Postnatal maturation of somatostatin-expressing inhibitory cells in the somatosensory cortex of GIN mice

Frontiers in Neural Circuits

Volumn , Issue MAY2012, 2012, Pages 1-12

  Kinnischtzke, Amanda K ^a   Sewall, Anna M ^a   Berkepile, Jon M ^a   Fanselow, Erika E ^a  

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

Author keywords

Inhibition; Postnatal development; Somatosensory cortex; Somatostatin

Indexed keywords

GREEN FLUORESCENT PROTEIN; SOMATOSTATIN;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL MATURATION; CONTROLLED STUDY; FREQUENCY MODULATION; MOLECULAR DYNAMICS; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIMARY SOMATOSENSORY CORTEX; QUANTITATIVE ANALYSIS; REPOLARIZATION; WAVEFORM;

EID: 84863617618     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2012.00033     Document Type: Article

References (90)

1. Agmon, A., and Connors, B. W. (1991). Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41, 365-379.
2. Amitai, Y., Gibson, J. R., Beierlein, M., Patrick, S. L., Ho, A. M., Connors, B. W., and Golomb, D. (2002). The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J. Neurosci. 22, 4142-4152.
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., Feldmeyer, D., Fishell, G., Fregnac, Y., Freund, T. F., Gardner, D., Gardner, E. P., Goldberg, J. H., Helmstaedter, M., Hestrin, S., Karube, F., Kisvarday, Z. F., Lambolez, B., Lewis, D. A., Marin, O., Markram, H., Munoz, A., Packer, A., Petersen, C. C., Rockland, K. S., Rossier, J., Rudy, B., Somogyi, P., Staiger, J. F., Tamas, G., Thomson, A. M., Toledo-Rodriguez, M., Wang, Y., West, D. C., and Yuste, R. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568.
4. Beierlein, M., Gibson, J. R., and Connors, B. W. (2000). A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 3, 904-910.
5. Beierlein, M., Gibson, J. R., and Connors, B. W. (2003). Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987-3000.
6. Buckmaster, P. S., and Jongen-Relo, A. L. (1999). Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J. Neurosci. 19, 9519-9529.
7. Chance, F. S., Abbott, L. F., and Reyes, A. D. (2002). Gain modulation from background synaptic input. Neuron 35, 773-782.
8. Chapman, C. A., and Lacaille, J. C. (1999a). Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. J. Neurosci. 19, 8637-8645.
9. Chapman, C. A., and Lacaille, J. C. (1999b). Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. J. Neurophysiol. 81, 1296-1307.
10. Chittajallu, R., and Isaac, J. T. (2010). Emergence of cortical inhibition by coordinated sensory-driven plasticity at distinct synaptic loci. Nat. Neurosci. 13, 1240-1248.
11. Chow, A., Erisir, A., Farb, C., Nadal, M. S., Ozaita, A., Lau, D., Welker, E., andRudy, B. (1999). K(+) channel expression distinguishes subpopulations of parvalbumin-and somatostatin-containing neocorti-cal interneurons. J. Neurosci. 19, 9332-9345.
12. Cossart, R., Dinocourt, C., Hirsch, J. C., Merchan-Perez, A., De Felipe, J., Ben-Ari, Y., Esclapez, M., and Bernard, C. (2001). Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 4, 52-62.
13. Dani, V. S., Chang, Q., Maffei, A., Turrigiano, G. G., Jaenisch, R., and Nelson, S. B. (2005). Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 102, 12560-12565.
14. Daw, M. I., Ashby, M. C., and Isaac, J. T. (2007). Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat. Neurosci. 10, 453-461.
15. de la Rocha, J., Doiron, B., Shea-Brown, E., Josic, K., and Reyes, A. (2007). Correlation between neural spike trains increases with firing rate. Nature 448, 802-806.
16. Destexhe, A., and Pare, D. (1999). Impact of network activity on the integrative properties of neocorti-cal pyramidal neurons in vivo. J. Neurophysiol. 81, 1531-1547.
17. Destexhe, A., Rudolph, M., and Pare, D. (2003). The high-conductance state of neocortical neurons in vivo. Nat. Rev. Neurosci. 4, 739-751.
18. Diaz-Quesada, M., and Maravall, M. (2008). Intrinsic mechanisms for adaptive gain rescaling in barrel cortex. J. Neurosci. 28, 696-710.
19. Ehret, G.(1976). Developmentofabso-lute auditory thresholds in the house mouse (Mus musculus). J. Am. Audiol. Soc. 1, 179-184.
20. Fanselow, E. E., and Connors, B. W. (2010). The roles of somatostatin-expressing (GIN) and fast-spiking inhibitory interneurons in UP-DOWN states of mouse neocortex. J. Neurophysiol. 104, 596-606.
21. Fanselow, E. E., Richardson, K. A., and Connors, B. W. (2008). Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J. Neurophysiol. 100, 2640-2652.
22. Frick, A., Feldmeyer, D., and Sakmann, B. (2007). Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex. J. Physiol. 585, 103-116.
23. Gentet, L. J., Kremer, Y., Taniguchi, H., Huang, Z. J., Staiger, J. F., and Petersen, C. C. (2012). Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607-612.
24. Gibson, J. R., Beierlein, M., and Connors, B. W. (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79.
25. Goldberg, E. M., Jeong, H. Y., Kruglikov, I., Tremblay, R., Lazarenko, R. M., and Rudy, B. (2011). Rapid developmental maturation of neocortical FS cell intrinsic excitability. Cereb. Cortex 21, 666-682.
26. Griguoli, M., Maul, A., Nguyen, C., Giorgetti, A., Carloni, P., and Cherubini, E. (2010). Nicotine blocks the hyperpolarization-activated current Ih and severely impairs the oscillatory behavior of oriens-lacunosum moleculare interneurons. J. Neurosci. 30, 10773-10783.
27. Guan, D., Horton, L. R., Armstrong, W. E., and Foehring, R. C. (2011). Postnatal development of A-type and Kv1-and Kv2-mediated potassium channel currents in neocortical pyramidal neurons. J. Neurophysiol. 105, 2976-2988.
28. Guerra, L., McGarry, L. M., Robles, V., Bielza, C., Larranaga, P., and Yuste, R. (2011). Comparison between supervised and unsupervised classifications of neuronal cell types: a case study. Dev. Neurobiol. 71, 71-82.
29. Gupta, A., Wang, Y., and Markram, H. (2000). Organizingprinciplesfor a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273-278.
30. Halabisky, B., Shen, F., Huguenard, J. R., and Prince, D. A. (2006). Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J. Neurophysiol. 96, 834-845.
31. Hayut, I., Fanselow, E. E., Connors, B. W., and Golomb, D. (2011). LTS and FS inhibitory interneurons, shortterm synaptic plasticity, and cortical circuit dynamics. PLoS Comput. Biol. 7:e1002248. doi: 10.1371/jour-nal.pcbi.1002248
32. Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888.
33. Hu, H., Ma, Y., and Agmon, A. (2011). Submillisecond firing synchrony between different subtypes of cortical interneurons connected chemically but not electrically. J. Neurosci. 31, 3351-3361.
34. Jiao, Y., Zhang, C., Yanagawa, Y., and Sun, Q. Q. (2006). Major effects of sensory experiences on the neocor-tical inhibitory circuits. J. Neurosci. 26, 8691-8701.
35. Jiao, Y., Zhang, Z., Zhang, C., Wang, X., Sakata, K., Lu, B., and Sun, Q. Q. (2011). A key mechanism underlying sensory experience-dependent maturation of neocortical GABAergic circuits in vivo. Proc. Natl. Acad. Sci. U.S.A. 108, 12131-12136.
36. Kapfer, C., Glickfeld, L. L., Atallah, B. V., and Scanziani, M. (2007). Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat. Neurosci. 10, 743-753.
37. Kawaguchi, Y. (1995). Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638-2655.
38. Kawaguchi, Y., and Kondo, S. (2002). Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J. Neurocytol. 31, 277-287.
39. Kawaguchi, Y., and Kubota, Y. (1996). Physiological and morphological identification of somatostatin-or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J. Neurosci. 16, 2701-2715.
40. Klausberger, T., Magill, P. J., Marton, L. F., Roberts, J. D., Cobden, P. M., Buzsaki, G., and Somogyi, P. (2003). Brain-state-and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848.
41. Kobayashi, M., Hamada, T., Kogo, M., Yanagawa, Y., Obata, K., and Kang, Y. (2008). Developmental profile of GABAA-mediated synaptic transmission in pyramidal cells of the somatosensory cortex. Eur. J. Neurosci. 28, 849-861.
42. Larkum, M. E., Senn, W., and Luscher, H. R. (2004). Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 14, 1059-1070.
43. Larkum, M. E., Zhu, J. J., and Sakmann, B. (1999). A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338-341.
44. Larkum, M. E., Zhu, J. J., and Sakmann, B. (2001). Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J. Physiol. 533, 447-466.
45. Lawrence, J. J., Grinspan, Z. M., Statland, J. M., and McBain, C. J. (2006). Muscarinic receptor activation tunes mouse stratum oriens interneurones to amplify spike reliability. J. Physiol. 571, 555-562.
46. Lazarus, M. S., and Huang, Z. J. (2011). Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period of ocular dominance plasticity. J. Neurophysiol. 106, 775-787.
47. Lee, S. H., Land, P. W., and Simons, D. J. (2007). Layer-and cell-type-specific effects of neonatal whisker-trimming in adult rat barrel cortex. J. Neurophysiol. 97, 4380-4385.
48. Lewis, D. A., Hashimoto, T., and Volk, D. W. (2005). Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312-324.
49. Lewis, T. J., and Rinzel, J. (2003). Dynamics of spiking neurons connected by both inhibitory and electrical coupling. J. Comput. Neurosci. 14, 283-309.
50. Lien, C. C., and Jonas, P. (2003). Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J. Neurosci. 23, 2058-2068.
51. Long, M. A., Cruikshank, S. J., Jutras, M. J., and Connors, B. W. (2005). Abrupt maturation of a spike-synchronizing mechanism in neocortex. J. Neurosci. 25, 7309-7316.
52. Lovett-Barron, M., Turi, G. F., Kaifosh, P., Lee, P. H., Bolze, F., Sun, X. H., Nicoud, J. F., Zemelman, B. V., Sternson, S. M., and Losonczy, A. (2012). Regulation of neuronal input transformations by tunable dendritic inhibition. Nat. Neurosci. 15, 423-430.
53. Luthi, A., and McCormick, D. A. (1998). H-current: properties of a neuronal and network pacemaker. Neuron 21, 9-12.
54. Ma, Y., Hu, H., and Agmon, A. (2012). Short-term plasticity of unitary inhibitory-to-inhibitory synapses depends on the presynap-tic interneuron subtype. J. Neurosci. 32, 983-988.
55. Ma, Y., Hu, H., Berrebi, A. S., Mathers, P. H., and Agmon, A. (2006). Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069-5082.
56. Maccaferri, G., and McBain, C. J. (1996). The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J. Physiol. 497(Pt 1), 119-130.
57. Mancilla, J. G., Lewis, T. J., Pinto, D. J., Rinzel, J., and Connors, B. W. (2007). Synchronization of electrically coupled pairs of inhibitory interneurons in neocortex. J. Neurosci. 27, 2058-2073.
58. Maravall, M., Stern, E. A., and Svoboda, K. (2004). Development of intrinsic properties and excitability of layer 2/3 pyramidal neurons during a critical period for sensory maps in rat barrel cortex. J. Neurophysiol. 92, 144-156.
59. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807.
60. McCormick, D. A., and Pape, H. C. (1990). Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol. 431, 291-318.
61. McCormick, D. A., and Prince, D. A. (1987). Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J. Physiol. 393, 743-762.
62. McGarry, L. M., Packer, A. M., Fino, E., Nikolenko, V., Sippy, T., and Yuste, R. (2010). Quantitative classification of somatostatin-positive neocortical interneurons identifies three interneuron subtypes. Front. Neural Circuits 4:12. doi: 10.3389/fncir.2010.00012
63. Mehaffey, W. H., Doiron, B., Maler, L., and Turner, R. W. (2005). Deterministic multiplicative gain control with active dendrites. J. Neurosci. 25, 9968-9977.
64. Mitchell, S. J., and Silver, R. A. (2003). Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433-445.
65. Mosconi, T., Woolsey, T. A., and Jacquin, M. F. (2010). Passive vs. active touch-induced activity in the developing whisker pathway. Eur. J. Neurosci. 32, 1354-1363.
66. Murayama, M., and Larkum, M. E. (2009). Enhanced dendritic activity in awake rats. Proc. Natl. Acad. Sci. U.S.A. 106, 20482-20486.
67. Oliva, A. A. Jr., Jiang, M., Lam, T., Smith, K. L., and Swann, J. W. (2000). Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J. Neurosci. 20, 3354-3368.
68. Oswald, A. M., and Reyes, A. D. (2008). Maturation ofintrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditorycortex. J. Neurophysiol. 99, 2998-3008.
69. Oswald, A. M., and Reyes, A. D. (2011). Development of inhibitory timescales in auditory cortex. Cereb. Cortex 21, 1351-1361.
70. Pape, H. C. (1996). Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu. Rev. Physiol. 58, 299-327.
71. Perez-Garci, E., Gassmann, M., Bettler, B., and Larkum, M. E. (2006). The GABAB1b isoform mediates long-lasting inhibition of dendritic Ca2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 50, 603-616.
72. Petersen, C. C., Hahn, T. T., Mehta, M., Grinvald, A., and Sakmann, B. (2003). Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. U.S.A. 100, 13638-13643.
73. Petreanu, L., Huber, D., Sobczyk, A., and Svoboda, K. (2007). Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663-668.
74. Petreanu, L., Mao, T., Sternson, S. M., and Svoboda, K. (2009). The sub-cellular organization of neocortical excitatory connections. Nature 457, 1142-1145.
75. Porter, J. T., Johnson, C. K., and Agmon, A. (2001). Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J. Neurosci. 21, 2699-2710.
76. Rudolph, M., Pelletier, J. G., Pare, D., and Destexhe, A. (2005). Characterization of synaptic conductances and integrative properties during electrically induced EEG-activated states in neocortical neurons in vivo. J. Neurophysiol. 94, 2805-2821.
77. Rudy, B., and McBain, C. J. (2001). Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci. 24, 517-526.
78. Sanchez-Vives, M. V., and McCormick, D. A. (2000). Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027-1034.
79. Shu, Y., Hasenstaub, A., and McCormick, D. A. (2003). Turning on and off recurrent balanced cortical activity. Nature 423, 288-293.
80. Silberberg, G., and Markram, H. (2007). Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735-746.
81. Silver, R. A. (2010). Neuronal arithmetic. Nat. Rev. Neurosci. 11, 474-489.
82. Steriade, M., Nunez, A., and Amzica, F. (1993). A novel slow (<1Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolar-izing components. J. Neurosci. 13, 3252-3265.
83. Steriade, M., Timofeev, I., and Grenier, F. (2001). Natural waking and sleep states: a view from inside neocor-tical neurons. J. Neurophysiol. 85, 1969-1985.
84. Sugino, K., Hempel, C. M., Miller, M. N., Hattox, A. M., Shapiro, P., Wu, C., Huang, Z. J., and Nelson, S. B. (2006). Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 9, 99-107.
85. Tan, Z., Hu, H., Huang, Z. J., and Agmon, A. (2008). Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc. Natl. Acad. Sci. U.S.A. 105, 2187-2192.
86. Vierling-Claassen, D., Cardin, J. A., Moore, C. I., and Jones, S. R. (2010). Computational modeling of distinct neocortical oscillations driven by cell-type selective optogenetic drive: separable resonant circuits controlled by low-threshold spiking and fast-spiking interneurons. Front. Hum. Neurosci. 4:198. doi: 10.3389/fnhum.2010.00198
87. Welker, W. I. (1964). Analysis of sniffing of the albino rat. Behavior 22, 223-244.
88. Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O'Shea, D. J., Sohal, V. S., Goshen, I., Finkelstein, J., Paz, J. T., Stehfest, K., Fudim, R., Ramakrishnan, C., Huguenard, J. R., Hegemann, P., and Deisseroth, K. (2011). Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171-178.
89. Zhang, L., and McBain, C. J. (1995). Potassium conductances underlying repolarization and after-hyperpolarization in rat CA1 hippocampal interneurones. J. Physiol. 488(Pt 3), 661-672.
90. Zhang, Z., Jiao, Y. Y., and Sun, Q. Q. (2011). Developmental maturation of excitation and inhibition balance in principal neurons across four layers of somatosensory cortex. Neuroscience 174, 10-25.