Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex

Cerebral Cortex

Volumn 14, Issue 12, 2004, Pages 1310-1327

  Toledo Rodriguez, Maria ^a,b   Blumenfeld, Barak ^b   Wu, Caizhi ^c   Luo, Junyi ^c   Attali, Bernard ^d   Goodman, Philip ^e   Markram, Henry ^a  

^a EPFL   (Switzerland)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c Simons Center for Quantitative Biology   (United States)

^d TEL AVIV UNIVERSITY   (Israel)

^e UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Cortex; Electrophysiology; Ion channel; Neuron; Single cell RT PCR

Indexed keywords

CALBINDIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM BINDING PROTEIN; CALRETININ; ION CHANNEL; PARVALBUMIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.2; POTASSIUM CHANNEL KV1.4; POTASSIUM CHANNEL KV1.6; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CALCIUM ACTIVATED POTASSIUM CHANNEL SK2; CALCULATION; DNA LIBRARY; ELECTROPHYSIOLOGY; GENE EXPRESSION PROFILING; NEOCORTEX; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; POTASSIUM CHANNEL KV2.1; POTASSIUM CHANNEL KV2.2; POTASSIUM CHANNEL KV3.1; POTASSIUM CHANNEL KV3.2; POTASSIUM CHANNEL KV3.3; POTASSIUM CHANNEL KV3.4; POTASSIUM CHANNEL KV4.2; POTASSIUM CHANNEL KV4.3; POTASSIUM CHANNEL KVBETA1; POTASSIUM CHANNEL KVBETA2; PREDICTION; PRIORITY JOURNAL; RAT; REGRESSION ANALYSIS; RELIABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM POTASSIUM PERMEABLE HYPERPOLARIZATION ACTIVATED CHANNEL HCN1; SODIUM POTASSIUM PERMEABLE HYPERPOLARIZATION ACTIVATED CHANNEL HCN2; SODIUM POTASSIUM PERMEABLE HYPERPOLARIZATION ACTIVATED CHANNEL HCN3; SODIUM POTASSIUM PERMEABLE HYPERPOLARIZATION ACTIVATED CHANNEL HCN4; VOLTAGE GATED CALCIUM CHANNEL CALCIUM ALPHA1A; VOLTAGE GATED CALCIUM CHANNEL CALCIUM ALPHA1B; VOLTAGE GATED CALCIUM CHANNEL CALCIUM ALPHA1G; VOLTAGE GATED CALCIUM CHANNEL CALCIUM ALPHA1I; VOLTAGE GATED CALCIUM CHANNEL CALCIUM BETA1; VOLTAGE GATED CALCIUM CHANNEL CALCIUM BETA3; VOLTAGE GATED CALCIUM CHANNEL CALCIUM BETA4;

ACTION POTENTIALS; ANIMALS; GENE EXPRESSION PROFILING; NEOCORTEX; NEURONS; PREDICTIVE VALUE OF TESTS; RATS; RATS, WISTAR;

EID: 5044239577     PISSN: 10473211     EISSN: None     Source Type: Journal    
DOI: 10.1093/cercor/bhh092     Document Type: Article

References (66)

1. Adamson C, Reid M, Mo Z, Bowne-English J, Davis R (2002) Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. J Comp Neurol 447:331-350.
2. Aranda-Abreu G, Behar L, Chung S, Furneaux H, Ginzburg I (1999) Embryonic lethal abnormal vision-like RNA·binding proteins regulate neurite outgrowth and tau expression in PC12 cells. J Neurosci 19:6907-6917.
3. Baranauskas G, Tkatch T, Surmeier DJ (1999) Delayed rectifier currents in rat globus pallidus neurons are attributable to Kv2.1 and Kv3.1/3.2 K(+) channels. J Neurosci 19:6394-6404.
4. Baranauskas G, Tkatch T, Nagata K, Yeh JZ, Surmeier DJ (2003) Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons. Nat Neurosci 6:258-266.
5. Brady G, Barbara M, Iscove NN (1990) Representative in vitro cDNA amplification from individual hemopoietic cells and colonies. Methods Mol Cell Biol 2:17-25.
6. Castellano A, Wei X, Birnbaumer L, Perez-Reyes E (1993) cloning and expression of a third calcium channel beta subunit. J Biol Chem 268:3450-3455.
7. 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.
8. 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 USA 97:6144-6149.
9. Chiang MK, Melton DA (2003) Single-cell transcript analysis of pancreas development. Dev Cell 4:383-393.
10. Chitwood R, Hubbard A, Jaffe D (1999) Passive electrotonic properties of rat hippocampal Ca3 interneurones. J Physiol 515:743-756.
11. Chow A, Erisir A, Farb C, Nadal MS, Ozaita A, Lau D, Welker E, Rudy B (1999) K(+) channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J Neurosci 19:9332-9345.
12. Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, Moreno H, Nadal MS, Ozaita A, Pountney D, Saganich M, Vega-Saenz de Miera E, Rudy B (1999) Molecular diversity of K+ channels. Ann N Y Acad Sci 868:233-285.
13. DeFelipe J (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1-19.
14. Dixon AK, Richardson PJ, Lee K, Carter NP, Freeman TC (1998) Expression profiling of single cells using 3 prime end amplification (TPEA) PCR., Nucleic Acids Res 26:4426-4431.
15. Du J, Haak LL, Phillips-Tansey E, Russell JT, McBain CJ (2000) Frequency-dependent regulation of rat hippocampal somatodendritic excitability by the K+ channel subunit Kv2.1. J Physiol 522:19-31.
16. Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195-206.
17. Eberwine J, Yeh H, Miyarisho KCY (1992) Analysis of gene expression in single live neurons. Proc Natl Acad Sci USA 89:3010-3014.
18. Edwards MC, Gibbs RA (1994) Multiplex PCR: advantages, development, and applications. PCR Methods Appl 3:S65-S75.
19. Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476-2489.
20. Ertel S, Eitel E (1997) Low-voltage-activated T-type Ca2+ channels. Trends Pharmacol Sci 18:37-42.
21. Fan Y, Horn E, Waldrop T (2001) Biophysical characterization of rat caudal hypothalamic neurons: calcium channel contribution to excitability. J Neurophysiol 84:2896-2903.
22. Foehring RC, Mermelstein PG, Song WJ, Ulrich S, Surmeier DJ (2000) Unique properties of R-type calcium currents in neocortical and neostriatal neurons. J Neurophysiol 84:2225-2236.
23. Franz O, Liss B, Neu A, Roeper J (2000) Single-cell mRNA expression of HCN1 correlates with a fast gating phenotype of hyperpolarization-activated cyclic nucleotide-gated ion channels (Ih) in central neurons. Eur J Neurosci 12:2685-2693.
24. Ginsberg S, Che S (2002) RNA amplification in brain tissues. Neurochem Res 27:981-992.
25. Glasgow E, Kusano K, Chin H, Mezey E, Young WS III, Gainer H (1999) Single cell reverse transcription-polymerase chain reaction analysis of rat supraoptic magnocellular neurons: neuropeptide phenotypes and high voltage-gated calcium channel subtypes. Endocrinology 140:5391-5401.
26. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273-278.
27. Harvey A (1997) Recent studies on dendrotoxins and potassium ion channels. Gen Pharmacol 28:7-12.
28. Hille B (2001) Ionic channels of excitable membranes. Sunderland, MA: Sinauer.
29. Johnston D, Wu SM-S (1995) Fundations of cellular neurophysiology. Cambridge, MA: MIT Press.
30. Kamme F, Salunga R, Yu J, Tran DT, Zhu J, Luo L, Bittner A, Guo HQ, Miller N, Wan J, Erlander M (2003) Single-cell microarray analysis in hippocampus CA1: demonstration and validation of cellular heterogeneity. J Neurosci 23:3607-3615.
31. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
32. Lambolez B, Audinat E, Bochet P, Crepel F, Rossier J (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9:247-258.
33. Lee JH, Daud A, Cribbs L, Lacerda A, Pereverzev A, Klockner U, Schneider T, Perez-Reyes E (1999) Cloning and expression of a novel member of the low voltage-activated T-type calcium channel family. J Neurosci 19:1912-1921.
34. Lien C, 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.
35. Lien CC, Martina M, Schultz JH, Ehmke H, Jonas P (2002) Gating, modulation and subunit composition of voltage-gated K(+) channels in dendritic inhibitory interneurones of rat hippocampus. J Physiol 538:405-419.
36. Lin SL, Chuong CM, Widelitz RB, Ying SY (1999) In vivo analysis of cancerous gene expression by RNA-polymerase chain reaction. Nucleic Acids Res 27:4585-4589.
37. Liss B, Franz O, Sewing S, Bruns R, Neuhoff H, Roeper J (2001) Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription. EMBO J 20:5715-5724.
38. Magee J (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
39. Markram H, Lubke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500:409-440.
40. Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:8111-8125.
41. Mermelstein PG, Foehring RC, Tkatch T, Song WJ, Baranauskas G, Surmeier DJ (1999) Properties of Q-type calcium channels in neostriatal and cortical neurons are correlated with beta subunit expression. J Neurosci 19:7268-7277.
42. Miller A (2002) Subset selection in regression. New York: Chapman & Hall/CRC.
43. Monyer H, Jonas P (1995) Polymerase chain reaction analysis of ion channel expression in single neurons of brain slices. In: Single-channel recordings (Sakmann B, Neher E, eds), pp. 357-373. New York: Plenum Press.
44. Monyer H, Lambolez B (1995) Molecular biology and physiology at the single-cell level. Curr Opin Neurobiol 5:382-387.
45. Moreno Davila H (1999) Molecular and functional diversity of voltage-gated calcium channels. Ann N Y Acad Sci 868:102-117.
46. Plant TD, Schirra C, Katz E, Uchitel OD, Konnerth A (1998) Single-cell RT-PCR and functional characterization of Ca2+ channels in motoneurons of the rat facial nucleus. J Neurosci 18:9573-9584.
47. 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.
48. Rettig J, Heinemann SH, Wunder F, Lorra C, Parcej DN, Dolly JO, Pongs O (1994) Inactivation properties of voltage-gated K+ channels altered by presence of beta-subunit. Nature 369:289-294.
49. Rudy B, McBain CJ (2001) Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci 24:517-526.
50. Sakmann B, Neher E (1995) Single-channel recordings. New York: Plenum Press.
51. Santoro B, Tibbs GR (1999) The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels. Ann N Y Acad Sci 868:741-764.
52. Seifert G, Kuprijanova E, Zhou M, Steinhauser C (1999) Developmental changes in the expression of Shaker- and Shab-related K(+) channels in neurons of the rat trigeminal ganglion. Brain Res Mol Brain Res 74:55-68.
53. Shibata R, Nakahira K, Shibasaki K, Wakazono Y, Imoto K, Ikenaka K (2000) A-type K+ current mediated by the Kv4 channel regulates the generation of action potential in developing cerebellar granule cells. J Neurosci 20:4145-4155.
54. Song WJ, Tkatch T, Baranauskas G, Ichinohe N, Kitai ST, Surmeier DJ (1998) Somatodendritic depolarization-activated potassium currents in rat neostriatal cholinergic interneurons are predominantly of the A type and attributable to coexpression of Kv4.2 and Kv4.1 subunits. J Neurosci 18:3124-3137.
55. Stocker M, Pedarzani P (2000) Differential distribution of three Ca(2+)-activated K(+) channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol Cell Neurosci 15:476-493.
56. Sucher NJ, Deitcher DL (1995) PCR and patch-clamp analysis of single neurons. Neuron 14:1095-1100.
57. Surmeier DJ, Song WJ, Van Z (1996) Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 16:6579-6591.
58. Talley E, Cribbs L, Lee J, Daud A, Perez-Reyes E, Bayliss D (1999) Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19:1895-1911.
59. Tanaka O, Sakagami H, Kondo H (1995) Localization of mRNAs of voltage-dependent Ca(2+)-channels: four subtypes of alpha 1- and beta-subunits in developing and mature rat brain. Brain Res Mol Brain Res 30:1-16.
60. Tietjen I, Rihel J, Cao Y, Koentges G, Zakhary L, Dulac C (2003) Single-cell transcriptional analysis of neuronal progenitors. Neuron 38:161-175.
61. Toledo-Rodriguez M, Gupta A, Wang Y, Wu CZ, Markram H (2002) Neocortex, basic neuron types. In: The handbook of brain theory and neural networks (Arbib MA, ed.), pp. 719-725. Cambridge, MA: MIT Press.
62. Vergara C, Latorre R, Marrion NV, Adelman JP (1998) Calcium-activated potassium channels. Curr Opin Neurobiol 8:321-329.
63. Wang F, Parcej DN, Dolly JO (1999) Alpha subunit compositions of Kv1.1-containing K channel subtypes fractionated from rat brain using dendrotoxins. Eur J Biochem 263:230-237.
64. 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.
65. Ward JHJ (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236-244.
66. Yan Z, Surmeier DJ (1996) Muscarinic (m2/m4) receptors reduce N- and P-type Ca2+ currents in rat neostriatal cholinergic interneurons through a fast, membrane-delimited, G-protein pathway. J Neurosci 16:2592-2604.