Functional and molecular development of striatal fast-spiking GABAergic interneurons and their cortical inputs

European Journal of Neuroscience

Volumn 22, Issue 5, 2005, Pages 1097-1108

  Plotkin, Joshua L ^a   Wu, Nanping ^a   Chesselet, Marie Françoise ^a   Levine, Michael S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

GAD67; Kv3.1; Parvalbumin; Rat; Striatum

Indexed keywords

BICUCULLINE METHIODIDE; CALSENILIN; GLUTAMATE DECARBOXYLASE 67; MESSENGER RNA; PARVALBUMIN;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CORPUS STRIATUM; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; INTERNEURON; MALE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPTOGENESIS;

ACTION POTENTIALS; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; CEREBRAL CORTEX; CORPUS STRIATUM; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DECARBOXYLASE; IN SITU HYBRIDIZATION; INTERNEURONS; ISOENZYMES; MALE; MEMBRANE POTENTIALS; NEURONS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 25844435768     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04303.x     Document Type: Article

References (51)

1. Bayer, S.A. (1984) Neurogenesis in the rat neostriatum. Int. J. Dev. Neurosci., 2, 163-175.
2. Bennett, B.D. & Bolam, J.P. (1994) Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat. Neuroscience, 62, 707-719.
3. 2+-binding protein parvalbumin: molecular cloning and developmental regulation of mRNA abundance. Proc. Natl Acad. Sci. USA, 82, 1414-1418.
4. Bracci, E., Centonze, D., Bernardi, G. & Calabresi, P. (2002) Dopamine excites fast-spiking interneurons in the striatum. J. Neurophysiol., 87, 2190-2194.
5. Cepeda, C., Hurst, R.S., Altemus, K.L., Flores-Hernandez, J., Calvert, C.R., Jokel, E.S., Grandy, D.K., Low, M.J., Rubinstein, M., Ariano, M.A. & Levine, M.S. (2001) Facilitated glutamatergic transmission in the striatum of D2 dopamine receptor-deficient mice. J. Neurophysiol., 85, 659-670.
6. Chapman, D.E., Keefe, K.A. & Wilcox, K.S. (2003) Evidence for functionally distinct synaptic NMDA receptors in ventromedial versus dorsolateral striatum. J. Neurophysiol., 89, 69-80.
7. Chesselet, M.F. (1996) Quantitative analysis and interpretation of data for in situ hybridization at the cellular level. In Henderson, Z. (Ed.), In Situ Hybridization Techniques for the Brain. John Wiley and Sons Ltd, Chichester, England, pp. 141-149.
8. Chesselet, M.F., MacKenzie, L. & Eberle-Wang, K. (1996) In situ hybridization using 35S- and digoxigenin-labeled RNA probes. In Henderson, Z. (Ed.), In Situ Hybridization Techniques for the Brain. John Wiley and Sons Ltd, Chichester, England, pp. 79-109.
9. Chesselet, M.F., Mercugliano, M., Soghomonian, J.J., Salin, P., Qin, Y. & Gonzales, C. (1993) Regulation of glutamic acid decarboxylase gene expression in efferent neurons of the basal ganglia. Prog. Brain Res., 99, 143-154.
10. Chesselet, M.F. & Robbins, E. (1989) Characterization of striatal neurons expressing high levels of glutamic acid decarboxylase messenger RNA. Brain Res., 492, 237-244.
11. Chesselet, M.F., Weiss, L., Wuenschell, C., Tobin, A.J. & Affolter, H.U. (1987) Comparative distribution of mRNAs for glutamic acid decarboxylase, tyrosine hydroxylase, and tachykinins in the basal ganglia: an in situ hybridization study in the rodent brain. J. Comp. Neurol., 262, 125-140.
12. Colwell, C.S., Cepeda, C., Crawford, C. & Levine, M.S. (1998) Postnatal development of glutamate receptor-mediated responses in the neostriatum. Dev. Neurosci., 20, 154-163.
13. Cowan, R.L., Wilson, C.J., Emson, P.C. & Heizmann, C.W. (1990) Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J. Comp. Neurol., 302, 197-205.
14. Fentress, J.C., Stanfield, B.B. & Cowan, W.M. (1981) Observation on the development of the striatum in mice and rats. Anat. Embryol (Berl.), 163, 275-298.
15. Hattori, T. & McGeer, P.L. (1973) Synaptogenesis in the corpus striatum of infant rat. Exp. Neurol., 38, 70-79.
16. Hurst, R.S., Cepeda, C., Shumate, L.W. & Levine, M.S. (2001) Delayed postnatal development of NMDA receptor function in medium-sized neurons of the rat striatum. Dev. Neurosci., 23, 122-134.
17. + currents. Neurosci. Lett., 231, 13-16.
18. Kanemasa, T., Gan, L., Perney, T.M., Wang, L.Y. & Kaczmarek, L.K. (1995) Electrophysiological and pharmacological characterization of a mammalian Shaw channel expressed in NIH 3T3 fibroblasts. J. Neurophysiol., 74, 207-217.
19. Kawaguchi, Y. (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci., 13, 4908-4923.
20. Kawaguchi, Y., Wilson, C.J., Augood, S.J. & Emson, P.C. (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci., 18, 527-535.
21. Kita, H. & Armstrong, W. (1991) A biotin-containing compound N-(2-aminoethyl) biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin. J. Neurosci. Meth, 37, 141-150.
22. Kita, H., Kosaka, T. & Heizmann, C.W. (1990) Parvalbumin- immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res., 536, 1-15.
23. Koos, T. & Tepper, J.M. (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci., 2, 467-472.
24. Kuppers, E., Sabolek, M., Anders, U., Pilgrim, C. & Beyer, C. (2000) Developmental regulation of glutamic acid decarboxylase mRNA expression and splicing in the rat striatum by dopamine. Brain Res. Mol. Brain Res., 81, 19-28.
25. Lenz, S., Perney, T.M., Qin, Y., Robbins, E. & Chesselet, M.F. (1994) GABAergic interneurons of the striatum express the Shaw-like potassium channel Kv3.1. Synapse, 18, 55-66.
26. Liu, S.Q. & Kaczmarek, L.K. (1998) Depolarization selectively increases the expression of the Kv3.1 potassium channel in developing inferior colliculus neurons. J. Neurosci., 18, 8758-8769.
27. Luk, K.C. & Sadikot, A.F. (2001) GABA promotes survival but not proliferation of parvalbumin-immunoreactive interneurons in rodent neostriatum: an in vivo study with stereology. Neuroscience, 104, 93-103.
28. + channel diversity in the mammalian central nervous system. Proc. Natl Acad. Sci. USA, 88, 3932-3936.
29. Misgeld, U., Dodt, H.U. & Frotscher, M. (1986) Late development of intrinsic excitation in the rat neostriatum: an in vitro study. Brain Res., 392, 59-67.
30. Miyazaki, H., Nakamura, Y., Arai, T. & Kataoka, K. (1997) Increase of glutamate uptake in astrocytes: a possible mechanism of action of volatile anesthetics. Anesthesiology, 86, 1359-1366; discussion 1358A.
31. Perney, T.M. & Kaczmarek, L.K. (1997) Localization of a high threshold potassium channel in the rat cochlear nucleus. J. Comp. Neurol., 386, 178-202.
32. Plenz, D. & Aertsen, A. (1996) Neural dynamics in cortex-striatum co-cultures -I. anatomy and electrophysiology of neuronal cell types. Neuroscience, 70, 861-891.
33. Plenz, D. & Kitai, S.T. (1998) Up and down states in striatal medium spiny neurons simultaneously recorded with spontaneous activity in fast-spiking interneurons studied in cortex-striatum-substantia nigra organotypic cultures. J. Neurosci., 18, 266-283.
34. Porter, L.L., Rizzo, E. & Hornung, J.P. (1999) Dopamine affects parvalbumin expression during cortical development in vitro. J. Neurosci., 19, 8990-9003.
35. Sadikot, A.F. & Sasseville, R. (1997) Neurogenesis in the mammalian neostriatum and nucleus accumbens: parvalbumin-immunoreactive GABAergic interneurons. J. Comp. Neurol., 389, 193-211.
36. Schlosser, B., Klausa, G., Prime, G. & Ten Bruggencate, G. (1999) Postnatal development of calretinin- and parvalbumin-positive interneurons in the rat neostriatum: an immunohistochemical study. J. Comp. Neurol., 405, 185-198.
37. Schmidt-Kastner, R., Meller, D. & Eysel, U.T. (1992) Immunohistochemical changes of neuronal calcium-binding proteins parvalbumin and calbindin-D-28k following unilateral deafferentation in the rat visual system. Exp. Neurol., 117, 230-246.
38. Sharpe, N.A. & Tepper, J.M. (1998) Postnatal development of excitatory synaptic input to the rat neostriatum: an electron microscopic study. Neuroscience, 84, 1163-1175.
39. Soghomonian, J.J. & Chesselet, M.F. (1991) Lesions of the dopaminergic nigrostriatal pathway alter preprosomatostatin messenger RNA levels in the striatum, the entopeduncular nucleus and the lateral hypothalamus of the rat. Neuroscience, 42, 49-59.
40. Szele, F.G., Dowling, J.J., Gonzales, C., Theveniau, M., Rougon, G. & Chesselet, M.F. (1994) Pattern of expression of highly polysialylated neural cell adhesion molecule in the developing and adult rat striatum. Neuroscience, 60, 133-144.
41. Tang, K.C., Low, M.J., Grandy, D.K. & Lovinger, D.M. (2001) Dopamine-dependent synaptic plasticity in striatum during in vivo development. Proc. Natl Acad. Sci. USA, 98, 1255-1260.
42. Tepper, J.M., Koos, T. & Wilson, C.J. (2004) GABAergic microcircuits in the neostriatum. Trends Neurosci., 27, 662-669.
43. Tepper, J.M., Sharpe, N.A., Koos, T.Z. & Trent, F. (1998) Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev. Neurosci., 20, 125-145.
44. Tepper, J.M. & Trent, F. (1993) In vivo studies of the postnatal development of rat neostriatal neurons. Prog. Brain Res., 99, 35-50.
45. Tigges, M. & Tigges, J. (1991) Parvalbumin immunoreactivity of the lateral geniculate nucleus in adult rhesus monkeys after monocular eye enucleation. Vis. Neurosci., 6, 375-382.
46. Uryu, K., Butler, A.K. & Chesselet, M.F. (1999) Synaptogenesis and ultrastructural localization of the polysialylated neural cell adhesion molecule in the developing striatum. J. Comp. Neurol., 405, 216-232.
47. Wang, L.Y., Gan, L., Forsythe, I.D. & Kaczmarek, L.K. (1998) Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J. Physiol. (Lond.), 509, 183-194.
48. Wilson, C.J. (1984) Passive cable properties of dendritic spines and spiny neurons. J. Neurosci., 4, 281-297.
49. Wilson, C.J., Kita, H. & Kawaguchi, Y. (1989) GABAergic interneurons, rather than spiny cell axon collaterals, are responsible for the IPSP responses to afferent stimulation in neostriatal spiny neurons. Soc. Neurosci. Abstr., 15, 907.
50. Wu, W. & Parent, A. (2000) Striatal interneurons expressing calretinin, parvalbumin or NADPH-diaphorase: a comparative study in the rat, monkey and human. Brain Res., 863, 182-191.
51. Yokoyama, S., Imoto, K., Kawamura, T., Higashida, H., Iwabe, N., Miyata, T. & Numa, S. (1989) Potassium channels from NG108-15 neuroblastomaglioma hybrid cells. Primary structure and functional expression from cDNAs. FEBS Lett., 259, 37-42.