The late and dual origin of cerebrospinal fluid-contacting neurons in the mouse spinal cord

Development (Cambridge)

Volumn 143, Issue 5, 2016, Pages 880-891

  Petracca, Yanina L ^a   Sartoretti, Maria Micaela ^a   di Bella, Daniela J ^a   Marin Burgin, Antonia ^a,b   Carcagno, Abel L ^a   Schinder, Alejandro F ^a   Lanuza, Guillermo M ^a  

^a Instituto Leloir and Consejo Nacional de Investigaciones Cientıf́icas y Técnicas ^*  (Argentina)

^b Instituto de Investigación en Biomedicina de Buenos Aires   (Argentina)

Author keywords

Central canal; Ependyma; Late born neurons; Spinal cord; Transcription factor

Indexed keywords

EYE PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXN4 PROTEIN, MOUSE; GATA2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR GATA 2;

ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CEREBROSPINAL FLUID; CYTOLOGY; ELECTROPHYSIOLOGY; EMBRYOLOGY; FEMALE; GENETICS; GENOTYPE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; METABOLISM; MOTONEURON; MOUSE; NERVE CELL; PHYSIOLOGY; SPINAL CORD; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CEREBROSPINAL FLUID; ELECTROPHYSIOLOGY; EYE PROTEINS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GATA2 TRANSCRIPTION FACTOR; GENOTYPE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURONS; MICE; MOTOR NEURONS; NEURONS; SPINAL CORD; STEM CELLS;

EID: 84959259183     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.129254     Document Type: Article

References (99)

1. Altman, J. and Bayer, S. A. (1984). The development of the rat spinal cord. Adv. Anat. Embryol. Cell Biol. 85, 1-164.
2. Balaskas, N., Ribeiro, A., Panovska, J., Dessaud, E., Sasai, N., Page, K. M., Briscoe, J. and Ribes, V. (2012). Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 148, 273-284.
3. Barber, R. P., Vaughn, J. E. and Roberts, E. (1982). The cytoarchitecture of GABAergic neurons in rat spinal cord. Brain Res. 238, 305-328.
4. Batista, M. F., Jacobstein, J. and Lewis, K. E. (2008). Zebrafish V2 cells develop into excitatory CiD and Notch signalling dependent inhibitory VeLD interneurons. Dev. Biol. 322, 263-275.
5. Bielle, F., Griveau, A., Narboux-Nême, N., Vigneau, S., Sigrist, M., Arber, S., Wassef, M. and Pierani, A. (2005). Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat. Neurosci. 8, 1002-1012.
6. Briscoe, J. and Novitch, B. G. (2008). Regulatory pathways linking progenitor patterning, cell fates and neurogenesis in the ventral neural tube. Philos. Trans. R. Soc. B Biol. Sci. 363, 57-70.
7. Briscoe, J., Sussel, L., Serup, P., Hartigan-O’Connor, D., Jessell, T. M., Rubenstein, J. L. and Ericson, J. (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398, 622-627.
8. Briscoe, J., Pierani, A., Jessell, T. M. and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445.
9. Brockschnieder, D., Lappe-Siefke, C., Goebbels, S., Boesl, M. R., Nave, K.-A. and Riethmacher, D. (2004). Cell depletion due to diphtheria toxin fragment A after Cre-mediated recombination. Mol. Cell. Biol. 24, 7636-7642.
10. Bruni, J. E. (1998). Ependymal development, proliferation, and functions: a review. Microsc. Res. Tech. 41, 2-13.
11. Bylund, M., Andersson, E., Novitch, B. G. and Muhr, J. (2003). Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 6, 1162-1168.
12. Carcagno, A. L., Di Bella, D. J., Goulding, M., Guillemot, F. and Lanuza, G. M. (2014). Neurogenin3 restricts serotonergic neuron differentiation to the hindbrain. J. Neurosci. 34, 15223-15233.
13. Chen, J.-A., Huang, Y.-P., Mazzoni, E. O., Tan, G. C., Zavadil, J. and Wichterle, H. (2011). Mir-17-3p controls spinal neural progenitor patterning by regulating Olig2/Irx3 cross-repressive loop. Neuron 69, 721-735.
14. Cheng, L., Arata, A., Mizuguchi, R., Qian, Y., Karunaratne, A., Gray, P. A., Arata, S., Shirasawa, S., Bouchard, M., Luo, P. et al. (2004). Tlx3 and Tlx1 are postmitotic selector genes determining glutamatergic over GABAergic cell fates. Nature Neurosci. 7, 510-517.
15. Crone, S. A., Quinlan, K. A., Zagoraiou, L., Droho, S., Restrepo, C. E., Lundfald, L., Endo, T., Setlak, J., Jessell, T. M., Kiehn, O. et al. (2008). Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 60, 70-83.
16. Dale, N., Roberts, A., Ottersen, O. P. and Storm-Mathisen, J. (1987a). The development of a population of spinal cord neurons and their axonal projections revealed by GABA immunocytochemistry in frog embryos. Proc. R. Soc. B Biol. Sci. 232, 205-215.
17. Dale, N., Roberts, A., Ottersen, O. P. and Storm-Mathisen, J. (1987b). The morphology and distribution of ‘Kolmer-Agduhr cells’, a class of cerebrospinalfluid- contacting neurons revealed in the frog embryo spinal cord by GABA immunocytochemistry. Proc. R. Soc. B Biol. Sci. 232, 193-203.
18. DeCaen, P. G., Delling, M., Vien, T. N. and Clapham, D. E. (2013). Direct recording and molecular identification of the calcium channel of primary cilia. Nature 504, 315-318.
19. Del Barrio, M. G., Taveira-Marques, R., Muroyama, Y., Yuk, D.-I., Li, S., Wines- Samuelson, M., Shen, J., Smith, H. K., Xiang, M., Rowitch, D. et al. (2007). A regulatory network involving Foxn4, Mash1 and delta-like 4/Notch1 generates V2a and V2b spinal interneurons from a common progenitor pool. Development 134, 3427-3436.
20. Dessaud, E., Ribes, V., Balaskas, N., Yang, L. L., Pierani, A., Kicheva, A., Novitch, B. G., Briscoe, J. and Sasai, N. (2010). Dynamic assignment and maintenance of positional identity in the ventral neural tube by the morphogen sonic hedgehog. PLoS Biol. 8, e1000382.
21. Djenoune, L., Khabou, H., Joubert, F., Quan, F. B., Nunes Figueiredo, S., Bodineau, L., Del Bene, F., Burcklé C, Tostivint H, and Wyart C. (2014). Investigation of spinal cerebrospinal fluid-contacting neurons expressing PKD2L1: evidence for a conserved system from fish to primates. Front. Neuroanat. 8, 26
22. Dougherty, K. J., Zagoraiou, L., Satoh, D., Rozani, I., Doobar, S., Arber, S., Jessell, T. M. and Kiehn, O. (2013). Locomotor rhythm generation linked to the output of spinal shox2 excitatory interneurons. Neuron 80, 920-933.
23. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M. and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
24. Espósito M. S, Piatti V. C, Laplagne D. A, Morgenstern N. A, Ferrari C. C, Pitossi F. J, and Schinder A. F. (2005). Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 25, 10074-10086
25. Fidelin, K., Djenoune, L., Stokes, C., Prendergast, A., Gomez, J., Baradel, A., Del Bene, F. and Wyart C. (2015). State-dependent modulation of locomotion by GABAergic spinal sensory neurons. Curr. Biol. 25, 3035-3047.
26. Francius, C., Harris, A., Rucchin, V., Hendricks, T. J., Stam, F. J., Barber, M., Kurek, D., Grosveld, F. G., Pierani, A., Goulding, M. et al. (2013). Identification of multiple subsets of ventral interneurons and differential distribution along the rostrocaudal axis of the developing spinal cord. PLoS ONE 8, e70325.
27. Fu, H., Qi, Y., Tan, M., Cai, J., Hu, X., Liu, Z., Jensen, J. and Qiu, M. (2003). Molecular mapping of the origin of postnatal spinal cord ependymal cells: evidence that adult ependymal cells are derived from Nkx6.1+ ventral neural progenitor cells. J. Comp. Neurol. 456, 237-244.
28. Gosgnach, S., Lanuza, G. M., Butt, S. J. B., Saueressig, H., Zhang, Y., Velasquez, T., Riethmacher, D., Callaway, E. M., Kiehn, O. and Goulding, M. (2006). V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440, 215-219.
29. Goulding, M. (2009). Circuits controlling vertebrate locomotion: moving in a new direction. Nat. Rev. Neurosci. 10, 507-518.
30. Gross, M. K., Dottori, M. and Goulding, M. (2002). Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34, 535-549.
31. Hochstim, C., Deneen, B., Lukaszewicz, A., Zhou, Q. and Anderson, D. J. (2008). Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 133, 510-522.
32. Holz, A., Kollmus, H., Ryge, J., Niederkofler, V., Dias, J., Ericson, J., Stoeckli, E. T., Kiehn, O. and Arnold, H.-H. (2010). The transcription factors Nkx2.2 and Nkx2.9 play a novel role in floor plate development and commissural axon guidance. Development 137, 4249-4260.
33. Huang, A. L., Chen, X., Hoon, M. A., Chandrashekar, J., Guo, W., Tränkner D, Ryba N. J. P, and Zuker C. S. (2006). The cells and logic for mammalian sour taste detection. Nature 442, 934-938
34. Huang, P., Xiong, F., Megason, S. G. and Schier, A. F. (2012). Attenuation of Notch and Hedgehog signaling is required for fate specification in the spinal cord. PLoS Genet. 8, e1002762.
35. Ishimaru, Y., Inada, H., Kubota, M., Zhuang, H., Tominaga, M. and Matsunami, H. (2006). Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc. Natl. Acad. Sci. USA 103, 12569-12574.
36. Jalalvand, E., Robertson, B., Wallén P, Hill R. H, and Grillner S. (2014). Laterally projecting cerebrospinal fluid-contacting cells in the lamprey spinal cord are of two distinct types. J. Comp. Neurol. 522, 1753-1768
37. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
38. Joshi, K., Lee, S., Lee, B., Lee, J. W. and Lee, S.-K. (2009). LMO4 controls the balance between excitatory and inhibitory spinal V2 interneurons. Neuron 61, 839-851.
39. Karunaratne, A., Hargrave, M., Poh, A. and Yamada, T. (2002). GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Dev. Biol. 249, 30-43.
40. Kimura, Y., Satou, C. and Higashijima, S.-i. (2008). V2a and V2b neurons are generated by the final divisions of pair-producing progenitors in the zebrafish spinal cord. Development 135, 3001-3005.
41. Kirby, B. B., Takada, N., Latimer, A. J., Shin, J., Carney, T. J., Kelsh, R. N. and Appel, B. (2006). In vivo time-lapse imaging shows dynamic oligodendrocyteprogenitor behavior during zebrafish development. Nat. Neurosci. 9, 1506-1511
42. Kútna V, Ševc J, Gombalová Z, Matiašová, A, Daxnerová Z. (2014). Enigmatic cerebrospinal fluid-contacting neurons arise even after the termination of neurogenesis in the rat spinal cord during embryonic development and retain their immature-like characteristics until adulthood. Acta Histochem. 116, 278-285
43. Lanuza, G. M., Gosgnach, S., Pierani, A., Jessell, T. M. and Goulding, M. (2004). Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42, 375-386
44. Laplagne D. A., Zylberman, V., Ainciart, N., Steward, M.W., Sciutto, E., Fossati, C. A. and Goldbaum, F. A. (2004). Engineering of a polymeric bacterial protein as a scaffold for the multiple display of peptides. Proteins 57, 820-828.
45. Lek, M., Dias, J. M., Marklund, U., Uhde, C. W., Kurdija, S., Lei, Q., Sussel, L., Rubenstein, J. L., Matise, M. P., Arnold, H.-H. et al. (2010). A homeodomain feedback circuit underlies step-function interpretation of a Shh morphogen gradient during ventral neural patterning. Development 137, 4051-4060.
46. Li, S., Mo, Z., Yang, X., Price, S. M., Shen, M. M. and Xiang, M. (2004). Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors. Neuron 43, 795-807.
47. Li, S., Misra, K., Matise, M. P. and Xiang, M. (2005). Foxn4 acts synergistically with Mash1 to specify subtype identity of V2 interneurons in the spinal cord. Proc. Natl. Acad. Sci. USA 102, 10688-10693.
48. Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C. D. and Rowitch, D. H. (2002). Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86.
49. Lundfald, L., Restrepo, C. E., Butt, S. J. B., Peng, C.-Y., Droho, S., Endo, T., Zeilhofer, H. U., Sharma, K. and Kiehn, O. (2007). Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur. J. Neurosci. 26, 2989-3002.
50. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R. et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140.
51. Mao, X., Fujiwara, Y., Chapdelaine, A., Yang, H. and Orkin, S. H. (2001). Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood 97, 324-326.
52. Marichal, N., Garcia, G., Radmilovich M., Trujillo-Cenoz, O. and Russo R. E. (2009). Enigmatic central canal contacting cells: immature neurons in “standby mode”? J. Neurosci. 29, 10010-10024.
53. Marichal, N., Garcı́a G, Radmilovich M, Trujillo-Cenóz O, Russo R. E. (2012). Spatial domains of progenitor-like cells and functional complexity of a stem cell niche in the neonatal rat spinal cord. Stem Cells 30, 2020-2031
54. McKinney, M. and McNamara, K. J. (1991). Heterochrony: The Evolution of Ontogeny. New York: Springer US.
55. Meletis, K., Barnabé-Heider F, Carlén M, Evergren E, Tomilin N, Shupliakov O, Frisén J. (2008). Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol. 6, e182
56. Orts-Del’Immagine, A, Wanaverbecq, N., Tardivel, C., Tillement, V., Dallaporta, M. and Trouslard, J. (2012). Properties of subependymal cerebrospinal fluid contacting neurones in the dorsal vagal complex of the mouse brainstem. J. Physiol. 590, 3719-3741
57. Orts-Del’Immagine, A., Kastner, A., Tillement, V., Tardivel, C., Trouslard, J. and Wanaverbecq, N. (2014). Morphology, distribution and phenotype of polycystin kidney disease 2-like 1-positive cerebrospinal fluid contacting neurons in the brainstem of adult mice. PLoS ONE 9, e87748
58. Orts Del’Immagine, A., Seddik, R., Tell, F., Airault, C., Er-Raoui, G., Najimi, M., Trouslard, J, Wanaverbecq, N. (2016). A single polycystic kidney disease 2- like 1 channel opening acts as a spike generator in cerebrospinal fluid-contacting neurons of adult mouse brainstem. Neuropharmacology. 101, 549-565.
59. Panayi, H., Panayiotou, E., Orford, M., Genethliou, N., Mean, R., Lapathitis, G., Li, S., Xiang, M., Kessaris, N., Richardson, W. D. et al. (2010). Sox1 is required for the specification of a novel p2-derived interneuron subtype in the mouse ventral spinal cord. J. Neurosci. 30, 12274-12280.
60. Panayiotou, E., Panayi, E., Lapathitis, G., Francius, C., Clotman, F., Kessaris, N., Richardson, W. D. and Malas, S. (2013). Pax6 is expressed in subsets of V0 and V2 interneurons in the ventral spinal cord in mice. Gene Expr. Patterns 13, 328-334.
61. Park, H.-C., Shin, J. and Appel, B. (2004). Spatial and temporal regulation of ventral spinal cord precursor specification by Hedgehog signaling. Development 131, 5959-5969.
62. Peng, C.-Y., Yajima, H., Burns, C. E., Zon, L. I., Sisodia, S. S., Pfaff, S. L. and Sharma, K. (2007). Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53, 813-827.
63. Pierani, A., Moran-Rivard, L., Sunshine, M. J., Littman, D. R., Goulding, M. and Jessell, T. M. (2001). Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29, 367-384.
64. Reali, C., Fernández A, Radmilovich M, Trujillo-Cenóz O, Russo R. E. (2011). GABAergic signalling in a neurogenic niche of the turtle spinal cord. J. Physiol. 589, 5633-5647
65. Rocha, S. F., Lopes, S. S., Gossler, A. and Henrique, D. (2009). Dll1 and Dll4 function sequentially in the retina and pV2 domain of the spinal cord to regulate neurogenesis and create cell diversity. Dev. Biol. 328, 54-65
66. Rowitch, D. H. (2004). Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419.
67. Rowitch, D. H. and Kriegstein, A. R. (2010). Developmental genetics of vertebrate glial-cell specification. Nature 468, 214-222.
68. Sabourin, J.-C., Ackema, K. B., Ohayon, D., Guichet, P.-O., Perrin, F. E., Garces, A., Ripoll, C., Charité J, Simonneau L, Kettenmann H, et al. (2009). A mesenchymal-like ZEB1(+) niche harbors dorsal radial glial fibrillary acidic protein-positive stem cells in the spinal cord. Stem Cells 27, 2722-2733
69. Sapir, T., Geiman, E. J, Wang, Z., Velasquez, T., Mitsui, S., Yoshihara, Y., Frank, E., Alvarez, F. J. and Goulding, M. (2004). Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development. J. Neurosci. 24, 1255-1264.
70. Schäfer M, Kinzel D, and Winkler C. (2007). Discontinuous organization and specification of the lateral floor plate in zebrafish. Dev. Biol. 301, 117-129
71. Semmo, M., Köttgen M, and Hofherr A. (2014). The TRPP subfamily and polycystin-1 proteins. Handb. Exp. Pharmacol. 222, 675-711
72. Shin, J., Poling, J., Park, H.-C. and Appel, B. (2007). Notch signaling regulates neural precursor allocation and binary neuronal fate decisions in zebrafish. Development 134, 1911-1920.
73. Smith, K. K. (2003). Time’s arrow: heterochrony and the evolution of development. Int. J. Dev. Biol. 47, 613-621.
74. Spassky, N., Merkle, F. T., Flames, N., Tramontin, A. D., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J. Neurosci. 25, 10-18.
75. Stam, F. J., Hendricks, T. J., Zhang, J., Geiman, E. J., Francius, C., Labosky, P. A., Clotman, F. and Goulding, M. (2012). Renshaw cell interneuron specialization is controlled by a temporally restricted transcription factor program. Development 139, 179-190.
76. Stoeckel, M.-E., Uhl-Bronner, S., Hugel, S., Veinante, P., Klein, M.-J., Mutterer, J., Freund-Mercier, M.-J. and Schlichter, R. (2003). Cerebrospinal fluidcontacting neurons in the rat spinal cord, a gamma-aminobutyric acidergic system expressing the P2X2 subunit of purinergic receptors, PSA-NCAM, and GAP-43 immunoreactivities: light and electron microscopic study. J. Comp. Neurol. 457, 159-174.
77. Strähle U, Lam C. S, Ertzer R, and Rastegar S. (2004). Vertebrate floor-plate specification: variations on common themes. Trends Genet. 20, 155-162
78. Suzuki, N., Ohneda, O., Minegishi, N., Nishikawa, M., Ohta, T., Takahashi, S., Engel, J. D. and Yamamoto, M. (2006). Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proc. Natl. Acad. Sci. USA 103, 2202-2207.
79. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J.-I., Obata, K. and Kaneko, T. (2003). Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 467, 60-79.
80. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsiani, D., Fu, Y., Lu, J., Lin, Y. et al. (2011). A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013.
81. Temple, S. (2001). The development of neural stem cells. Nature 414, 112-117.
82. Tsai, H.-H., Li, H., Fuentealba, L. C., Molofsky, A. V., Taveira-Marques, R., Zhuang, H., Tenney, A., Murnen, A. T., Fancy, S. P. J., Merkle, F. et al. (2012). Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337, 358-362.
83. Vallstedt, A., Klos, J. M. and Ericson, J. (2005). Multiple dorsoventral origins of oligodendrocyte generation in the spinal cord and hindbrain. Neuron 45, 55-67.
84. van Doorninck, J. H., van Der Wees, J., Karis, A., Goedknegt, E., Engel, J. D., Coesmans, M., Rutteman, M., Grosveld, F. and De Zeeuw, C. I. (1999). GATA-3 is involved in the development of serotonergic neurons in the caudal raphe nuclei. J. Neurosci. 19, RC12.
85. Vigh, B. and Vigh-Teichmann, I. (1971). Structure of the medullo-spinal liquor contacting neuronal system. Acta Biol. Acad. Sci. Hung. 22, 227-243.
86. Vigh, B. and Vigh-Teichmann, I. (1998). Actual problems of the cerebrospinal fluidcontacting neurons. Microsc. Res. Tech. 41, 57-83.
87. Vigh, B., Vigh-Teichmann, I. and Aros, B. (1977). Special dendritic and axonal endings formed by the cerebrospinal fluid contacting neurons of the spinal cord. Cell Tissue Res. 183, 541-552.
88. Vigh, B., Vigh-Teichmann, I., Manzano e Silva, M. J. and van den Pol, A. N. (1983). Cerebrospinal fluid-contacting neurons of the central canal and terminal ventricle in various vertebrates. Cell Tissue Res. 231, 615-621.
89. Vigh, B., Manzano e Silva, M. J., Frank, C. L., Vincze, C., Czirok, S. J., Szabo, A., Lukats, A. and Szel, A. (2004). The system of cerebrospinal fluid-contacting neurons. Its supposed role in the nonsynaptic signal transmission of the brain. Histol. Histopathol. 19, 607-628.
90. Wyart C., Del Bene, F, Warp, E., Scott, E. K., Trauner, D., Baier, H. and Isacoff, E. Y. (2009). Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461, 407-410.
91. Yang, L., Rastegar S. and Strahle, U. (2010). Regulatory interactions specifying Kolmer-Agduhr interneurons. Development 137, 2713-2722.
92. Yeo, S.-Y. and Chitnis, A. B. (2007). Jagged-mediated Notch signaling maintains proliferating neural progenitors and regulates cell diversity in the ventral spinal cord. Proc. Natl. Acad. Sci. USA 104, 5913-5918.
93. Yu, K., McGlynn, S. and Matise, M. P. (2013). Floor plate-derived sonic hedgehog regulates glial and ependymal cell fates in the developing spinal cord. Development 140, 1594-1604.
94. Zhang, Z.-w. (2004). Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J. Neurophysiol. 91, 1171-1182.
95. Zhang, Y., Narayan, S., Geiman, E., Lanuza, G. M., Velasquez, T., Shanks, B., Akay, T., Dyck, J., Pearson, K., Gosgnach, S. et al. (2008). V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 60, 84-96.
96. Zhang, J., Lanuza, G. M., Britz, O., Wang, Z., Siembab, V. C., Zhang, Y., Velasquez, T., Alvarez, F. J., Frank, E. and Goulding, M. (2014). V1 and v2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion. Neuron 82, 138-150.
97. Zhou, Q. and Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73.
98. Zhou, Y., Yamamoto, M. and Engel, J. D. (2000). GATA2 is required for the generation of V2 interneurons. Development 127, 3829-3838
99. Ziskind-Conhaim, L. (1988). Electrical properties of motoneurons in the spinal cord of rat embryos. Dev. Biol. 128, 21-29.