Abstract
Of all cerebellar cells, the development of inhibitory interneurons is arguably least understood. The issue is further convoluted by the fact that knowledge of the diversity of this group of cells is rather limited. However, recent results allow to complement traditional morphological classifications with molecular and functional data that open a new perspective on cerebellar histogenesis and function. The early development of all cerebellar GABAergic interneurons is dependent on a single gene, Ptf1a. After leaving the ventricular neuroepithelium, precursors of these cells may be distinguished by their specific expression of the paired box gene, Pax2. These essentially postmitotic precursors are characterized by a so-far unique developmental plasticity. The terminal differentiation of cerebellar GABAergic interneurons is realized through an instructive mechanism thought to operate within the prospective white matter of the nascent cerebellum.
This is a preview of subscription content, log in via an institution.
References
Agbulut O, Huet A, Niederlander N, Puceat M, Menasche P, Coirault C (2007) Green fluorescent protein impairs actin-myosin interactions by binding to the actin-binding site of myosin. J Biol Chem 282:10465–10471
Aizenman CD, Huang EJ, Linden DJ (2003) Morphological correlates of intrinsic electrical excitability in neurons of the deep cerebellar nuclei. J Neurophysiol 89:1738–1747
Altman J (1972) Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granular layer. J Comp Neurol 145:465–514
Altman J (1973) Experimental reorganization of the cerebellar cortex. IV. Parallel fiber reorientation following regeneration of the external germinal layer. J Comp Neurol 149:181–192
Altman J, Bayer SA (1978) Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. J Comp Neurol 179:23–48
Altman J, Bayer SA (1997) Development of the cerebellar system in relation to its evolution, structure, and functions. CRC Press, Boca Raton
Alvarez-Otero R, Anadon R (1992) GOLGI cells of the cerebellum of the dogfish, Scyliorhinus canicula (elasmobranchs): a GOLGI and ultrastructural study. J Hirnforsch 33:321–327
Alvarez-Otero R, Perez SE, Rodriguez MA, Adrio F, Anadon R (1995) GABAergic neuronal circuits in the cerebellum of the dogfish Scyliorhinus canicula (elasmobranchs): an immunocytochemical study. Neurosci Lett 187:87–90
Ango F, Di CG, Higashiyama H, Bennett V, Wu P, Huang ZJ (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119:257–272
Ango F, Wu C, van der Want JJ, Wu P, Schachner M, Huang ZJ (2008) Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biol 6:e103
Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N (2005) Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19:1028–1033
Armengol JA, Sotelo C (1991) Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axonal tracing in ‘in vitro’ slices. Brain Res Dev Brain Res 64:95–114
Baader SL, Bergmann M, Mertz K, Fox PA, Gerdes J, Oberdick J, Schilling K (1999) The differentiation of cerebellar interneurons is independent of their mitotic history. Neuroscience 90:1243–1254
Bagnall MW, Zingg B, Sakatos A, Moghadam SH, Zeilhofer HU, du Lac S (2009) Glycinergic projection neurons of the cerebellum. J Neurosci 29:10104–10110
Baier C, Baader SL, Jankowski J, Gieselmann V, Schilling K, Rauch U, Kappler J (2007) Hyaluronan is organized into fiber-like structures along migratory pathways in the developing mouse cerebellum. Matrix Biol 26:348–358
Bäuerle J, Grüsser-Cornehls U (1997) Differential number of glycine- and GABA-immunopositive neurons and terminals in the deep cerebellar nuclei of normal and Purkinje cell degeneration mutant mice. J Comp Neurol 382:443–458
Baumel Y, Jacobson GA, Cohen D (2009) Implications of functional anatomy on information processing in the deep cerebellar nuclei. Front Cell Neurosci 3(14):14
Bengtsson F, Svensson P, Hesslow G (2004) Feedback control of Purkinje cell activity by the cerebello-olivary pathway. Eur J Neurosci 20:2999–3005
Berglund EO, Murai KK, Fredette B, Sekerkova G, Marturano B, Weber L, Mugnaini E, Ranscht B (1999) Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression. Neuron 24:739–750
Boukhtouche F, Janmaat S, Vodjdani G, Gautheron V, Mallet J, Dusart I, Mariani J (2006) Retinoid-related orphan receptor alpha controls the early steps of Purkinje cell dendritic differentiation. J Neurosci 26:1531–1538
Braun N, Papadopoulos T, Müller-Hermelink HK (1988) Cell cycle dependent distribution of the proliferation-associated Ki-67 antigen in human embryonic lung cells. Virchows Arch B Cell Pathol Incl Mol Pathol 56:25–33
Cameron DB, Kasai K, Jiang Y, Hu T, Saeki Y, Komuro H (2009) Four distinct phases of basket/stellate cell migration after entering their final destination (the molecular layer) in the developing cerebellum. Dev Biol 332:309–324
Carletti B, Grimaldi P, Magrassi L, Rossi F (2002) Specification of cerebellar progenitors after heterotopic-heterochronic transplantation to the embryonic CNS in vivo and in vitro. J Neurosci 22:7132–7146
Cesa R, Morando L, Strata P (2008) Transmitter-receptor mismatch in GABAergic synapses in the absence of activity. Proc Natl Acad Sci USA 105:18988–18993
Chalphin AV, Saha MS (2010) The specification of glycinergic neurons and the role of glycinergic transmission in development. Front Mol Neurosci 3(11):11
Chan-Palay V (1972) Arrested granule cells and their synapses with mossy fibers in the molecular layer of the cerebellar cortex. Z Anat Entwicklungsgesch 139:11–20
Chen S, Hillman DE (1993) Colocalization of neurotransmitters in the deep cerebellar nuclei. J Neurocytol 22:81–91
Corfas G, Rosen KM, Aratake H, Krauss R, Fischbach GD (1995) Differential expression of ARIA isoforms in the rat brain. Neuron 14:103–115
Crook J, Hendrickson A, Robinson FR (2006) Co-localization of glycine and gaba immunoreactivity in interneurons in Macaca monkey cerebellar cortex. Neuroscience 141:1951–1959
Das GD, Nornes HO (1972) Neurogenesis in the cerebellum of the rat: an autoradiographic study. Z Anat Entwicklungsgesch 138:155–165
Dehay C, Kennedy H (2007) Cell-cycle control and cortical development. Nat Rev Neurosci 8:438–450
Desai AR, McConnell SK (2000) Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127:2863–2872
Dessaud E, Yang LL, Hill K, Cox B, Ulloa F, Ribeiro A, Mynett A, Novitch BG, Briscoe J (2007) Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450:717–720
Dong PD, Provost E, Leach SD, Stainier DY (2008) Graded levels of Ptf1a differentially regulate endocrine and exocrine fates in the developing pancreas. Genes Dev 22:1445–1450
Eccles JC (1969) The development of the cerebellum of vertebrates in relation to the control of movement. Naturwissenschaften 56:525–534
Eccles JC, Taborikova H, Tsukahara N (1970) Responses of the granule cells of the selachian cerebellum (Mustelus canis). Brain Res 17:87–102
Ellison DW (2010) Childhood medulloblastoma: novel approaches to the classification of a heterogeneous disease. Acta Neuropathol 120:305–316
Englund C, Kowalczyk T, Daza RA, Dagan A, Lau C, Rose MF, Hevner RF (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci 26:9184–9195
Farrant M, Brickley SG (2003) Properties of GABA(A) receptor-mediated transmission at newly formed Golgi-granule cell synapses in the cerebellum. Neuropharmacology 44:181–189
Fink AJ, Englund C, Daza RA, Pham D, Lau C, Nivison M, Kowalczyk T, Hevner RF (2006) Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J Neurosci 26:3066–3076
Fritschy JM, Panzanelli P, Kralic JE, Vogt KE, Sassoe-Pognetto M (2006) Differential dependence of axo-dendritic and axo-somatic GABAergic synapses on GABAA receptors containing the alpha1 subunit in Purkinje cells. J Neurosci 26:3245–3255
Fukuda A, Kawaguchi Y, Furuyama K, Kodama S, Horiguchi M, Kuhara T, Kawaguchi M, Terao M, Doi R, Wright CV, Hoshino M, Chiba T, Uemoto S (2008) Reduction of Ptf1a gene dosage causes pancreatic hypoplasia and diabetes in mice. Diabetes 57:2421–2431
Geurts FJ, Timmermans J, Shigemoto R, De Schutter E (2001) Morphological and neurochemical differentiation of large granular layer interneurons in the adult rat cerebellum. Neuroscience 104:499–512
Glassmann A, Topka S, Wang-Eckardt L, Anders S, Weisheit G, Endl E, Zimmer A, Schilling K (2008) Basic molecular fingerprinting of immature cerebellar cortical inhibitory interneurons and their precursors. Neuroscience 159:69–82
Glickstein SB, Monaghan JA, Koeller HB, Jones TK, Ross ME (2009) Cyclin D2 is critical for intermediate progenitor cell proliferation in the embryonic cortex. J Neurosci 29:9614–9624
Gold DA, Gent PM, Hamilton BA (2006) RORalpha in genetic control of cerebellum development: 50 staggering years. Brain Res 1140:19–25
Hallonet MER, Le Douarin NM (1993) Tracing neuroepithelial cells of the mesencephalic and metencephalic alar plates during cerebellar ontogeny in quail-chick chimaeras. Eur J Neurosci 5:1145–1155
Hamilton BA, Frankel WN, Kerrebrock AW, Hawkins TL, FitzHugh W, Kusumi K, Russell LB, Mueller KL, van Berkel V, Birren BW, Kruglyak L, Lander ES (1996) Disruption of the nuclear hormone receptor RORα in staggerer mice. Nature 379:736–739
Hamori J, Somogyi J (1982) Presynaptic dendrites and perikarya in deafferented cerebellar cortex. Proc Natl Acad Sci USA 79:5093–5096
Hamori J, Somogyi J (1983) Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J Comp Neurol 220:365–367
Hausmann B, Mangold U, Sievers J, Berry M (1985) Derivation of cerebellar Golgi neurons from the external granular layer: evidence from explantation of external granule cells in vivo. J Comp Neurol 232:511–522
Hedstrom KL, Xu X, Ogawa Y, Frischknecht R, Seidenbecher CI, Shrager P, Rasband MN (2007) Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J Cell Biol 178:875–886
Hekmat A, Künemund V, Fischer G, Schachner M (1989) Small inhibitory cerebellar interneurons grow in a perpendicular orientation to granule cell neurites in culture. Neuron 2:1113–1122
Hoshino M, Nakamura S, Mori K, Kawauchi T, Terao M, Nishimura YV, Fukuda A, Fuse T, Matsuo N, Sone M, Watanabe M, Bito H, Terashima T, Wright CV, Kawaguchi Y, Nakao K, Nabeshima Y (2005) Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47:201–213
Huang M, Huang T, Xiang Y, Xie Z, Chen Y, Yan R, Xu J, Cheng L (2008) Ptf1a, Lbx1 and Pax2 coordinate glycinergic and peptidergic transmitter phenotypes in dorsal spinal inhibitory neurons. Dev Biol 322:394–405
Huang X, Liu J, Ketova T, Fleming JT, Grover VK, Cooper MK, Litingtung Y, Chiang C (2010) Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development. Proc Natl Acad Sci USA 107:8422–8427
Huard JMT, Forster CC, Carter ML, Sicinski P, Ross ME (1999) Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 126:1927–1935
Jankowski J, Holst MI, Liebig C, Oberdick J, Baader SL (2004) Engrailed-2 negatively regulates the onset of perinatal Purkinje cell differentiation. J Comp Neurol 472:87–99
Jenkins SM, Bennett V (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 155:739–746
Kornguth SE, Anderson JW, Scott G (1968) The development of synaptic contacts in the cerebellum of Macaca mulatta. J Comp Neurol 132:531–546
Koscheck T, Weyer A, Schilling RL, Schilling K (2003) Morphological development and neurochemical differentiation of cerebellar inhibitory interneurons in microexplant cultures. Neuroscience 116:973–984
Laine J, Axelrad H (1994) The candelabrum cell: a new interneuron in the cerebellar cortex. J Comp Neurol 339:159–173
Laine J, Axelrad H (2002) Extending the cerebellar Lugaro cell class. Neuroscience 115:363–374
Laine J, Axelrad H, Rahbi N (1992) Intermediate cells of Lugaro are present in the immature rat cerebellar cortex at an earlier stage than previously thought. Neurosci Lett 145:225–228
Landis DM, Sidman RL (1978) Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice. J Comp Neurol 179:831–863
Larramendi LMH (1969) Analysis of synaptogenesis in the cerebellum of the mouse. In: Llinás R (ed) Neurobiology of cerebellar evolution and development. American Medical Association, Chicago, pp 803–843
Larramendi LMH, Fickenscher L, Lemkey-Johnston N (1967) Synaptic vesicles of inhibitory and excitatory terminals in the cerebellum. Science 156:967–969
Larsell O (1967) The comparative anatomy and histology of the cerebellum from Myxinoids through birds. The University of Minnesota Press, Minneapolis
Laurie DJ, Wisden W, Seeburg PH (1992) The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain: III. Embryonic and postnatal development. J Neurosci 12:4151–4172
Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176
Lemkey-Johnston N, Larramendi LMH (1968a) Morphological characteristics of mouse stellate and basket cells and their neuroglial envelope: an electron microscopic study. J Comp Neurol 134:39–72
Lemkey-Johnston N, Larramendi LMH (1968b) Types and distribution of synapses upon basket and stellate cells of the mouse cerebellum. J Comp Neurol 134:73–112
Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK (2008) The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol 18:28–35
Leto K, Carletti B, Williams IM, Magrassi L, Rossi F (2006) Different types of cerebellar GABAergic interneurons originate from a common pool of multipotent progenitor cells. J Neurosci 26:11682–11694
Leto K, Bartolini A, Yanagawa Y, Obata K, Magrassi L, Schilling K, Rossi F (2009) Laminar fate and phenotype specification of cerebellar GABAergic interneurons. J Neurosci 29:7079–7091
Leto K, Bartolini A, Rossi F (2010) The prospective white matter: an atypical neurogenic niche in the developing cerebellum. Arch Ital Biol 148:137–146
Llinas R, Hillman DE (1969) Physiological and morphological organization of the cerebellar circuits in various vertebrates. In: Llinás R (ed) Neurobiology of cerebellar evolution and development. American Medical Association, Chicago, pp 43–73
Magyar-Lehmann S, Frei T, Schachner M (1995a) Fasciculation of granule cell neurites is responsible for the perpendicular orientation of small inhibitory interneurons in mouse cerebellar microexplant cultures in vitro. Eur J Neurosci 7:1460–1471
Magyar-Lehmann S, Suter CS, Stahel W, Schachner M (1995b) Behavior of small inhibitory interneurons in early postnatal mouse cerebellar microexplant cultures. Eur J Neurosci 7:1449–1459
Marc C, Clavel M-C, Rabié A (1986) Non-phosphorylated and phosphorylated neurofilaments in the cerebellum of the rat: an immunocytochemical study using monoclonal antibodies. Development in normal and thyroid-deficient animals. Brain Res 26:249–260
Mariani J, Crépel F, Mikoshiba K, Changeux J-P, Sotelo C (1977) Anatomical, physiological, and biochemical studies of the cerebellum from reeler mutant mouse. Philos Trans R Soc Lond B Biol Sci 281:1–28
Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41:281–294
McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282–285
Meguro R, Ohishi H, Hoshino K, Hicks TP, Norita M (1999) Metabotropic glutamate receptor 2/3 immunoreactivity in the developing rat cerebellar cortex. J Comp Neurol 410:243–255
Meredith DM, Masui T, Swift GH, MacDonald RJ, Johnson JE (2009) Multiple transcriptional mechanisms control Ptf1a levels during neural development including autoregulation by the PTF1-J complex. J Neurosci 29:11139–11148
Mertz K, Koscheck T, Schilling K (2000) Brain derived neurotrophic factor modulates dendritic morphology of cerebellar basket and stellate cells. Neuroscience 97:303–310
Midtgaard J (1992) Stellate cell inhibition of Purkinje cells in the turtle cerebellum in vitro. J Physiol 457:355–367
Mizuhara E, Minaki Y, Nakatani T, Kumai M, Inoue T, Muguruma K, Sasai Y, Ono Y (2010) Purkinje cells originate from cerebellar ventricular zone progenitors positive for Neph3 and E-cadherin. Dev Biol 338:202–214
Nakatsuji N, Nagata I (1989) Paradoxical perpendicular contact guidance displayed by mouse cerebellar granule cell neurons in vitro. Development 106:441–447
Napieralski JA, Eisenman LM (1993) Developmental analysis of the external granule cell layer in the meander tail mutant mouse: do cerebellar microneurons have independent progenitors? Dev Dyn 197:244–254
Palay SL, Chan-Palay V (1974) Cerebellar cortex. Cytology and organization. Springer, Berlin
Pascual M, Abasolo I, Mingorance-Le Meur A, Martinez A, Del Rio JA, Wright CV, Real FX, Soriano E (2007) Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc Natl Acad Sci USA 104:5193–5198
Patrizi A, Scelfo B, Viltono L, Briatore F, Fukaya M, Watanabe M, Strata P, Varoqueaux F, Brose N, Fritschy JM, Sassoe-Pognetto M (2008) Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors. Proc Natl Acad Sci USA 105:13151–13156
Paula-Barbosa MM, Tavares MA, Ruela C, Barroca H (1983) The distribution of stellate cell descending axons in the rat cerebellum: a Golgi and a combined Golgi-electron microscopical study. J Anat 137:757–764
Pietsch T, Taylor MD, Rutka JT (2004) Molecular pathogenesis of childhood brain tumors. J Neurooncol 70:203–215
Pouzat C, Hestrin S (1997) Developmental regulation of basket/stellate cell --> Purkinje cell synapses in the cerebellum. J Neurosci 17:9104–9112
Qiu CH, Shimokawa N, Iwasaki T, Parhar IS, Koibuchi N (2007) Alteration of cerebellar neurotropin messenger ribonucleic acids and the lack of thyroid hormone receptor augmentation by staggerer-type retinoic acid receptor-related orphan receptor-alpha mutation. Endocrinology 148:1745–1753
Rakic P (1972) Extrinsic cytological determinants of basket and stellate cell dendritic pattern in the cerebellar molecular layer. J Comp Neurol 146:335–354
Rakic P (1973) Kinetics and proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons. J Comp Neurol 147:523–546
Ramon y Cajal S (1909) Histologie du système nerveux de l’homme et des vertébrés. II. A. Maloine, Paris
Richardson CA, Leitch B (2002) Cerebellar Golgi, Purkinje, and basket cells have reduced gamma-aminobutyric acid immunoreactivity in stargazer mutant mice. J Comp Neurol 453:85–99
Rieff HI, Corfas G (2006) ErbB receptor signaling regulates dendrite formation in mouse cerebellar granule cells in vivo. Eur J Neurosci 23:2225–2229
Rio C, Rieff HI, Qi P, Khurana TS, Corfas G (1997) Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19:39–50
Rodolosse A, Chalaux E, Adell T, Hagege H, Skoudy A, Real FX (2004) PTF1alpha/p48 transcription factor couples proliferation and differentiation in the exocrine pancreas [corrected]. Gastroenterology 127:937–949
Rouaux C, Arlotta P (2010) Fezf2 directs the differentiation of corticofugal neurons from striatal progenitors in vivo. Nat Neurosci 13:1345–1347
Schilling K, Oberdick J (2010) The treasury of the commons: making use of public gene expression resources to better characterize the molecular diversity of inhibitory interneurons in the cerebellar cortex. Cerebellum 8:477–489
Schilling K, Dickinson MH, Connor JA, Morgan JI (1991) Electrical activity in cerebellar cultures determines Purkinje cell dendritic growth patterns. Neuron 7:891–902
Schuller U, Heine VM, Mao J, Kho AT, Dillon AK, Han YG, Huillard E, Sun T, Ligon AH, Qian Y, Ma Q, varez-Buylla A, McMahon AP, Rowitch DH, Ligon KL (2008) Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14:123–134
Sekerkova G, Ilijic E, Mugnaini E (2004) Time of origin of unipolar brush cells in the rat cerebellum as observed by prenatal bromodeoxyuridine labeling. Neuroscience 127:845–858
Sellick GS, Barker KT, Stolte-Dijkstra I, Fleischmann C, Coleman RJ, Garrett C, Gloyn AL, Edghill EL, Hattersley AT, Wellauer PK, Goodwin G, Houlston RS (2004) Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat Genet 36:1301–1305
Shimono T, Nosaka S, Sasaki K (1976) Electrophysiological study on the postnatal development of neuronal mechanisms in the rat cerebellar cortex. Brain Res 108:279–294
Sidman RL, Lane PW, Dickie MM (1962) Staggerer, a new mutation in the mouse affecting the cerebellum. Science 137:610–612
Simat M, Ambrosetti L, Lardi-Studler B, Fritschy JM (2007a) GABAergic synaptogenesis marks the onset of differentiation of basket and stellate cells in mouse cerebellum. Eur J Neurosci 26:2239–2256
Simat M, Parpan F, Fritschy JM (2007b) Heterogeneity of glycinergic and gabaergic interneurons in the granule cell layer of mouse cerebellum. J Comp Neurol 500:71–83
Sotelo C (1977) Formation of presynaptic dendrites in the rat cerebellum following neonatal X-irradiation. Neuroscience 2:275–283
Spacek J, Parizek J, Lieberman AR (1973) Golgi cells, granule cells and synaptic glomeruli in the molecular layer of the rabbit cerebellar cortex. J Neurocytol 2:407–428
Sultan F, Bower JM (1998) Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal component analysis. J Comp Neurol 393:353–373
Swanson DJ, Steshina EY, Wakenight P, Aldinger KA, Goldowitz D, Millen KJ, Chizhikov VV (2010) Phenotypic and genetic analysis of the cerebellar mutant tmgc26, a new ENU-induced ROR-alpha allele. Eur J Neurosci 32:707–716
Takayama C, Inoue Y (2004a) Extrasynaptic localization of GABA in the developing mouse cerebellum. Neurosci Res 50:447–458
Takayama C, Inoue Y (2004b) Morphological development and maturation of the GABAergic synapses in the mouse cerebellar granular layer. Brain Res Dev Brain Res 150:177–190
Takayama C, Inoue Y (2004c) Transient expression of GABAA receptor alpha2 and alpha3 subunits in differentiating cerebellar neurons. Brain Res Dev Brain Res 148:169–177
Takayama C, Inoue Y (2005) Developmental expression of GABA transporter-1 and 3 during formation of the GABAergic synapses in the mouse cerebellar cortex. Brain Res Dev Brain Res 158:41–49
Tanaka I, Ezure K (2004) Overall distribution of GLYT2 mRNA-containing versus GAD67 mRNA-containing neurons and colocalization of both mRNAs in midbrain, pons, and cerebellum in rats. Neurosci Res 49:165–178
Tidcombe H, Jackson-Fisher A, Mathers K, Stern DF, Gassmann M, Golding JP (2003) Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc Natl Acad Sci USA 100:8281–8286
Uusisaari M, Knopfel T (2010) GlyT2+ neurons in the lateral cerebellar nucleus. Cerebellum 9:42–55
Wall MJ, Usowicz MM (1997) Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9:533–548
Weisheit G, Gliem M, Endl E, Pfeffer PL, Busslinger M, Schilling K (2006) Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24:466–478
Wuenschell CW, Tobin AJ (1988) The abnormal cerebellar organization of weaver and reeler mice does not affect the cellular distribution of three neuronal mRNAs. Neuron 1:805–815
Yamanaka H, Yanagawa Y, Obata K (2004) Development of stellate and basket cells and their apoptosis in mouse cerebellar cortex. Neurosci Res 50:13–22
Zeilhofer HU, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bosl MR, Fritschy JM (2005) Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 482:123–141
Zhang L, Goldman JE (1996) Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 16:47–54
Acknowledgments
I am indebted to the members of the laboratories of Ferdinado Rossi, John Oberdick, Torsten Pietsch, Stephan Baader, and my own lab for many inspiring and thought-provoking discussions. Any imperfections that remain are my responsibility entirely.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media Dordrecht
About this entry
Cite this entry
Schilling, K. (2013). Specification and Development of GABAergic Interneurons. In: Manto, M., Schmahmann, J.D., Rossi, F., Gruol, D.L., Koibuchi, N. (eds) Handbook of the Cerebellum and Cerebellar Disorders. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1333-8_11
Download citation
DOI: https://doi.org/10.1007/978-94-007-1333-8_11
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-1332-1
Online ISBN: 978-94-007-1333-8
eBook Packages: Biomedical and Life SciencesReference Module Biomedical and Life Sciences