Classification of NPY-expressing neocortical interneurons

Journal of Neuroscience

Volumn 29, Issue 11, 2009, Pages 3642-3659

  Karagiannis, Anastassios ^a,b   Gallopin, Thierry ^a   Dávid, Csaba ^c   Battaglia, Demian ^d,e   Geoffroy, Hélène ^a   Rossier, Jean ^a   Hillman, Elizabeth M C ^f   Staiger, Jochen F ^c   Cauli, Bruno ^a,b,g  

^a PSL RESEARCH UNIVERSITY   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e Bernstein Center for Computational Neuroscience   (Germany)

^f Fu Foundation School of Engineering and Applied Science   (United States)

^g CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; NITRIC OXIDE SYNTHASE; NUCLEAR FACTOR Y; PARVALBUMIN; SOMATOSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; CELL LABELING; CELL POPULATION; CONTROLLED STUDY; GLIA; INTERNEURON; MALE; NEOCORTEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOMATOSENSORY CORTEX;

ACTION POTENTIALS; ANIMALS; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MALE; NEOCORTEX; NEUROPEPTIDE Y; RATS; RATS, WISTAR;

EID: 63849258894     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0058-09.2009     Document Type: Article

References (116)

1. Abounader R, Hamel E (1997) Associations between neuropeptide Y nerve terminals and intraparenchymal microvessels in rat and human cerebral cortex. J Comp Neurol 388:444-453.
2. Allen YS, Adrian TE, Allen JM, Tatemoto K, Crow TJ, Bloom SR, Polak JM (1983) Neuropeptide Y distribution in the rat brain. Science 221:877-879.
3. Andjelic S, Gallopin T, Cauli B, Hill EL, Roux L, Badr S, Hu E, Tamás G, Lambolez B (2009) Glutamatergic non-pyramidal neurons from neocortical layer VI and their comparison with pyramidal and spiny stellate neurons. J Neurophysiol 101:641-654.
4. Aoki C, Pickel VM (1989) Neuropeptide Y in the cerebral cortex and the caudate-putamen nuclei: ultrastructural basis for interactions with GABAergic and non-GABAergic neurons. J Neurosci 9:4333-4354.
5. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairén A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, et al. (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557-568.
6. Bacci A, Huguenard JR, Prince DA (2002) Differential modulation of synaptic transmission by neuropeptide Y in rat neocortical neurons. Proc Natl Acad Sci U S A 99:17125-17130.
7. Bannon AW, Seda J, Carmouche M, Francis JM, Norman MH, Karbon B, McCaleb ML (2000) Behavioral characterization of neuropeptide Y knockout mice. Brain Res 868:79-87.
8. Bao L, Kopp J, Zhang X, Xu ZQ, Zhang LF, Wong H, Walsh J, Hökfelt T (1997) Localization of neuropeptide Y Yl receptors in cerebral blood vessels. Proc Natl Acad Sci U S A 94:12661-12666.
9. Baraban SC, Hollopeter G, Erickson JC, Schwartzkroin PA, Palmiter RD (1997) Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J Neurosci 17:8927-8936.
10. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P (1993) The metabotropic glutamate receptor (mGluRl alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
11. Bayraktar T, Staiger JF, Acsady L, Cozzari C, Freund TF, Zilles K (1997) Co-localization of vasoactive intestinal polypeptide, gamma- aminobutyric acid and choline acetyltransferase in neocortical interneurons of the adult rat. Brain Res 757:209-217.
12. Bayraktar T, Welker E, Freund TF, Zilles K, Staiger JF (2000) Neurons immunoreactive for vasoactive intestinal polypeptide in the rat primary somatosensory cortex: morphology and spatial relationship to barrel-related columns. J Comp Neurol 420:291-304.
13. Beierlein M, Gibson JR, Connors BW (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3:904-910.
14. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987-3000.
15. Bidmon HJ, Wu J, Gödecke A, Schleicher A, Mayer B, Zilles K (1997) Nitric oxide synthase-expressing neurons are area-specifically distributed within the cerebral cortex of the rat. Neuroscience 81:321-330.
16. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17:3894-3906.
17. Cauli B, Porter JT, Tsuzuki K, Lambolez B, Rossier J, Quenet B, Audinat E (2000) Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci U S A 97:6144-6149.
18. Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E (2004) Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 24:8940-8949.
19. Celio MR (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231:995-997.
20. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
21. Choudhuri R, Cui L, Yong C, Bowyer S, Klein RM, Welch KM, Berman NE (2002) Cortical spreading depression and gene regulation: relevance to migraine. Ann Neurol 51:499-506.
22. Christophe E, Roebuck A, Staiger JF, Lavery DJ, Charpak S, Audinat E (2002) Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons. J Neurophysiol 88:1318-1327.
23. Chu Z, Galarreta M, Hestrin S (2003) Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 23:96-102.
24. Clausen TR, Møller M, Woldbye DP (2001) Inhibitory effect of neuropeptide Y on morphine withdrawal is accompanied by reduced c-fos expression in specific brain regions. J Neurosci Res 64:410-417.
25. Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99-104.
26. Dacey RG Jr, Bassett JE, Takayasu M (1988) Vasomotor responses of rat intracerebral arterioles to vasoactive intestinal peptide, substance P, neuropeptide Y, and bradykinin. J Cereb Blood Flow Metab 8:254-261.
27. Dávid C, Schleicher A, Zuschratter W, Staiger JF (2007) The innervation of parvalbumin-containing interneurons by VIP-immunopositive interneurons in the primary somatosensory cortex of the adult rat. Eur J Neurosci 25:2329-2340.
28. Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH (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.
29. de Kock CP, Sakmann B (2008) High frequency action potential bursts ( > or = 100 Hz) in L2/3 and L5B thick tufted neurons in anaesthetized and awake rat primary somatosensory cortex. J Physiol 586:3353-3364.
30. Demeulemeester H, Vandesande F, Orban GA, Brandon C, Vanderhaeghen JJ (1988) Heterogeneity of GABAergic cells in cat visual cortex. J Neurosci 8:988-1000.
31. Demeulemeester H, Arckens L, Vandesande F, Orban GA, Heizmann CW, Pochet R (1991) Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp Brain Res 84:538-544.
32. Devor A, Tian P, Nishimura N, Teng IC, Hillman EM, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM (2007) Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 27:4452-4459.
33. Dodt HU, Zieglgänsberger W (1998) Visualization of neuronal form and function in brain slices by infrared videomicroscopy. Histochem J 30:141-152.
34. Dumitriu D, Cossart R, Huang J, Yuste R (2007) Correlation between axonal morphologies and synaptic input kinetics of interneurons from mouse visual cortex. Cereb Cortex 17:81-91.
35. Estrada C, DeFelipe J (1998) Nitric oxide-producing neurons in the neocortex: morphological and functional relationship with intraparenchymal microvasculature. Cereb Cortex 8:193-203.
36. Férézou I, Cauli B, Hill EL, Rossier J, Hamel E, Lambolez B (2002) 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J Neurosci 22:7389-7397.
37. Férézou I, Hill EL, Cauli B, Gibelin N, Kaneko T, Rossier J, Lambolez B (2007) Extensive overlap of μ-opioid and nicotinic sensitivity in cortical interneurons. Cereb Cortex 17:1948-1957.
38. Fisher RA, Yates F (1963) Statistical tables for biological, agricultural and medical research. Edinburgh: Oliver and Boyd.
39. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33-42.
40. Fuentealba P, Begum R, Capogna M, Jinno S, Márton LF, Csicsvari J, Thomson A, Somogyi P, Klausberger T (2008) Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 57:917-929.
41. Gabbott PL, Dickie BG, Vaid RR, Headlam AJ, Bacon SJ (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.
42. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
43. Gallopin T, Geoffroy H, Rossier J, Lambolez B (2006) Cortical sources of CRF, NKB, and CCK and their effects on pyramidal cells in the neocortex. Cereb Cortex 16:1440-1452.
44. Gerashchenko D, Wisor JP, Burns D, Reh RK, Shiromani PJ, Sakurai T, de la Iglesia HO, Kilduff TS (2008) Identification of a population of sleep-active cerebral cortex neurons. Proc Natl Acad Sci USA 105:10227-10232.
45. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
46. + channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58:387-400.
47. Golomb D, Donner K, Shacham L, Shlosberg D, Amitai Y, Hansel D (2007) Mechanisms of firing patterns in fast-spiking cortical interneurons. PLoS Comput Biol 3:e156.
48. Gonchar Y, Burkhalter A (1997) Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7:347-358.
49. Gonchar Y, Wang Q, Burkhalter A (2007) Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat 1:3.
50. Görcs TJ, Léránth C, MacLusky NJ (1986) The use of gold-substituted silver-intensified diaminobenzidine (DAB) and non-intensified DAB for simultaneous electron microscopic immunoperoxidase labeling of tyrosine hydroxylase and glutamic acid decarboxylase immunoreactivity in the rat medial preoptic area. J Histochem Cytochem 34:1439-1447.
51. Gulledge AT, ParkSB, Kawaguchi Y, Stuart GJ (2007) Heterogeneity of phasic cholinergic signalling in neocortical neurons. J Neurophysiol 97:2215-2229.
52. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273-278.
53. Haj-Dahmane S, Andrade R (1997) Calcium-activated cation nonselective current contributes to the fast afterdepolarization in rat prefrontal cortex neurons. J Neurophysiol 78:1983-1989.
54. Halabisky B, Shen F, Huguenard JR, Prince DA (2006) Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol 96:834-845.
55. Hartigan JA, Wong MA (1979) Algorithm AS 136: a K-means clustering algorithm. Appl Stat 28:100-108.
56. Helmstaedter M, Sakmann B, Feldmeyer D (2009) The relation between dendritic geometry, electrical excitability, and axonal projections of L2/3 interneurons in rat barrel cortex. Cereb Cortex 19:938-950.
57. Hendry SH, Jones EG, DeFelipe J, Schmechel D, Brandon C, Emson PC (1984a) Neuropeptide-containing neurons of the cerebral cortex are also GABAergic. Proc Natl Acad Sci USA 81:6526-6530.
58. Hendry SH, Jones EG, Emson PC (1984b) Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex. J Neurosci 4:2497-2517.
59. Hestrin S, Armstrong WE (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci 16:5290-5300.
60. Higo S, Udaka N, Tamamaki N (2007) Long-range GABAergic projection neurons in the cat neocortex. J Comp Neurol 503:421-431.
61. Hodgkin AL (1948) The local electric changes associated with repetitive action in a non-medullated axon. J Physiol 107:165-181.
62. Jacobowitz DM, Winsky L (1991) Immunocytochemical localization of calretinin in the forebrain of the rat. J Comp Neurol 304:198-218.
63. Jin X, Mathers PH, Szabo G, Katarova Z, Agmon A (2001) Vertical bias in dendritic trees of non-pyramidal neocortical neurons expressing GAD67-GFP in vitro. Cereb Cortex 11:666-678.
64. Judas M, Sestan N, Kostoviæ: 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.
65. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M (2007) Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10:743-753.
66. Karube F, Kubota Y, Kawaguchi Y (2004) Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J Neurosci 24:2853-2865.
67. Kawaguchi Y (1993) Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69:416-431.
68. 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.
69. Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387-396.
70. Kawaguchi Y, 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.
71. Kubota Y, Hattori R, Yui Y (1994) Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649:159-173.
72. Kuljis RO, Rakic P (1989a) Distribution of neuropeptide Y-containing perikarya and axons in various neocortical areas in the macaque monkey. J Comp Neurol 280:383-392.
73. Kuljis RO, Rakic P (1989b) Multiple types of neuropeptide Y-containing neurons in primate neocortex. J Comp Neurol 280:393-409.
74. Lambolez B, Audinat E, Bochet P, Crépel F, Rossier J (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9:247-258.
75. Lee JE, Jeon CJ (2005) Immunocytochemical localization of nitric oxide synthase-containing neurons in mouse and rabbit visual cortex and colocalization with calcium-binding proteins. Mol Cells 19:408-417.
76. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A (2006) Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26:5069-5082.
77. MacQueen JB (1967) Some methods of classification and analysis of multivariate observations. In: Proceedings of the fifth Berkeley symposium in mathematical statistics and probability, Vol 1, pp 281-297. Berkeley, CA: University of California.
78. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806.
79. Morrison JH, Magistretti PJ, Benoit R, Bloom FE (1984) The distribution and morphological characteristics of the intracortical VIP-positive cell: an immunohistochemical analysis. Brain Res 292:269-282.
80. Mountcastle VB, Talbot WH, Sakata H, Hyvärinen J (1969) Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol 32:452-484.
81. Nelson SB, Sugino K, Hempel CM (2006) The problem of neuronal cell types: a physiological genomics approach. Trends Neurosci 29:339-345.
82. Oláh S, Komlósi G, Szabadics J, Varga C, Tóth E, Barzó P, Tamás G (2007) Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex. Front Neural Circuits 1:4.
83. Porter JT, Cauli B, Staiger JF, Lambolez B, Rossier J, Audinat E ( 1998) Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex. Eur J Neurosci 10:3617-3628.
84. Porter JT, Cauli B, Tsuzuki K, Lambolez B, Rossier J, Audinat E (1999) Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J Neurosci 19:5228-5235.
85. Povysheva NV, Zaitsev AV, Kröner S, Krimer OA, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS (2007) Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. J Neurophysiol 97:1030-1039.
86. Povysheva NV, Zaitsev AV, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS (2008) Parvalbumin-positive basket interneurons in monkey and rat prefrontal cortex. J Neurophysiol 100:2348-2360.
87. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CAl area. J Neurosci 25:6775-6786.
88. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1:279-285.
89. Rogers JH (1992) Immunohistochemical markers in rat cortex: colocalization of calretinin and calbindin-D28k with neuropeptides and GABA. Brain Res 587:147-157.
90. Rousseeuw PJ (1987) Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math 20:53-65.
91. Schubert D, Staiger JF, Cho N, Kötter R, Zilles K, Luhmann HJ (2001) Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J Neurosci 21:3580-3592.
92. Schubert D, Kötter R, Zilles K, Luhmann HJ, Staiger JF (2003) Cell type-specific circuits of cortical layer IV spiny neurons. J Neurosci 23:2961-2970.
93. Simon A, Oláh S, Molnár G, Szabadics J, Tamás G (2005) Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J Neurosci 25:6278-6285.
94. Smiley JF, McGinnis JP, Javitt DC (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.
95. Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu JY (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material. J Neurosci 4:2590-2603.
96. Staiger JF, Schubert D, Zuschratter W, Kötter R, Luhmann HJ, Zilles K (2002) Innervation of interneurons immunoreactive for VIP by intrinsically bursting pyramidal cells and fast-spiking interneurons in infragranular layers of juvenile rat neocortex. Eur J Neurosci 16:11-20.
97. Staiger JF, Flagmeyer I, Schubert D, Zilles K, Kötter R, Luhmann HJ (2004) Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cereb Cortex 14:690-701.
98. Stuart GJ, Dodt HU, Sakmann B (1993) Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch 423:511-518.
99. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, Wu C, Huang ZJ, Nelson SB (2006) Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 9:99-107.
100. Szabadics J, Tamás G, Soltesz I (2007) Different transmitter transients underlie presynaptic cell type specificity of GABAA, slow and GABAA, fast. Proc Natl Acad Sci U S A 104:14831-14836.
101. Tamás G, Buhl EH, Somogyi P (1997) Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J Physiol 500:715-738.
102. Tamas G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902-1905.
103. Tamas G, Szabadics J, Lörincz A, Somogyi P (2004) Input and frequency-specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin. Eur J Neurosci 20:2681-2690.
104. Toledo-Rodriguez M, Goodman P, Illic M, Wu C, Markram H (2005) Neuropeptide and calcium binding protein gene expression profiles predict neuronal anatomical type in the juvenile rat. J Physiol 567:401-413.
105. Tomioka R, Rockland KS (2007) Long-distance corticocortical GABAergic neurons in the adult monkey white and gray matter. J Comp Neurol 505:526-538.
106. Tomioka R, Okamoto K, Furuta T, Fujiyama F, Iwasato T, Yanagawa Y, Obata K, Kaneko T, Tamamaki N (2005) Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur J Neurosci 21:1587-1600.
107. Tyner CF (1975) The naming of neurons: applications of taxonomic theory to the study of cellular populations. Brain Behav Evol 12:75-96.
108. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, Kawaguchi Y (2008) Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 18:315-330.
109. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H (2002) Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12:395-410.
110. Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, Luo J, Markram H (2004) Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 561:65-90.
111. Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236-244.
112. Yan XX, Garey LJ (1997) Morphological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex. J Hirnforsch 38:165-172.
113. Yan XX, Jen LS, Garey LJ (1996) NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb Cortex 6:524-529.
114. Zaitsev AV, Povysheva NV, Gonzalez-Burgos G, Rotaru D, Fish KN, Krimer LS, Lewis DA (2008) Interneuron diversity in layers 2-3 of monkey prefrontal cortex. Cereb Cortex. Advance online publication. Retrieved March 5, 2009. doi:10.1093/cercor/bhnl98.
115. Zhou FM, Hablitz JJ (1996) Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties. J Neurophysiol 76:651-667.
116. Zhou FM, Hablitz JJ (1999) Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex. J Neurophysiol 82:2989-2999.