The origin of neocortical nitric oxide synthase-expressing inhibitory neurons

Frontiers in Neural Circuits

Volumn , Issue JULY 2012, 2012, Pages

  Jaglin, Xavier H ^a   Hjerling Leffler, Jens ^b   Fishell, Gord ^a,c   Batista Brito, Renata ^a,d  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cortex; Fate mapping; GABAergic; Hippocampus; Inhibition; Interneuron; MGE; nNOS

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALRETININ; NEURONAL NITRIC OXIDE SYNTHASE; NEUROPEPTIDE Y; SOMATOSTATIN RECEPTOR; TRANSCRIPTION FACTOR SOX6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; MALE; MEDIAN EMINENCE; MOUSE; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION;

EID: 84865109295     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2012.00044     Document Type: Article

References (95)

1. Anderson, S. A., Eisenstat, D. D., Shi, L., and Rubenstein, J. L. (1997a). Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474-476.
2. Anderson, S. A., Qiu, M., Bulfone, A., Eisenstat, D. D., Meneses, J., Pedersen, R., and Rubenstein, J. L. (1997b). Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19, 27-37.
3. Anderson, S. A., Marin, O., Horn, C., Jennings, K., and Rubenstein, J. L. (2001). Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353-363.
4. Arancio, O., Kiebler, M., Lee, C. J., Lev-Ram, V., Tsien, R. Y., Kandel, E. R., and Hawkins, R. D. (1996). Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87, 1025-1035.
5. Aroniadou-Anderjaska, V., and Keller, A. (1996). Intrinsic inhibitory pathways in mouse barrel cortex. Neuroreport 7, 2363-2368.
6. Azim, E., Jabaudon, D., Fame, R. M., and Macklis, J. D. (2009). SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 12, 1238-1247.
7. Baraban, S. C., Hollopeter, G., Erickson, J. C., Schwartzkroin, P. A., and Palmiter, R. D. (1997). Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J. Neurosci. 17, 8927-8936.
8. Batista-Brito, R., and Fishell, G. (2009). The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 87, 81-118.
9. Batista-Brito, R., Machold, R., Klein, C., and Fishell, G. (2008). Gene expression in cortical interneuron precursors is prescient of their mature function. Cereb. Cortex 18, 2306-2317.
10. Batista-Brito, R., Rossignol, E., Hjerling-Leffler, J., Denaxa, M., Wegner, M., Lefebvre, V., Pachnis, V., and Fishell, G. (2009). The cellintrinsic requirement of Sox6 for cortical interneuron development. Neuron 63, 466-481.
11. Belmonte, M. K., Cook, E. H. Jr., Anderson, G. M., Rubenstein, J. L., Greenough, W. T., Beckel-Mitchener, A., Courchesne, E., Boulanger, L. M., Powell, S. B., Levitt, P. R., Perry, E. K., Jiang, Y. H., DeLorey, T. M., and Tierney, E. (2004). Autism as a disorder of neural information processing: directions for research and targets for therapy. Mol. Psychiatry 9, 646-663.
12. Burette, A., Zabel, U., Weinberg, R. J., Schmidt, H. H., and Valtschanoff, J. G. (2002). Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J. Neurosci. 22, 8961-8970.
13. Butt, S. J., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J. G., and Fishell, G. (2005). The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48, 591-604.
14. Butt, S. J., Sousa, V. H., Fuccillo, M. V., Hjerling-Leffler, J., Miyoshi, G., Kimura, S., and Fishell, G. (2008). The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59, 722-732.
15. Caceda, R., Kinkead, B., and Nemeroff, C. B. (2007). Involvement of neuropeptide systems in schizophrenia: human studies. Int. Rev. Neurobiol. 78, 327-376.
16. Cauli, B., Tong, X. K., Rancillac, A., Serluca, N., Lambolez, B., Rossier, J., and Hamel, E. (2004). Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940-8949.
17. Centonze, D., Bracci, E., Pisani, A., Gubellini, P., Bernardi, G., and Calabresi, P. (2002). Activation of dopamine D1-like receptors excites LTS interneurons of the striatum. Eur. J. Neurosci. 15, 2049-2052.
18. Chowdhury, S. A., Kawashima, T., Konishi, T., and Matsunami, K. (1996). GABAergic characteristics of transcallosal activity of cat motor cortical neurons. Neurosci. Res. 26, 323-333.
19. Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C., and Rubenstein, J. L. (2005). Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 8, 1059-1068.
20. Cossart, R., Bernard, C., and Ben-Ari, Y. (2005). Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci. 28, 108-115.
21. Dachtler, J., Hardingham, N. R., Glazewski, S., Wright, N. F., Blain, E. J., and Fox, K. (2011). Experience-dependent plasticity acts via GluR1 and a novel neuronal nitric oxide synthase-dependent synaptic mechanism in adult cortex. J. Neurosci. 31, 11220-11230.
22. 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.
23. Dawson, V. L., and Dawson, T. M. (1998). Nitric oxide in neurodegeneration. Prog. Brain Res. 118, 215-229.
24. Du, T., Xu, Q., Ocbina, P. J., and Anderson, S. A. (2008). NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 135, 1559-1567.
25. Dumitriu, B., Dy, P., Smits, P., and Lefebvre, V. (2006). Generation of mice harboring a Sox6 conditional null allele. Genesis 44, 219-224.
26. Fishell, G., and Rudy, B. (2011). Mechanisms of inhibition within the telencephalon: "where the wild things are". Annu. Rev. Neurosci. 34, 535-567.
27. Flames, N., Long, J. E., Garratt, A. N., Fischer, T. M., Gassmann, M., Birchmeier, C., Lai, C., Rubenstein, J. L., and Marin, O. (2004). Shortand long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44, 251-261.
28. Flames, N., Pla, R., Gelman, D. M., Rubenstein, J. L., Puelles, L., and Marin, O. (2007). Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27, 9682-9695.
29. Fogarty, M., Grist, M., Gelman, D., Marin, O., Pachnis, V., and Kessaris, N. (2007). Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27, 10935-10946.
30. Franklin, K. B. J., and Paxinos, G. (2001). The Mouse Brain in Stereotaxic coordinates, 3rd Edn. San Diego, CA: Academic Press.
31. Fuentealba, P., Begum, R., Capogna, M., Jinno, S., Marton, L. F., Csicsvari, J., Thomson, A., Somogyi, P., and Klausberger, T. (2008). Ivy cells: a population of nitric-oxideproducing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 57, 917-929.
32. Garthwaite, J. (2008). Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 27, 2783-2802.
33. Garthwaite, J., and Boulton, C. L. (1995). Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 57, 683-706.
34. Gelman, D., Griveau, A., Dehorter, N., Teissier, A., Varela, C., Pla, R., Pierani, A., and Marin, O. (2011). A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area. J. Neurosci. 31, 16570-16580.
35. Gelman, D. M., Martini, F. J., Nobrega-Pereira, S., Pierani, A., Kessaris, N., and Marin, O. (2009). The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J. Neurosci. 29, 9380-9389.
36. Gerashchenko, D., Wisor, J. P., Burns, D., Reh, R. K., Shiromani, P. J., Sakurai, T., de la Iglesia, H. O., and Kilduff, T. S. (2008). Identification of a population of sleep-active cerebral cortex neurons. Proc. Natl. Acad. Sci. U.S.A. 105, 10227-10232.
37. Ghanem, N., Yu, M., Long, J., Hatch, G., Rubenstein, J. L., and Ekker, M. (2007). Distinct cis-regulatory elements from the Dlx1/Dlx2 locus mark different progenitor cell populations in the ganglionic eminences and different subtypes of adult cortical interneurons. J. Neurosci. 27, 5012-5022.
38. Gittis, A. H., Nelson, A. B., Thwin, M. T., Palop, J. J., and Kreitzer, A. C. (2010). Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J. Neurosci. 30, 2223-2234.
39. Gonchar, Y. A., Johnson, P. B., and Weinberg, R. J. (1995). GABA- immunopositive neurons in rat neocortex with contralateral projections to S-I. Brain Res. 697, 27-34.
40. Gonchar, Y., Wang, Q., and Burkhalter, A. (2007). Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front. Neuroanat. 1:3. doi: 10.3389/neuro. 05.003.2007
41. Gonzalez-Burgos, G., and Lewis, D. A. (2008). GABA neurons and the mechanisms of network oscillations: implications for under- standing cortical dysfunction in schizophrenia. Schizophr. Bull. 34, 944-961.
42. Haider, B., and McCormick, D. A. (2009). Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62, 171-189.
43. Hardingham, N., and Fox, K. (2006). The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation. J. Neurosci. 26, 7395-7404.
44. Jinno, S., Jeromin, A., Roder, J., and Kosaka, T. (2002). Immunocytochemical localization of neuronal calcium sensor-1 in the hippocampus and cerebellum of the mouse, with special reference to presynaptic terminals. Neuroscience 113, 449-461.
45. Jinno, S., and Kosaka, T. (2002a). Immunocytochemical characterization of hippocamposeptal projecting GABAergic nonprincipal neurons in the mouse brain: a retrograde labeling study. Brain Res. 945, 219-231.
46. Jinno, S., and Kosaka, T. (2002b). Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J. Comp. Neurol. 449, 1-25.
47. Judas, M., Sestan, N., and Kostovic, I. (1999). Nitrinergic neurons in the developing and adult human telencephalon: transient and permanent patterns of expression in comparison to other mammals. Microsc. Res. Tech. 45, 401-419.
48. Karagiannis, A., Gallopin, T., David, C., Battaglia, D., Geoffroy, H., Rossier, J., Hillman, E. M., Staiger, J. F., and Cauli, B. (2009). Classification of NPY-expressing neocortical interneurons. J. Neurosci. 29, 3642-3659.
49. Kawaguchi, Y., and Kubota, Y. (1996). Physiological and morphological identification of somatostatinor vasoactive intestinal polypeptidecontaining cells among GABAergic cell subtypes in rat frontal cortex. J. Neurosci. 16, 2701-2715.
50. Kawaguchi, Y., Wilson, C. J., Augood, S. J., and Emson, P. C. (1995). Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 18, 527-535.
51. Keimpema, E., Straiker, A., Mackie, K., Harkany, T., and Hjerling-Leffler, J. (2012). Sticking out of the crowd: the molecular identity and development of cholecystokinin-containing basket cells. J. Physiol. 590, 703-714.
52. Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., and Richardson, W. D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9, 173-179.
53. Kimura, F., and Baughman, R. W. (1997). GABAergic transcallosal neurons in developing rat neocortex. Eur. J. Neurosci. 9, 1137-1143.
54. Lavdas, A. A., Grigoriou, M., Pachnis, V., and Parnavelas, J. G. (1999). The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881-7888.
55. Lee, J. E., and Jeon, C. J. (2005). Immunocytochemical localization of nitric oxide synthase-containing neurons in mouse and rabbit visual cortex and co-localization with calcium-binding proteins. Mol. Cells 19, 408-417.
56. Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G., and Rudy, B. (2010). The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J. Neurosci. 30, 16796-16808.
57. Levitt, P., Eagleson, K. L., and Powell, E. M. (2004). Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci. 27, 400-406.
58. Li, D. P., Chen, S. R., and Pan, H. L. (2002). Nitric oxide inhibits spinally projecting paraventricular neurons through potentiation of presynaptic GABA release. J. Neurophysiol. 88, 2664-2674.
59. Liodis, P., Denaxa, M., Grigoriou, M., Akufo-Addo, C., Yanagawa, Y., and Pachnis, V. (2007). Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J. Neurosci. 27, 3078-3089.
60. Marin, O., and Rubenstein, J. L. (2001). A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2, 780-790.
61. 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.
62. McDonald, C. T., and Burkhalter, A. (1993). Organization of longrange inhibitory connections with rat visual cortex. J. Neurosci. 13, 768-781.
63. Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J., Battiste, J., Johnson, J. E., Machold, R. P., and Fishell, G. (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582-1594.
64. Morris, H. M., Hashimoto, T., and Lewis, D. A. (2008). Alterations in somatostatin mRNA expression in the dorsolateral prefrontal cortex of subjects with schizophrenia or schizoaffective disorder. Cereb. Cortex 18, 1575-1587.
65. Nery, S., Fishell, G., and Corbin, J. G. (2002). The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5, 1279-1287.
66. Pasumarthi, R. K., Gerashchenko, D., and Kilduff, T. S. (2010). Further characterization of sleep-active neuronal nitric oxide synthase neurons in the mouse brain. Neuroscience 169, 149-157.
67. Petryniak, M. A., Potter, G. B., Rowitch, D. H., and Rubenstein, J. L. (2007). Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 55, 417-433.
68. Pleasure, S. J., Anderson, S., Hevner, R., Bagri, A., Marin, O., Lowenstein, D. H., and Rubenstein, J. L. (2000). Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28, 727-740.
69. Potter, G. B., Petryniak, M. A., Shevchenko, E., McKinsey, G. L., Ekker, M., and Rubenstein, J. L. (2009). Generation of Cretransgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol. Cell. Neurosci. 40, 167-186.
70. Pouille, F., and Scanziani, M. (2001). Enforcement of temporal fidelity in pyramidal cells by somatic feedforward inhibition. Science 293, 1159-1163.
71. Rudy, B., Fishell, G., Lee, S., and Hjerling-Leffler, J. (2011). Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45-61.
72. Salin, P. A., and Prince, D. A. (1996). Electrophysiological mapping of GABAA receptor-mediated inhibition in adult rat somatosensory cortex. J. Neurophysiol. 75, 1589-1600.
73. Schwarzer, C., Williamson, J. M., Lothman, E. W., Vezzani, A., and Sperk, G. (1995). Somatostatin, neuropeptide Y, neurokinin B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy. Neuroscience 69, 831-845.
74. Shlosberg, D., Buskila, Y., Abu- Ghanem, Y., and Amitai, Y. (2012). Spatiotemporal alterations of corti- cal network activity by selective loss of NOS-expressing interneurons. Front. Neural Circuits 6:3. doi: 10.3389/fncir.2012.00003
75. Sousa, V. H., Miyoshi, G., Hjerling- Leffler, J., Karayannis, T., and Fishell, G. (2009). Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb. Cortex 19(Suppl. 1), i1-i10.
76. Sperk, G., Marksteiner, J., Gruber, B., Bellmann, R., Mahata, M., and Ortler, M. (1992). Functional changes in neuropeptide Y- and somatostatin-containing neurons induced by limbic seizures in the rat. Neuroscience 50, 831-846.
77. Stenman, J., Toresson, H., and Campbell, K. (2003). Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 23, 167-174.
78. Sussel, L., Marin, O., Kimura, S., and Rubenstein, J. L. (1999). Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359-3370.
79. Szabadics, J., and Soltesz, I. (2009). Functional specificity of mossy fiber innervation of GABAergic cells in the hippocampus. J. Neurosci. 29, 4239-4251.
80. Szabadits, E., Cserep, C., Ludanyi, A., Katona, I., Gracia-Llanes, J., Freund, T. F., and Nyiri, G. (2007). Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling. J. Neurosci. 27, 8101-8111.
81. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsiani, D., Fu, Y., Lu, J., Lin, Y., Miyoshi, G., Shima, Y., Fishell, G., Nelson, S. B., and Huang, Z. J. (2011). A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013.
82. Tomioka, R., Okamoto, K., Furuta, T., Fujiyama, F., Iwasato, T., Yanagawa, Y., Obata, K., Kaneko, T., and Tamamaki, N. (2005). Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur. J. Neurosci. 21, 1587-1600.
83. Tricoire, L., Pelkey, K. A., Daw, M. I., Sousa, V. H., Miyoshi, G., Jeffries, B., Cauli, B., Fishell, G., and McBain, C. J. (2010). Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J. Neurosci. 30, 2165-2176.
84. Tricoire, L., Pelkey, K. A., Erkkila, B. E., Jeffries, B. W., Yuan, X., and McBain, C. J. (2011). A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J. Neurosci. 31, 10948-10970.
85. Volk, D. W., Pierri, J. N., Fritschy, J. M., Auh, S., Sampson, A. R., and Lewis, D. A. (2002). Reciprocal alterations in preand postsynaptic inhibitory markers at chandelier cell inputs to pyramidal neurons in schizophrenia. Cereb. Cortex 12, 1063-1070.
86. Vucurovic, K., Gallopin, T., Ferezou, I., Rancillac, A., Chameau, P., van Hooft, J. A., Geoffroy, H., Monyer, H., Rossier, J., and Vitalis, T. (2010). Serotonin 3A receptor subtype as an early and protracted marker of cortical interneuron subpopulations. Cereb. Cortex 20, 2333-2347.
87. Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G., and Alvarez-Buylla, A. (1999). Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2, 461-466.
88. Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G., and Alvarez-Buylla, A. (2001). In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128, 3759-3771.
89. Wonders, C. P., and Anderson, S. A. (2006). The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7, 687-696.
90. Wonders, C. P., Taylor, L., Welagen, J., Mbata, I. C., Xiang, J. Z., and Anderson, S. A. (2008). A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev. Biol. 314, 127-136.
91. Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J. L., and Anderson, S. A. (2004). Origins of cortical interneuron subtypes. J. Neurosci. 24, 2612-2622.
92. Xu, Q., Tam, M., and Anderson, S. A. (2008). Fate mapping Nkx2.1lineage cells in the mouse telencephalon. J. Comp. Neurol. 506, 16-29.
93. Yan, X. X., Jen, L. S., and Garey, L. J. (1996). NADPH-diaphorasepositive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb. Cortex 6, 524-529.
94. Yau, H. J., Wang, H. F., Lai, C., and Liu, F. C. (2003). Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tan- gentially migrating from the ganglionic eminences. Cereb. Cortex 13, 252-264.
95. Yu, D., and Eldred, W. D. (2005). Nitric oxide stimulates gammaaminobutyric acid release and inhibits glycine release in retina. J. Comp. Neurol. 483, 278-291.