992, 320:353-369.
17. Buhl E.H., Halasy K., Somogyi P. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 1994, 368:823-828.
18. Caputi A., Melzer S., Michael M., Monyer H. The long and short of GABAergic neurons. Curr Opin Neurobiol 2013, 23:179-186.
19. Pfeffer C.K., Xue M., He M., Huang Z.J., Scanziani M. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 2013, 16:1068-1076.
20. Somogyi P., Tamas G., Lujan R., Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 1998, 26:113-135.
21. DeFelipe J., Lopez-Cruz P.L., Benavides-Piccione R., Bielza C., Larranaga P., Anderson S., Burkhalter A., Cauli B., Fairen A., Feldmeyer D., Fishell G., et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 2013, 14:202-216.
22. Karube F., Kubota Y., Kawaguchi Y. Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J Neurosci Official J Soc Neurosci 2004, 24:2853-2865.
23. Kawaguchi Y., Karube F., Kubota Y. Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. Cereb Cortex 2006, 16:696-711.
24. Kawaguchi Y., Kubota Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindind28k-immunoreactive neurons in layer v of rat frontal cortex. J Neurophysiol 1993, 70:387-396.
25. Kubota Y., Hattori R., Yui Y. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 1994, 649:159-173.
26. Kubota Y., Shigematsu N., Karube F., Sekigawa A., Kato S., Yamaguchi N., Hirai Y., Morishima M., Kawaguchi Y. Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb Cortex 2011, 21:1803-1817.
27. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 2004, 5:793-807.
28. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
29. Liu G. Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat Neurosci 2004, 7:373-379.
30. Cossart R., Dinocourt C., Hirsch J.C., Merchan-Perez A., De Felipe J., Ben-Ari Y., Esclapez M., Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 2001, 4:52-62.
31. Chiu C.Q., Lur G., Morse T.M., Carnevale N.T., Ellis-Davies G.C., Higley M.J. Compartmentalization of GABAergic inhibition by dendritic spines. Science 2013, 340:759-762.
32. Chen J.L., Villa K.L., Cha J.W., So P.T., Kubota Y., Nedivi E. Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 2012, 74:361-373.
33. Knott G.W., Quairiaux C., Genoud C., Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 2002, 34:265-273.
34. Gonchar Y., Wang Q., Burkhalter A. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat 2007, 1:3.
35. Xu X., Roby K.D., Callaway E.M. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 2010, 518:389-404.
36. 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. Cereb Cortex 2002, 12:395-410.
37. Kawaguchi Y. Distinct firing patterns of neuronal subtypes in cortical synchronized activities. J Neurosci Official J Soc Neurosci 2001, 21:7261-7272.
38. Chow A., Erisir A., Farb C., Nadal M.S., Ozaita A., Lau D., Welker E., Rudy B. K(+) channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J Neurosci Official J Soc Neurosci 1999, 19:9332-9345.
39. Erisir A., Lau D., Rudy B., Leonard C.S. Function of specific k(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 1999, 82:2476-2489.
40. Massengill J.L., Smith M.A., Son D.I., O'Dowd D.K. Differential expression of k4-ap currents and kv3.1 potassium channel transcripts in cortical neurons that develop distinct firing phenotypes. J Neurosci Official J Soc Neurosci 1997, 17:3136-3147.
41. Bacci A., Huguenard J.R., Prince D.A. Functional autaptic neurotransmission in fast-spiking interneurons: a novel form of feedback inhibition in the neocortex. J Neurosci 2003, 23:859-866.
42. Isomura Y., Harukuni R., Takekawa T., Aizawa H., Fukai T. Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 2009, 12:1586-1593.
43. Massi L., Lagler M., Hartwich K., Borhegyi Z., Somogyi P., Klausberger T. Temporal dynamics of parvalbumin-expressing axo-axonic and basket cells in the rat medial prefrontal cortex in vivo. J Neurosci Official J Soc Neurosci 2012, 32:16496-16502.
44. Lapray D., Lasztoczi B., Lagler M., Viney T.J., Katona L., Valenti O., Hartwich K., Borhegyi Z., Somogyi P., Klausberger T. Behavior-dependent specialization of identified hippocampal interneurons. Nat Neurosci 2012, 15:1265-1271.
45. Puig M.V., Ushimaru M., Kawaguchi Y. Two distinct activity patterns of fast-spiking interneurons during neocortical up states. Proc Natl Acad Sci USA 2008, 105:8428-8433.
46. Ma Y., Hioki H., Konno M., Pan S., Nakamura H., Nakamura K.C., Furuta T., Li J.L., Kaneko T. Expression of gap junction protein connexin36 in multiple subtypes of GABAergic neurons in adult rat somatosensory cortex. Cereb Cortex 2011, 21:2639-2649.
47. Galarreta M., Hestrin S. Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci USA 2002, 99:12438-12443.
48. Gibson J.R., Beierlein M., Connors B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 1999, 402:75-79.
49. Meyer A.H., Katona I., Blatow M., Rozov A., Monyer H. In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci Official J Soc Neurosci 2002, 22:7055-7064.
50. Fukuda T., Kosaka T., Singer W., Galuske R.A. Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network. J Neurosci Official J Soc Neurosci 2006, 26:3434-3443.
51. Eggan S.M., Melchitzky D.S., Sesack S.R., Fish K.N., Lewis D.A. Relationship of cannabinoid cb1 receptor and cholecystokinin immunoreactivity in monkey dorsolateral prefrontal cortex. Neuroscience 2010, 169:1651-1661.
52. Katona I., Sperlagh B., Sik A., Kafalvi A., Vizi E.S., Mackie K., Freund T.F. Presynaptically located cb1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci Official J Soc Neurosci 1999, 19:4544-4558.
53. Glickfeld L.L., Scanziani M. Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat Neurosci 2006, 9:807-815.
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 2007, 578(Pt 1):233-247.
55. Hefft S., Jonas P. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 2005, 8:1319-1328.
56. Larkum M.E. The yin and yang of cortical layer 1. Nat Neurosci 2013, 16:114-115.
57. Kapfer C., Glickfeld L.L., Atallah B.V., Scanziani M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 2007, 10:743-753.
58. Silberberg G., Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by martinotti cells. Neuron 2007, 53:735-746.
59. Murayama M., Perez-Garci E., Nevian T., Bock T., Senn W., Larkum M.E. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 2009, 457:1137-1141.
60. Karagiannis A., Gallopin T., David C., Battaglia D., Geoffroy H., Rossier J., Hillman E.M., Staiger J.F., Cauli B. Classification of NPY-expressing neocortical interneurons. J Neurosci Official J Soc Neurosci 2009, 29:3642-3659.
61. Tomioka R., Rockland K.S. Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter. J Comp Neurol 2007, 505:526-538.
62. Lee S., Hjerling-Leffler J., Zagha E., Fishell G., Rudy B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci Official J Soc Neurosci 2010, 30:16796-16808.
63. Gulyas A.I., Hajos N., Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci Official J Soc Neurosci 1996, 16:3397-3411.
64. Hioki H., Okamoto S., Konno M., Kameda H., Sohn J., Kuramoto E., Fujiyama F., Kaneko T. Cell type-specific inhibitory inputs to dendritic and somatic compartments of parvalbumin-expressing neocortical interneuron. J Neurosci Official J Soc Neurosci 2013, 33:544-555.
65. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci Official J Soc Neurosci 1995, 15:2638-2655.
66. Tamas G., Lorincz A., Simon A., Szabadics J. Identified sources and targets of slow inhibition in the neocortex. Science 2003, 299:1902-1905.
67. Palmer L.M., Schulz J.M., Murphy S.C., Ledergerber D., Murayama M., Larkum M.E. The cellular basis of GABA(b)-mediated interhemispheric inhibition. Science 2012, 335:989-993.
68. Somogyi P. A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res 1977, 136:345-350.
69. Hao J., Wang X.D., Dan Y., Poo M.M., Zhang X.H. An arithmetic rule for spatial summation of excitatory and inhibitory inputs in pyramidal neurons. Proc Natl Acad Sci USA 2009, 106:21906-21911.
70. Baldi R., Varga C., Tamas G. Differential distribution of kcc2 along the axo-somato-dendritic axis of hippocampal principal cells. Eur J Neurosci 2010, 32:1319-1325.
71. Szabadics J., Varga C., Molnar G., Olah S., Barzo P., Tamas G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 2006, 311:233-235.
72. Woodruff A., Xu Q., Anderson S.A., Yuste R. Depolarizing effect of neocortical chandelier neurons. Front Neural Circuits 2009, 3:15.
73. Glickfeld L.L., Roberts J.D., Somogyi P., Scanziani M. Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat Neurosci 2009, 12:21-23.
74. Woodruff A.R., McGarry L.M., Vogels T.P., Inan M., Anderson S.A., Yuste R. State-dependent function of neocortical chandelier cells. J Neurosci Official J Soc Neurosci 2011, 31:17872-17886.
75. Taniguchi H., Lu J., Huang Z.J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 2013, 339:70-74.
76. Lewis D.A., Lund J.S. Heterogeneity of chandelier neurons in monkey neocortex: corticotropin-releasing factor- and parvalbumin-immunoreactive populations. J Comp Neurol 1990, 293:599-615.
77. Fino E., Yuste R. Dense inhibitory connectivity in neocortex. Neuron 2011, 69:1188-1203.
78. Packer A.M., Yuste R. Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition?. J Neurosci Official J Soc Neurosci 2011, 31:13260-13271.
79. Yoshimura Y., Callaway E.M. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat Neurosci 2005, 8:1552-1559.
80. Kerlin A.M., Andermann M.L., Berezovskii V.K., Reid R.C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 2010, 67:858-871.
81. Sohya K., Kameyama K., Yanagawa Y., Obata K., Tsumoto T. GABAergic neurons are less selective to stimulus orientation than excitatory neurons in layer II/III of visual cortex, as revealed by in vivo functional Ca2+ imaging in transgenic mice. J Neurosci Official J Soc Neurosci 2007, 27:2145-2149.
82. Chen T.W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., Looger L.L. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
83. Bock D.D., Lee W.C., Kerlin A.M., Andermann M.L., Hood G., Wetzel A.W., Yurgenson S., Soucy E.R., Kim H.S., Reid R.C. Network anatomy and in vivo physiology of visual cortical neurons. Nature 2011, 471:177-182.
84. Ohki K., Chung S., Ch'ng Y.H., Kara P., Reid R.C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 2005, 433:597-603.
85. Yoshimura Y., Dantzker J.L., Callaway E.M. Excitatory cortical neurons form fine-scale functional networks. Nature 2005, 433:868-873.