Characterization of type I and type II nNOS-expressing interneurons in the barrel cortex of mouse

Frontiers in Neural Circuits

Volumn , Issue JUNE 2012, 2012, Pages

  Perrenoud, Quentin ^a   Geoffroy, Hélène ^a   Gauthier, Benjamin ^a   Rancillac, Armelle ^a   Alfonsi, Fabienne ^b,c   Kessaris, Nicoletta ^b,c   Rossier, Jean ^a   Vitalis, Tania ^a   Gallopin, Thierry ^a  

^a Brain Plasticity Unit   (France)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Development; Immunohistochemistry; Neuropeptide Y; Nitric oxide; Parvalbumin; Patch clamp; Somatostatin; Vasointestinal peptide

Indexed keywords

MESSENGER RNA; NEURONAL NITRIC OXIDE SYNTHASE; PARVALBUMIN; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL POPULATION; CELL TYPE; DENDRITE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MOUSE; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOMATOSENSORY CORTEX;

EID: 84865149322     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (74)

1. Aoki, C., Fenstemaker, S., Lubin, M., and Go, C. G. (1993). Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry. Brain Res. 620, 97-113.
2. Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., Benavides-Piccione, R., Burkhalter, A., Buzsáki, G., Cauli, B., Defelipe, J., Fairén, A., Feldmeyer, D., Fishell, G., Fregnac, Y., Freund, T. F., Gardner, D., Gardner, E. P., Goldberg, J. H., Helmstaedter, M., Hestrin, S., Karube, F., Kisvárday, Z. F., Lambolez, B., Lewis, D. A., Marin, O., Markram, H., Muñoz, 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.
3. Bureau, I., von Saint, P. F., and Svoboda, K. (2006). Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 4, e382. doi:10.1371/journal.pbio.0040382
4. Burkhalter, A. (2008). Many specialists for suppressing cortical excitation. Front. Neurosci. 22. doi:10.3389/neuro.01.026.2008
5. 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.
6. Cauli, B., Audinat, E., Lambolez, B., Angulo, M. C., Ropert, N., Tsuzuki, K., Hestrin, S., and Rossier, J. (1997). Molecular and physiological diversity of cortical nonpyramidal cells. J. Neurosci. 17, 3894-3906.
7. Cauli, B., Porter, J. T., Tsuzuki, K., Lambolez, B., Rossier, J., Quenet, B., and Audinat, E. (2000). Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc. Natl. Acad. Sci. U.S.A. 97, 6144-6149.
8. 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.
9. Clancy, B., Silva-Filho, M., and Friedlander, M. J. (2001). Structure and projections of white matter neurons in the postnatal rat visual cortex. J. Comp. Neurol. 434, 233-252.
10. Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M., and Snyder, S. H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. U.S.A. 88, 7797-7801.
11. Dawson, V. L., and Dawson, T. M. (1998). Nitric oxide in neurode-generation. Prog. Brain Res. 118, 215-229.
12. Douketis, C., Wang, Z., Haslett, T. L., and Moskovits, M. (1995). Fractal character of cold-deposited silver films determined by low-temperature scanning tunneling microscopy. Phys. Rev. B Condens. Matter 51, 11022-11031.
13. 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.
14. Dumitriu, D., Cossart, R., Huang, J., and Yuste, R. (2007). Correlation between axonal morphologies and synaptic input kinetics of interneurons from mouse visual cortex. Cereb. Cortex 17, 81-91.
15. Estrada, C., and Defelipe, J. (1998). Nitric oxide-producing neurons in the neocortex: morphological and functional relationship with intraparenchymal microvasculature. Cereb. Cortex 8, 193-203.
16. 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.
17. 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.
18. Franca, J. G., Volchan, E., Jain, N., Catania, K. C., Oliveira, R. L., Hess, F. F., Jablonka, M., Rocha-Miranda, C. E., and Kaas, J. H. (2000). Distribution of NADPH-diaphorase cells in visual and somatosensory cortex in four mammalian species. Brain Res. 864, 163-175.
19. Freire, M. A., Faber, J., Picanco-Diniz, C. W., Franca, J. G., and Pereira, A. (2012). Morphometric variability of nicotinamide adenine dinucleotide phosphate diaphorase neurons in the primary sensory areas of the rat. Neuroscience 205, 140-153.
20. Freire, M. A., Franca, J. G., Picanco-Diniz, C. W., and Pereira, A. Jr. (2005). Neuropil reactivity, distribution and morphology of NADPH diaphorase type I neurons in the barrel cortex of the adult mouse. J. Chem. Neuroanat. 30, 71-81.
21. Gabbott, P. L., and Bacon, S. J. (1995). Co-localisation of NADPH diaphorase activity and GABA immunoreactivity in local circuit neurones in the medial prefrontal cortex (mPFC) of the rat. Brain Res. 699, 321-328.
22. Gabbott, P. L., Dickie, B. G., Vaid, R. R., Headlam, A. J., and Bacon, S. J. (1997). Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: morphology and quantitative distribution. J. Comp. Neurol. 377, 465-499.
23. Gallopin, T., Geoffroy, H., Rossier, J., and Lambolez, B. (2006). Cortical sources of CRF, NKB, and CCK and their effects on pyramidal cells in the neocortex. Cereb. Cortex 16, 1440-1452.
24. Garbossa, D., Fontanella, M., Pagni, C. A., and Vercelli, A. (2001). Nitric oxide synthase and cytochrome c oxidase changes in the tumoural and peritumoural cerebral cortex. Acta Neurochir. (Wien) 143, 897-908.
25. Garthwaite, J. (2008). Concepts of neuralnitricoxide-mediated transmission. Eur. J. Neurosci. 27, 2783-2802.
26. Garthwaite, J., and Boulton, C. L. (1995). Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 57, 683-706.
27. Gelman, D. M., and Marin, O. (2010). Generation of interneuron diversity in the mouse cerebral cortex. Eur. J. Neurosci. 31, 2136-2141.
28. 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.
29. Gonchar, Y., and Burkhalter, A. (1997). Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7, 347-358.
30. 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
31. Hashikawa, T., Leggio, M. G., Hattori, R., and Yui, Y. (1994). Nitric oxide synthase immunoreactivity colocalized with NADPH-diaphorase histochemistry in monkey cerebral cortex. Brain Res. 641, 341-349.
32. Higo, S., Akashi, K., Sakimura, K., and Tamamaki, N. (2009). Sub-types of GABAergic neurons project axons in the neocortex. Front. Neuroanat. 3:25. doi:10.3389/neuro.05.025.2009
33. Higo, S., Udaka, N., and Tamamaki, N. (2007). Long-range GABAergic projection neurons in the cat neocortex. J. Comp. Neurol. 503, 421-431.
34. Iadecola, C., Beitz, A. J., Renno, W., Xu, X., Mayer, B., and Zhang, F. (1993). Nitric oxide synthase-containing neural processes on large cerebral arteries and cerebral microvessels. Brain Res. 606, 148-155.
35. 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.
36. Karagiannis, A., Gallopin, T., David, C., Battaglia, D., Geoffroy, H., Rossier, J., Hillman, E. M. C., Staiger, J. F., and Cauli, B. (2009). Classification of NPY-expressing neocortical interneurons. J. Neurosci. 29, 3642-3659.
37. Kilduff, T. S., Cauli, B., and Gerashchenko, D. (2011). Activation of cortical interneurons during sleep: an anatomical link to homeostatic sleep regulation? Trends Neurosci. 34, 10-19.
38. Kiss, J. P. (2000). Role of nitric oxide in the regulation of monoaminergic neurotransmission. Brain Res. Bull. 52, 459-466.
39. Kawaguchi, Y.(1995). Physiological subgroups of nonpyramidal cells with specific morphologicalcharacteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638-2655.
40. Kubota, Y., Hattori, R., and Yui, Y. (1994). Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res. 649, 159-173.
41. Kubota, Y., Shigematsu, N., Karube, F., Sekigawa, A., Kato, S., Yamaguchi, N., Hirai, Y., Morishima, M., and Kawaguchi, Y. (2011). Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb. Cortex 21, 1803-1817.
42. Lambolez, B., Audinat, E., Bochet, P., Crepel, F., and Rossier, J. (1992). AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247-258.
43. 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.
44. 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.
45. 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
46. Miyoshi, G., Butt, S. J., Takebayashi, H., and Fishell, G. (2007). Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2expressing precursors. J. Neurosci. 27, 7786-7798.
47. Moro, V., Badaut, J., Springhetti, V., Edvinsson, L., Seylaz, J., and Lasbennes, F. (1995). Regional study of the co-localization of neuronal nitric oxide synthase with muscarinic receptors in the rat cerebral cortex. Neuroscience 69, 797-805.
48. Oermann, E., Bidmon, H. J., Mayer, B., and Zilles, K. (1999). Differential maturational patterns of nitric oxide synthase-I and NADPH diaphorase in functionally distinct cortical areas of the mouse cerebral cortex. Anat. Embryol. 200, 27-41.
49. Paxinos, G., and Franklin, K. B. J. (2001). The Mouse Brain in Stereotaxic Coordinates. San Diego: Elsevier.
50. Perrenoud, Q., Rossier, J., Geoffroy, H., Vitalis, T., and Gallopin, T. (2012). Diversity of GABAergic interneurons in layer VIa and VIb of mouse barrel cortex. Cereb. Cortex. PMID: 22357664, [Epub ahead of print].
51. Rancillac, A., and Crepel, F. (2004). Synapses between parallel fibres and stellate cells express long-term changes in synaptic efficacy in rat cerebellum. J. Physiol. (Lond.) 554, 707-720.
52. Rancillac, A., Rossier, J., Guille, M., Tong, X. K., Geoffroy, H., Amatore, C., Arbault, S., Hamel, E., and Cauli, B. (2006). Glutamatergic control of microvascular tone by distinct GABA neurons in the cerebellum. J. Neurosci. 26, 6997-7006.
53. Sandell, J. H.(1986).NADPH diaphorasehistochemistryin the macaque striate cortex. J. Comp. Neurol. 251, 388-397.
54. Sholl, D. A. (1953). Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87, 387-406.
55. Smiley, J. F., McGinnis, J. P., and Javitt, D. C. (2000). Nitric oxide synthase interneurons in the monkey cerebral cortex are subsets of the somatostatin, neuropeptide Y, and calbindin cells. Brain Res. 863, 205-212.
56. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K., and Kaneko, T. (2003). Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 467, 60-79.
57. Tamas, G., Buhl, E. H., and Somogyi, P. (1997). Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J. Physiol. (Lond.) 500(Pt 3), 715-738.
58. 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.
59. Tomioka, R., and Rockland, K. S. (2007). Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter. J. Comp. Neurol. 505, 526-538.
60. Tsuzuki, K., Lambolez, B., Rossier, J., and Ozawa, S. (2001). Absolute quantification of AMPA receptor subunit mRNAs in single hippocampal neurons. J. Neurochem. 77, 1650-1659.
61. Valtschanoff, J. G., Weinberg, R. J., Kharazia, V. N., Schmidt, H. H., Nakane, M., and Rustioni, A. (1993). Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA. Neurosci. Lett. 157, 157-161.
62. Vercelli, A., Garbossa, D., Biasiol, S., Repici, M., and Jhaveri, S. (2000). NOS inhibition during postnatal development leads to increased ipsilateral retinocollicular and retinogeniculate projections in rats. Eur. J. Neurosci. 12, 473-490.
63. Vitalis, T., and Rossier, J. (2011). New insights into cortical interneurons development and classification: contribution of developmental studies. Dev. Neurobiol. 71, 34-44.
64. Vruwink, M., Schmidt, H. H., Weinberg, R. J., and Burette, A. (2001). Substance P and nitric oxide signaling in cerebral cortex: anatomical evidence for reciprocal signaling between two classes of interneurons. J. Comp. Neurol. 441, 288-301.
65. 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.
66. Ward, J. H. (1963). Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236-244.
67. Wiencken, A. E., and Casagrande, V. A. (2000). The distribution of NADPH diaphorase and nitric oxide synthetase (NOS) in relation to the functional compartments of areas V1 and V2 of primate visual cortex. Cereb. Cortex 10, 499-511.
68. Wonders, C. P., and Anderson, S. A. (2006). The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7, 687-696.
69. 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.
70. Xu, Q., Wonders, C. P., and Anderson, S. A. (2005). Sonic hedgehog maintains the identity of cor interneuron progenitors in the ventral telencephalon. Development 132, 4987-4998.
71. Xu, X., Roby, K. D., and Callaway, E. M. (2010). Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 518, 389-404.
72. Yan, X. X., and Garey, L. J. (1997). Mor- phological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex. J. Hirnforsch. 38, 165-172.
73. Yan, X. X., Jen, L. S., and Garey, L. J. (1996). NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb. Cortex 6, 524-529.
74. Zhou, L., and Zhu, D. Y. (2009). Neuronal nitric oxide synthase: structure, subcellular localization, regulation, and clinical implications. Nitric Oxide 20, 223-230.