A novel inhibitory nucleo-cortical circuit controls cerebellar Golgi cell activity

eLife

Volumn 4, Issue MAY, 2015, Pages

  Ankri, Lea ^a   Husson, Zoé ^b,c   Pietrajtis, Katarzyna ^b,c   Proville, Rémi ^b,c   Léna, Clément ^b,c   Yarom, Yosef ^a   Dieudonné, Stéphane ^b,c   Uusisaari, Marylka Yoe ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b PSL RESEARCH UNIVERSITY   (France)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CHANNEL RHODOPSIN; GLYCINE RECEPTOR; MEMBRANE PROTEIN; NEUROTRANSMITTER; UNCLASSIFIED DRUG; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM CORTEX; CONTROLLED STUDY; ELECTRICAL POTENTIAL PARAMETERS; FEMALE; GAP JUNCTION; GOLGI COMPLEX; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LATENT PERIOD; MALE; MEMBRANE STEADY POTENTIAL; MOTOR COORDINATION; MOUSE; NERVE CELL; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE FIBER; NONHUMAN; NUCLEO CORTICAL CIRCUIT; OPTOGENETICS; PHENOTYPE; PURKINJE CELL; SYNAPSE; ANIMAL; BIOLOGICAL MODEL; CEREBELLUM NUCLEUS; CYTOLOGY; INTERNEURON; NERVE TRACT; PHYSIOLOGY;

ANIMALS; CEREBELLAR CORTEX; CEREBELLAR NUCLEI; IMMUNOHISTOCHEMISTRY; INTERNEURONS; LUMINESCENT PROTEINS; MICE; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; OPTOGENETICS;

EID: 84930637272     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06262     Document Type: Article

References (96)

1. Andersen BB, Korbo L, Pakkenberg B. A quantitative study of the human cerebellum with unbiased stereological techniques. J. Comp. Neurol. 326: 549-60, 1992. doi: 10.1002/cne.903260405.
2. Angaut P, Cicirata F, Serapide F. Topographic organizationof the cerebellothalamic projections in the rat. Anautoradiographic study. Neurosci. 15:389-401, 1985. doi:10.1016/0306- 4522(85)90221-0.
3. Ankri L, Yarom Y, Uusisaari M. Slice It Hot: Acute Adult Brain Slicing in Physiological Temperature. JoVE92, 2014. doi:10.3791/520688.
4. Aoki S, Sato Y, Yanagihara D. Effect of inactivation of the intermediate cerebellum on overground locomotion in the rat: A comparative study of the anterior and posterior lobes. Neurosci. lett. 576: 22-27, 2014.doi:10.1016/j.neulet.2014.05.027.
5. Apps R, Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat. Rev. Neurosci.6: 297-311, 2005. doi: 10.1038/nrn1646.
6. Apps R, Hawkes R. Cerebellar cortical organization: a one-map hypothesis. Nat. Rev. Neurosci.10: 670-681, 2009. doi: 10.1038/nrn2698.
7. Asanuma C, Thach WT, Jones EG. Nucleus interpositus projection to spinal interneurons in monkeys. Brain research191: 245-248, 1980. doi:10.1016/0006-8993(80)90327-3.
8. Aubrey K, Rossi F, Ruivo R, Alboni S, Bellenchi G, Goff A, Gasnier B, Supplisson S. The Transporters GlyT2 and VIAAT Cooperate to Determine the Vesicular Glycinergic Phenotype. J Neurosci.27: 6273-6281, 2007. doi: 10.1523/JNEUROSCI.1024-07.2007.
9. Bagnall MW, Zingg B, Sakatos A, Moghadam SH, Zeilhofer HU, du Lac S. Glycinergic projection neurons of the cerebellum. J. Neurosci.29: 10104-10110, 2009. doi: 10.1523/JNEUROSCI.2087-09.2009.
10. Batini C, Buisseret-Delmas C, Compoint C, Daniel H. The GABAergic neurones of the cerebellar nuclei in the rat: projections to the cerebellar cortex. Neurosci. lett, 99: 251-256, 1989. doi: 10.1016/0304-3940(89)90455-2.
11. Batini C, Compoint C, Buisseret-Delmas C, Daniel H, Guegan M. Cerebellar nuclei and the nucleocortical projections in the rat: Retrograde tracing coupled to GABA and glutamate immunohistochemistry. J. Comp. Neurol.315: 74-84, 1992. doi: 10.1002/cne.903150106.
12. Bazzigaluppi P, Ruigrok T, Saisan P, De Zeeuw C, Jeu M. Properties of the Nucleo-Olivary Pathway: An In Vivo Whole-Cell Patch Clamp Study. PLoS ONE7, 2012. doi: 10.1371/journal.pone.0046360.
13. Bengtsson F, Hesslow G. Cerebellar control of the inferior olive. The Cerebellum, 5:7-14, 2006.
14. Bengtsson F, Jörntell H. Ketamine and xylazine depress sensory-evoked parallel fiber and climbing fiber responses. J neurophys, 98(3): 1697-1705, 2007. doi: 10.1152/jn.00057.2007.
15. Buisseret-Delmas C. Sagittal organization of the olivocerebellonuclear pathway inthe rat. I. Connections with the nucleus fastigii and the nucleus vestibularis lateralis. Neuroscience research, 5: 475-493, 1988. doi: 10.1016/0168-0102(88)90038-7.
16. Chadderton P, Margrie TW, Häusser M. Integration of quanta in cerebellar granule cells during sensory processing. Nature, 428: 856-860, 2004. doi: 10.1038/nature02442.
17. Chan-Palay V. The cerebellar dentate nucleus, Springer-Verlag, Berlin, 1977. doi: 10.1007/978- 3-642-66498-4_1.
18. Chan-Palay V, Palay S, Wu J. Gamma-aminobutyric acid pathways in the cerebellum studied by retrograde and anterograde transport of glutamic acid decarboxylase antibody after in vivo injections. Anat Embryol157: 114, 1979.
19. Chaumont J, Guyon N, Valera A, Dugué G, Popa D, Marcaggi P, Gautheron V, Reibel-Foisset S, Dieudonné S, Stephan A, Barrot M, Cassel J-C, Dupont J-L, Doussau F, Poulain B, Selimi F, Léna C, Isope P. Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge. Proc. Natl. Acad. Sci. U.S.A.110: 16223-16228, 2013. doi: 10.1073/pnas.1302310110.
20. Chen X, Kovalchuk Y, Adelsberger H, Henning H, Sausbier M, Wietzorrek G, Ruth P, Yarom Y, Konnerth A. Disruption of the olivo-cerebellar circuit by Purkinje neuron-specific ablation of BK channels. Proc. Natl. Acad. Sci. U.S.A.107: 12323-12328, 2010. doi: 10.1073/pnas.1001745107.
21. Clopath C, Badura A, De Zeeuw C, Brunel N. A Cerebellar Learning Model of Vestibulo-Ocular Reflex Adaptation in Wild-Type and Mutant Mice. J. Neurosci34: 7203-7215, 2014. doi: 10.1523/JNEUROSCI.2791-13.2014.
22. Coesmans M, Weber JT, De Zeeuw C, Hansel C. Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron, 44(4): 691-700, 2004. doi: 10.1016/j.neuron.2004.10.031.
23. D'Angelo E, De Zeeuw C. Timing and plasticity in the cerebellum: focus on the granular layer. Trends in neurosciences, 32:30-40, 2009. doi: 10.1016/j.tins.2008.09.007.
24. Dean P, Porrill J. The cerebellum as an adaptive filter: a general model?. Functional neurology, 25:173-180, 2010.
25. De Zeeuw C, Berrebi AS. Postsynaptic targets of Purkinje cell terminals in the cerebellar and ves- tibular nuclei of the rat. European Journal of Neuroscience 7: 2322-33, 1995. doi:10.1111/j.1460- 9568.1995.tb00653.x.
26. De Zeeuw C, Gerrits N, Voogd J, Leonard C, Simpson J. The rostral dorsal cap and ventrolateral outgrowth of the rabbit inferior olive receive a GABAergic input from dorsal group Y and the ven- tral dentate nucleus. J. Comp. Neurol.341: 420-432, 1994.
27. Dietrichs E, Walberg F. The cerebellar corticonuclear and nucleocortical projections in the cat as studied with anterograde and retrograde transport of horseradish peroxidase. I. The paramedian lobule. Anat. Embryol.158: 13-39, 1979.
28. Dieudonné S. Glycinergic synaptic currents in Golgi cells of the rat cerebellum. Proceedings of the National Academy of Sciences92: 1441-1445, 1995. doi: 10.1073/pnas.92.5.1441.
29. Dieudonné S. Submillisecond kinetics and low efficacy of parallel fibre-Golgi cell synaptic currents in the rat cerebellum. J phys, 510: 845-866 ,1998. doi: 10.1111/j.1469- 7793.1998.845bj.x.
30. Dijck G, Hulle M, Heiney S, Blazquez P, Meng H, Angelaki D, Arenz A, Margrie T, Mostofi A, Edgley S, Bengtsson F, Ekerot C-F, Jörntell H, Dalley J, Holtzman T. Probabilistic Identification of Cerebellar Cortical Neurones across Species. PLoS ONE8, 2013. doi: 10.1371/journal.pone.0057669.
31. Dugué G, Brunel N, Hakim V, Schwartz E, Chat M, Lévesque M, Courtemanche R, Léna C, Dieudonné S. Electrical Coupling Mediates Tunable Low-Frequency Oscillations and Resonance in the Cerebellar Golgi Cell Network. Neuron61: 126-139, 2009. doi: 10.1016/j.neuron.2008.11.028.
32. Dumoulin A, Triller A, Dieudonné S. IPSC kinetics at identified GABAergic and mixed GABAergic and glycinergic synapses onto cerebellar Golgi cells. J. Neurosci, 21: 6045-6057, 2001.
33. Fredette B, Mugnaini E. The GABAergic cerebello-olivary projection in the rat. Anat. Embryol. 184: 225-43, 1991.
34. Gao H, Solages C, Lena C. Tetrode recordings in the cerebellar cortex. J. Physiol. Paris106: 128- 36, 2011. doi: 10.1016/j.jphysparis.2011.10.005.
35. Gauck V, Jaeger D. The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci, 20: 3006-3016, 2000.
36. Gould BB, Graybiel AM. Afferents to the cerebellar cortex in the cat: evidence for an intrinsic pathway leading from the deep nuclei to the cortex. Brain research,100: 601-611, 2004. doi:10.1016/0006-8993(76)90869-6.
37. Gould B. The organization of afferents to the cerebellar cortex in thecat: Projections from the deep cerebellar nuclei. J. Comp. Neurol.184: 27-42, 1979. doi: 10.1002/cne.901840103.
38. Haines DE, Manto MU. The discovery and definitive proof of cerebellar nucleocortical projections 1976. Cerebellum, 8:1-18, 2009. doi: 10.1007/s12311-008-0054-8.
39. Haines D, Pearson J. Cerebellar corticonuclear - nucleocortical topography: A study of the tree shrew (Tupaia) paraflocculus. J. Comp. Neurol.187: 745-758, 1979. doi: 10.1002/cne.901870407.
40. Haines D. Evidence of intracerebellar collateralization of nucleocortical cell processes in a prosimian primate (Galago): A fluorescence retrograde study. J. Comp. Neurol.275: 441-451, 1988. doi: 10.1002/cne.902750308.
41. Hansel C, Linden DJ. Long-term depression of the cerebellar climbing fiber-Purkinje neuron synapse. Neuron 26: 473-482, 2000. doi:10.1016/S0896-6273(00)81179-4
42. Heck DH, Thach WT. On-beam synchrony in the cerebellum as the mechanism for the timing and coordination of movement. PNAS, 104:7658-7663, 2007. doi: 10.1073/pnas.0609966104
43. Holtzman T, Rajapaksa T, Mostofi A, Edgley SA.Different responses of rat cerebellar Purkinje cells and Golgi cells evoked by widespread convergent sensory inputs.J. Physiol574: 491-507, 2006. doi: 10.1113/jphysiol.2006.108282
44. Houck BD, Person AL. Cerebellar premotor output neurons collateralize to innervatethe cere- bellar cortex. J Comp Neurol, accepted article, 2015. doi: 10.1002/cne.23787.
45. Houck B, Person A. Cerebellar Loops: A Review of the Nucleocortical Pathway. Cerebellum13: 378-385, 2013. doi: 10.1007/s12311-013-0543-2
46. Huang S, Uusisaari M. Physiological temperature during brain slicing enhances the quality of acute slice preparations. Front Cell Neurosci 7: 48, 2013. 10.3389/fncel.2013.00048
47. Hull C, Chu Y, Thanawala M, Regehr W. Hyperpolarization Induces a Long-Term Increase in the Spontaneous Firing Rate ofCerebellar Golgi Cells. J Neurosci33: 5895-5902, 2013. doi: 0.1523/JNEUROSCI.4052-12.2013
48. Hull C, Regehr W. Identification of an Inhibitory Circuit that Regulates Cerebellar Golgi Cell Activ- ity. Neuron73, 2011. doi: 10.1016/j.neuron.2011.10.030
49. Husson Z, Rousseau C, Broll I, Zeilhofer H, Dieudonné S. Differential GABAergic and Glyciner- gic Inputs of Inhibitory Interneurons and Purkinje Cells to Principal Cells of the Cerebellar Nuclei. J Neurosci34: 9418-9431, 2014. doi: 10.1523/JNEUROSCI.0401-14.2014
50. Hámori J, Somogyi J. Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J Comp Neurol220:365-377, 1983. doi: 10.1002/cne.902200402.
51. Hámori J, Mezey É, Szentágothai J. Electron microscopic identification of cerebellar nucleo- cortical mossy terminals in the rat. Exp Brain Res44, 1980. doi: 10.1007/BF00238753
52. Hámori J, Takács J. Two types of GABA-containing axon terminals in cerebellar glomeruli of cat: An immunogold-EM study. Exp Brain Res74, 1988.
53. Ito M. Movement and thought: identical control mechanisms by the cerebellum. Trends Neurosci. 16: 448-50; discussion 453-4, 1993. doi:10.1016/0166-2236(93)90073-U
54. Jacobson G, Rokni D, Yarom Y. A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci.31: 617-25, 2008. doi:10.1016/j.tins.2008.09.005
55. Jakab RL, Hamori J. Quantitative morphology and synaptology of cerebellar glomeruli in the rat. Anat embryol 179: 81-88. doi: 10.1007/BF00305102
56. Kanichay R, Silver R.Synaptic and cellular properties of the feedforward inhibitorycircuit with- in the input layer of the cerebellar cortex. J Neurosci 28: 8955-67, 2008. doi: 10.1523/JNEUROSCI.5469-07.2008
57. Korbo L, Andersen BB, Ladefoged O, Møller A. Total numbers of various cell types in rat cere- bellar cortex estimated using an unbiased stereological method. Brain Res.609: 262-8, 1993. doi:10.1016/0006-8993(93)90881-M
58. Lefler Y, Yarom Y, Uusisaari M. Cerebellar Inhibitory Input to the Inferior Olive Decreases Elec- trical Coupling and Blocks Subthreshold Oscillations. Neuron81, 2014. doi: 10.1016/j.neuron.2014.02.032
59. Legendre A, Courville J. Cerebellar nucleocortical projection with a survey of factorsaffecting the transport of radioactive tracers. J. Comp. Neurol.252: 392-403, 1986. doi: 10.1002/cne.902520308
60. Leiner HC, Leiner AL, Dow RS. Cognitive and language functions of the human cerebellum. Trends Neurosci16: 444-447, 1993. doi:10.1016/0166-2236(93)90072-T
61. Longley M, Yeo C. Distribution of neural plasticity in cerebellum-dependent motor learning. Prog. Brain Res.210: 79-101, 2014. doi: 10.1016/B978-0-444-63356-9.00004-2
62. Medina JF, Lisberger SG. Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci 11, 1185 - 1192, 2008. doi:10.1038/nn.2197
63. Najac M, Raman IM. Integration of Purkinje Cell Inhibition by Cerebellar Nucleo-Olivary Neu- rons. J. Neurosci. 35: 544-9, 2015. doi: 10.1523/JNEUROSCI.3583-14.2015.
64. Ottersen OP, Storm-Mathisen J, Somogyi P. Colocalization of glycine-like and GABA-like im- munoreactivities in Golgi cell terminals in the rat cerebellum:a postembedding light and electron microscopic study. Brain Res.450: 342-53, 1988.
65. Payne J. The cerebellar nucleo-corticalprojection in the rat studied by the retrograde fluorescent double-labelling method. Brain Res271: 141144, 1983. doi: 10.1016/0006-8993(83)91374-4
66. Pedroarena CM, Schwarz C. Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons J neurophysiol89: 704-15, 2003. doi: 10.1152/jn.00558.2002
67. Person AL, Raman IM. Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature 481: 502-5, 2012. doi: 10.1038/nature10732
68. Pietrajtis K, Dieudonné S. Golgi Neurons. In: Handbook of the cerebellum and cerebellar disor- ders, Springer, 2013. doi: 10.1007/978-94-007-1333-8_34.
69. Pijpers A, Voogd J, Ruigrok T. Topography of olivo-cortico-nuclear modules in the intermediate cerebellum of the rat. J Comp. Neurol.492: 193-213, 2005. doi: 10.1002/cne.20707.
70. Provini L, Marcotti W, Morara S, Rosina A. Somatotopic nucleocorticalprojections to the multi- ple somatosensory cerebellar maps. Neuroscience83: 1085-104, 1998.
71. Ruigrok T, Teune TM. Collateralization of cerebellar output to functionally distinct brainstem areas. A retrograde, non-fluorescent tracing study in the rat Front Syst Neurosci8: 23, 2014. doi: 10.3389/fnsys.2014.00023
72. Ruigrok T. Ins and Outs of Cerebellar Modules. Cerebellum10: 464-474, 2010. doi:10.1007/s12311-010-0164-y
73. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White D, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. Fiji: an open-source platform for biological-image analysis. Nat Meth9: 676-682, 2012. doi: 10.1038/nmeth.2019
74. Schneider DM, Nelson A, Mooney R. A synaptic and circuit basis for corollary discharge in the auditory cortex Nature513: 189-94, 2014. doi: 10.1038/nature13724
75. Schulman JA, Bloom FE. Golgi cells of the cerebellum are inhibited by inferior oliveactivity. Brain Res210: 350-5, 1981. doi: 10.1016/0006-8993(81)90908-2
76. Simat M, Parpan F, Fritschy J-MM. Heterogeneity of glycinergic and gabaergic interneurons in the granule cell layer of mouse cerebellum. J. Comp. Neurol.500: 71-83, 2007. doi: 10.1002/cne.21142
77. Sommer MA, Wurtz RH. Brain circuits for the internal monitoring of movements Ann. rev. neu- rosci 31:37, 2008. doi: 10.1146/annurev.neuro.31.060407.125627.
78. Sultan F, Augath M, Hamodeh S, Murayama Y. Unravelling cerebellar pathways with high temporal precision targeting motor and extensive sensory and parietal networks. Nat comm 3: 924, 2012. doi: 10.1038/ncomms1912
79. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Kvitsani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson S, Huang Z. A Resource of Cre Driver Lines for Genetic Targeting of GABAergic Neurons in Cerebral Cortex. Neuron71, 2011. doi: 10.1016/j.neuron.2011.07.026
80. Telgkamp P, Padgett D, Ledoux V, Woolley C, Raman I. Maintenance of high-frequency trans- mission at purkinje to cerebellar nuclear synapses by spilloverfrom boutons with multiple re- lease sites. Neuron41: 113-26, 2004.
81. Telgkamp P, Raman I.Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci22: 8447-57, 2002.
82. Teune TM, Burg J, De Zeeuw C, Voogd J, Ruigrok TJH. Single Purkinje cell can innervate multi- ple classes of projection neurons in the cerebellar nuclei of the rat: A light microscopic and ultra- structural triple-tracer study in the rat. J. Comp. Neurol. 392: 164-178, 1998. doi: 10.1002 (SI- CI)1096-9861(19980309)392:2<164::AID-CNE2>3.0.CO;2-0
83. Thompson R, Steinmetz J. The role of the cerebellum in classical conditioning of discrete behav- ioral responses. Neuroscience162: 732-55, 2009. doi:10.1016/j.neuroscience.2009.01.041
84. Tolbert D, Kultas-Ilinsky K, Ilinsky I. EM-autoradiography of cerebellar nucleocortical termi- nals in the cat. Anat. and embryol.161: 215-223, 1980. doi: 10.1007/BF00305345.
85. Tolbert DL, Bantli H, Bloedel JR. Anatomical and physiologicalevidence for a cerebellar nu- cleo-cortical projection in the cat. Neuroscience 1: 205-17, 1976. doi:10.1016/0306- 4522(76)90078-6.
86. Tolbert D, Bantli H, Bloedel J. The intracerebellar nucleocortical projection in a primate. Exp Brain Res30-31, 1977. doi: 10.1007/BF00237266
87. Tolbert D, Bantli H, Bloedel J. Organizational features of the cat and monkey cerebellar nucleo- cortical projection. J. Comp. Neurol.182: 39-56, 1978. doi:10.1002/cne.901820104
88. Tolbert D, Bantli H. An HRP and autoradiographic study of cerebellar corticonuclear- nucleocortical reciprocity in the monkey. Exp Brain Res36:563-571, 1979. doi:10.1007/BF00238523
89. Tsukahara N, Bando T. Red nuclear and interposate nuclear excitation of pontine nuclear cells. Brain research 19: 295-298, 1970. doi:10.1016/0006-8993(70)90442-7
90. Uusisaari M, Knöpfel T. GlyT2+ neurons in the lateral cerebellar nucleus. The Cerebellum 9: 42- 55, 2010. doi 10.1007/s12311-009-0137-1
91. Uusisaari MY, Knöpfel T. Diversity of neuronal elements and circuitry in the cerebellar nuclei. The Cerebellum11: 420-1, 2012. doi: 10.1007/s12311-011-0350-6.
92. Vervaeke K, Lőrincz A, Gleeson P, Farinella M, Nusser Z, Silver R. Rapid Desynchronization of an Electrically Coupled Interneuron Network with Sparse Excitatory Synaptic Input. Neuron67, 2010. doi:10.1016/j.neuron.2010.06.028
93. Vos B, Volny-Luraghi A, Schutter E. Cerebellar Golgi cells in the rat: receptive fields and timing of responses to facial stimulation. Eur. J. Neurosci.11: 2621-2634, 1999. doi: 10.1046/j.1460- 9568.1999.00678.x
94. Wilms CD, Häusser M. Reading out a spatiotemporal population code by imaging neighbouring parallel fibre axons in vivo. Nature communications6:6464, 2015. doi: 10.1038/ncomms7464.
95. Xu W, Edgley S. Climbing fibre-dependent changes in Golgi cell responses to peripheral stimula- tion. J. Physiol. (Lond.)586: 4951-4959, 2008.
96. Zeilhofer H, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bösl M, Fritschy J. Gly- cinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromo- some transgenic mice. J. Comp. Neurol.482: 123-141, 2005.