Spinal motor neuron migration and the significance of topographic organization in the nervous system

Advances in Experimental Medicine and Biology

Volumn 800, Issue , 2014, Pages 133-148

  Kania, Artur ^a,b  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Cadherin; Neuronal migration; Reelin; Spinal cord; Topographic map; Transcription

Indexed keywords

CADHERIN; EPHRIN RECEPTOR; REELIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL MIGRATION; HUMAN; MOTONEURON; MUSCLE INNERVATION; NERVE FIBER GROWTH; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEUROANATOMY; NEUROMODULATION; NEUROTRANSMISSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL; TRANSCRIPTION REGULATION; CELL BODY; MOLECULAR BIOLOGY; MOTOR SYSTEM; MUSCLE; NERVE CELL NETWORK; NERVE FIBER; NERVOUS SYSTEM; NONHUMAN; TOPOGRAPHIC ORGANISATION;

EID: 84959255569     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-7-7687-6_8     Document Type: Article

References (116)

1. Altman J, Bayer SA (1984) The development of the rat spinal cord. Adv Anat Embryol Cell Biol 85:1-164
2. Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766-768
3. Arber S, Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S (1999) Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23(4):659-674
4. Bello SM, Millo H, Rajebhosale M, Price SR (2012) Catenindependent cadherin function drives divisional segregation of spinal motor neurons. J Neurosci 32(2):490-505. doi:10.1523/JNEUROSCI.4382-11.2012
5. Bikeles G (1905) Zur Lokalisation im Ruckenmark. Dtsch Z Nervenheilkd 29(3-4):180-207
6. Brown AG (1981) Organization in the spinal cord: the anatomy and physiology of identified neurones. Springer, Berlin/New York
7. Caviness VS (1976) Patterns of cell and fiber distribution in the neocortex of the reeler mutant mouse. J Comp Neurol 170(4):435-447. doi:10.1002/cne.901700404
8. Caviness VS, Frost DO (1980) Tangential organization of thalamic projections to the neocortex in the mouse. J Comp Neurol 194(2):335-367. doi:10.1002/cne.901940205
9. Caviness VS, Frost DO (1983) Thalamocortical projections in the reeler mutant mouse. J Comp Neurol 219(2):182-202. doi:10.1002/cne.902190205
10. Chang Q, Gonzalez M, Pinter MJ, Balice-Gordon RJ (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J Neurosci 19(24):10813-10828
11. Chen G, Sima J, Jin M, Wang KY, Xue XJ, Zheng W, Ding YQ, Yuan XB (2008) Semaphorin-3A guides radial migration of cortical neurons during development. Nat Neurosci 11(1):36-44. doi:10.1038/nn2018
12. Choi BH (1981) Radial glia of developing human fetal spinal cord: Golgi, immunohistochemical and electron microscopic study. Brain Res 227(2):249-267
13. Chu-Wang IW, Oppenheim RW, Farel PB (1981) Ultrastructure of migrating spinal motoneurons in anuran larvae. Brain Res 213(2):307-318
14. Cohen S, Funkelstein L, Livet J, Rougon G, Henderson CE, Castellani V, Mann F (2005) A semaphorin code defines subpopulations of spinal motor neurons during mouse development. Eur J Neurosci 21(7):1767-1776. doi:10.1111/j.1460- 9568.2005.04021.x
15. Coonan JR, Bartlett PF, Galea MP (2003) Role of EphA4 in defining the position of a motoneuron pool within the spinal cord. J Comp Neurol 458(1):98-111. doi:10.1002/cne.10571
16. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374(6524):719-723. doi:10.1038/374719a0
17. Dambly-Chaudiere C, Gysen A (1986) The sense organs in the Drosophila larva and their relation to the embryonic pattern of sensory neurons. Roux's Arch Dev Biol 195:222-228
18. Dasen JS, Liu JP, Jessell TM (2003) Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425(6961):926-933. doi:10.1038/nature02051
19. Dasen JS, Tice BC, Brenner-Morton S, Jessell TM (2005) A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123(3):477-491. doi:10.1016/j.cell.2005.09.009
20. Dasen JS, De Camilli A, Wang B, Tucker PW, Jessell TM (2008) Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 134(2):304-316. doi:10.1016/j.cell.2008.06.019
21. Demireva EY, Shapiro LS, Jessell TM, Zampieri N (2011) Motor neuron position and topographic order imposed by beta- and gamma-catenin activities. Cell 147(3):641-652. doi:10.1016/j.cell.2011.09.037
22. Dorado ME, Chmielewski CE, Quesada A, Genis-Gálvez JM, Prada FA (1990) Two modes of cell migration in the ventral horn of the spinal cord in the chick embryo. A Golgi study. Histol Histopathol 5(1):37-42
23. Eccles JC, Eccles RM, Lundberg A (1957) The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurones. J Physiol 137(1):22-50
24. Falconer DS (1951) Two new mutants, trembler and reeler, with neurological actions in the house mouse. J Genet 50:192-201
25. Farel PB, Bemelmans SE (1980) Retrograde labeling of migrating spinal motoneurons in bullfrog larvae. Neurosci Lett 18(2):133-136
26. Ferguson BA (1983) Development of motor innervation of the chick following dorsal-ventral limb bud rotations. J Neurosci 3(9):1760-1772
27. Ferns MJ, Hollyday M (1993) Motor innervation of dorsoventrally reversed wings in chick/quail chimeric embryos. J Neurosci 13(6):2463-2476
28. Fulton BP, Miledi R, Takahashi T (1980) Electrical synapses between motoneurons in the spinal cord of the newborn rat. Proc R Soc Lond B Biol Sci 208(1170):115-120
29. Garel S, Garcia-Dominguez M, Charnay P (2000) Control of the migratory pathway of facial branchiomotor neurones. Development 127(24):5297-5307
30. Golding JP, Cohen J (1997) Border controls at the mammalian spinal cord: late-surviving neural crest boundary cap cells at dorsal root entry sites may regulate sensory afferent ingrowth and entry zone morphogenesis. Mol Cell Neurosci 9(5-6):381-396. doi:10.1006/mcne.1997.0647
31. Gomez LA, Brusco A, Saavedra JP (1990) Immunocytochemical study of S-100 positive glial cells in the brainstem and spinal cord of the rat embryo. Int J Dev Neurosci 8(1):55-64
32. Gould TW, Burek MJ, Sosnowski JM, Prevette D, Oppenheim RW (1999) The spatial-temporal gradient of naturally occurring motoneuron death reflects the time of prior exit from the cell cycle and position within the lateral motor column. Dev Biol 216(2):611-621. doi:10.1006/dbio.1999.9490
33. Gutman CR, Ajmera MK, Hollyday M (1993) Organization of motor pools supplying axial muscles in the chicken. Brain Res 609(1-2):129-136
34. Haase G, Dessaud E, Garcès A, de Bovis B, Birling M, Filippi P, Schmalbruch H, Arber S, deLapeyrière O (2002) GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 35(5):893-905
35. Hamburgh M (1963a) Analysis of the postnatal developmental effects of "reeler," a neurological mutation in mice. A study in developmental genetics. Dev Biol 19:165-185
36. Hamburgh M (1963b) Analysis of the postnatal developmental effects of "reeler," a neurological mutation in mice. A study in developmental genetics. Dev Biol 8:165-185
37. Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24(2):481-489
38. Hirotsune S, Takahara T, Sasaki N, Hirose K, Yoshiki A, Ohashi T, Kusakabe M, Murakami Y, Muramatsu M, Watanabe S (1995) The reeler gene encodes a protein with an EGF-like motif expressed by pioneer neurons. Nat Genet 10(1):77-83
39. Hollyday M (1980) Organization of motor pools in the chick lumbar lateral motor column. J Comp Neurol 194(1):143-170. doi:10.1002/cne.901940108
40. Hollyday M (1981) Rules of motor innervation in chick embryos with supernumerary limbs. J Comp Neurol 202(3):439-465. doi:10.1002/cne.902020312
41. Hollyday M, Hamburger V (1977) An autoradiographic study of the formation of the lateral motor column in the chick embryo. Brain Res 132(2):197-208
42. Howell BW, Hawkes R, Soriano P, Cooper JA (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389(6652):733-737. doi:10.1038/39607
43. Huber AB, Kania A, Tran TS, Gu C, De Marco GN, Lieberam I, Johnson D, Jessell TM, Ginty DD, Kolodkin AL (2005) Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48(6):949-964. doi:10.1016/j.neuron.2005.12.003
44. Huettl RE, Soellner H, Bianchi E, Novitch BG, Huber AB (2011) Npn-1 contributes to axon-axon interactions that differentially control sensory and motor innervation of the limb. PLoS Biol 9(2):e1001020. doi:10.1371/journal. pbio.1001020
45. Iwamasa H, Ohta K, Yamada T, Ushijima K, Terasaki H, Tanaka H (1999) Expression of Eph receptor tyrosine kinases and their ligands in chick embryonic motor neurons and hindlimb muscles. Dev Growth Differ 41(6):685-698
46. Jacobson M (1991) Developmental neurobiology, 3rd edn. Plenum Press, New York
47. Jossin Y, Cooper JA (2011) Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat Neurosci 14(6):697-703. doi:10.1038/nn.2816
48. Kania A, Jessell TM (2003) Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38(4):581-596
49. Kania A, Johnson RL, Jessell TM (2000) Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102(2):161-173
50. Kao TJ, Law C, Kania A (2012) Eph and ephrin signaling: lessons learned from spinal motor neurons. Semin Cell Dev Biol 23(1):83-91. doi:10.1016/j. semcdb.2011.10.016
51. Klein R (2012) Eph/ephrin signalling during development. Development 139(22):4105-4109. doi:10.1242/dev.074997
52. Lance-Jones C, Landmesser L (1981) Pathway selection by chick lumbosacral motoneurons during normal development. Proc R Soc Lond B Biol Sci 214(1194):1-18
53. Landmesser L (1978a) The development of motor projection patterns in the chick hind limb. J Physiol (Lond) 284:391-414
54. Landmesser L (1978b) The distribution of motoneurones supplying chick hind limb muscles. J Physiol (Lond) 284:371-389
55. Landmesser LT, O'Donovan MJ (1984) The activation patterns of embryonic chick motoneurones projecting to inappropriate muscles. J Physiol 347:205-224
56. Leber SM, Sanes JR (1995) Migratory paths of neurons and glia in the embryonic chick spinal cord. J Neurosci 15(2):1236-1248
57. Leber SM, Sanes JR, Breedlove SM (1990) Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord. J Neurosci 10(7):2451-2462
58. Levi-Montalcini R (1950) The origin and development of the visceral system in the spinal cord of the chick embryo. J Morphol 86(2):253-283. doi:10.1002/Jmor.1050860203
59. Lin JH, Saito T, Anderson DJ, Lance-Jones C, Jessell TM, Arber S (1998) Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression. Cell 95(3):393-407
60. Livet J, Sigrist M, Stroebel S, De Paola V, Price SR, Henderson CE, Jessell TM, Arber S (2002) ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 35(5):877-892
61. Lu J, Tapia JC, White OL, Lichtman JW (2009) The interscutularis muscle connectome. PLoS Biol 7(2):e32. doi:10.1371/journal.pbio.1000032
62. Magdaleno S, Keshvara L, Curran T (2002) Rescue of ataxia and preplate splitting by ectopic expression of Reelin in reeler mice. Neuron 33(4):573-586
63. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127(24):5253-5263
64. Markham JA, Vaughn JE (1991) Migration patterns of sympathetic preganglionic neurons in embryonic rat spinal cord. J Neurobiol 22(8):811-822. doi:10.1002/neu.480220803
65. McHanwell S, Biscoe TJ (1981) The localization of motoneurons supplying the hindlimb muscles of the mouse. Philos Trans R Soc Lond B Biol Sci 293(1069):477-508
66. Moret F, Renaudot C, Bozon M, Castellani V (2007) Semaphorin and neuropilin co-expression in motoneurons sets axon sensitivity to environmental semaphorin sources during motor axon pathfinding. Development 134(24):4491-4501. doi:10.1242/dev.011452
67. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409(6821):714-720. doi:10.1038/35055553
68. Nollet F, Kools P, van Roy F (2000) Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 299(3):551-572. doi:10.1006/jmbi.2000.3777
69. Nornes HO, Das GD (1974) Temporal pattern of neurogenesis in spinal cord of rat. I. An autoradiographic study-time and sites of origin and migration and settling patterns of neuroblasts. Brain Res 73(1):121-138
70. O'Rourke NA, Dailey ME, Smith SJ, McConnell SK (1992) Diverse migratory pathways in the developing cerebral cortex. Science 258(5080):299-302
71. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14(5):899-912
72. Oppenheim RW, Cole T, Prevette D (1989) Early regional variations in motoneuron numbers arise by differential proliferation in the chick embryo spinal cord. Dev Biol 133(2):468-474
73. Palmesino E, Rousso DL, Kao TJ, Klar A, Laufer E, Uemura O, Okamoto H, Novitch BG, Kania A (2010) Foxp1 and lhx1 coordinate motor neuron migration with axon trajectory choice by gating Reelin signalling. PLoS Biol 8(8):e1000446. doi:10.1371/journal.pbio.1000446
74. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cortex of man as studied by electrical stimulation. Brain 60(4):389-443
75. Personius KE, Chang Q, Mentis GZ, O'Donovan MJ, Balice-Gordon RJ (2007) Reduced gap junctional coupling leads to uncorrelated motor neuron firing and precocious neuromuscular synapse elimination. Proc Natl Acad Sci U S A 104(28):11808-11813. doi:10.1073/pnas.0703357104
76. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM (1996) Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neurondependent step in interneuron differentiation. Cell 84(2):309-320
77. Phelps PE, Barber RP, Vaughn JE (1991) Embryonic development of choline acetyltransferase in thoracic spinal motor neurons: somatic and autonomic neurons may be derived from a common cellular group. J Comp Neurol 307(1):77-86. doi:10.1002/cne.903070108
78. Phelps PE, Phelps PE, Rich R, Dupuy-Davies S, Ríos Y, Wong T (2002) Evidence for a cell-specific action of Reelin in the spinal cord. Dev Biol 244(1):180-198. doi:10.1006/dbio.2002.0580
79. Prasad A, Hollyday M (1991) Development and migration of avian sympathetic preganglionic neurons. J Comp Neurol 307(2):237-258. doi:10.1002/cne.903070207
80. Price SR (2012) Cell adhesion and migration in the organization of spinal motor neurons. Cell Adhes Migr 6(5):385-389. doi:10.4161/cam.21044
81. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM (2002) Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109(2):205-216
82. Rakic P (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus rhesus. J Comp Neurol 141(3):283-312. doi:10.1002/cne.901410303
83. Rall W, Burke RE, Smith TG, Nelson PG, Frank K (1967) Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J Neurophysiol 30(5):1169-1193
84. Ramón y Cajal S (1911) Histologie du Système Nerveux de l'Homme et des Vertébrés. A. Maloine, Paris
85. Ramón y Cajal S (1989) Recollections of my life, 1st MIT Press pbk. edn. MIT Press, Cambridge, MA
86. Rice DS, Nusinowitz S, Azimi AM, Martinez A, Soriano E, Curran T (2001) The Reelin pathway modulates the structure and function of retinal synaptic circuitry. Neuron 31(6):929-941
87. Romanes GJ (1951) The motor cell columns of the lumbo-sacral spinal cord of the cat. J Comp Neurol 94(2):313-363
88. Romanes GJ (1964) The motor pools of the spinal cord. Prog Brain Res 11:93-119
89. Rousso DL, Gaber ZB, Wellik D, Morrisey EE, Novitch BG (2008) Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 59(2):226-240. doi:10.1016/j. neuron.2008.06.025
90. Sanyas I, Bozon M, Moret F, Castellani V (2012) Motoneuronal Sema3C is essential for setting stereotyped motor tract positioning in limb-derived chemotropic semaphorins. Development 139(19):3633-3643. doi:10.1242/dev.080051
91. Senturk A, Pfennig S, Weiss A, Burk K, Acker-Palmer A (2011) Ephrin Bs are essential components of the Reelin pathway to regulate neuronal migration. Nature 472(7343):356-360. doi:10.1038/nature09874
92. Sharma K, Leonard AE, Lettieri K, Pfaff SL (2000) Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature 406(6795):515-519. doi:10.1038/35020078
93. Sheldon M, Rice DS, D'Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389(6652):730-733. doi:10.1038/39601
94. Sockanathan S, Jessell TM (1998) Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94(4):503-514
95. Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci U S A 50:703-710
96. Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384(6610):630-634. doi:10.1038/384630a0
97. Summerbell D, Stirling RV (1981) The innervation of dorsoventrally reversed chick wings: evidence that motor axons do not actively seek out their appropriate targets. J Embryol Exp Morphol 61:233-247
98. Surmeli G, Akay T, Ippolito GC, Tucker PW, Jessell TM (2011) Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template. Cell 147(3):653-665. doi:10.1016/j.cell.2011.10.012
99. Suzuki SC, Inoue T, Kimura Y, Tanaka T, Takeichi M (1997) Neuronal circuits are subdivided by differential expression of type-II classic cadherins in postnatal mouse brains. Mol Cell Neurosci 9(5-6):433-447. doi:10.1006/mcne.1997.0626
100. Tanabe Y, William C, Jessell TM (1998) Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95(1):67-80
101. Thaler J, Harrison K, Sharma K, Lettieri K, Kehrl J, Pfaff SL (1999) Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23(4):675-687
102. Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4(6):496-505
103. Tosney KW, Landmesser LT (1985) Development of the major pathways for neurite outgrowth in the chick hindlimb. Dev Biol 109(1):193-214
104. Tripodi M, Stepien AE, Arber S (2011) Motor antagonism exposed by spatial segregation and timing of neurogenesis. Nature 479(7371):61-66. doi:10.1038/nature10538
105. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97(6):689-701
106. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL (1994) Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79(6):957-970
107. Villeda SA, Akopians AL, Babayan AH, Basbaum AI, Phelps PE (2006) Absence of Reelin results in altered nociception and aberrant neuronal positioning in the dorsal spinal cord. Neuroscience 139(4):1385-1396. doi:10.1016/j. neuroscience.2006.01.042
108. Vrieseling E, Arber S (2006) Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 127(7):1439-1452. doi:10.1016/j.cell.2006.10.042
109. Wang X, Babayan AH, Basbaum AI, Phelps PE (2012) Loss of the Reelin-signaling pathway differentially disrupts heat, mechanical and chemical nociceptive processing. Neuroscience 226:441-450. doi:10.1016/j.neuroscience. 2012.09.027
110. Whitelaw V, Hollyday M (1983) Thigh and calf discrimination in the motor innervation of the chick hindlimb following deletions of limb segments. J Neurosci 3(6):1199-1215
111. Xu Q, Mellitzer G, Robinson V, Wilkinson DG (1999) In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399(6733):267-271. doi:10.1038/20452
112. Yip JW, Yip YP, Nakajima K, Capriotti C (2000) Reelin controls position of autonomic neurons in the spinal cord. Proc Natl Acad Sci U S A 97(15):8612-8616. doi:10.1073/pnas.150040497
113. Yip YP, Capriotti C, Yip JW (2003a) Migratory pathway of sympathetic preganglionic neurons in normal and reeler mutant mice. J Comp Neurol 460(1):94-105. doi:10.1002/cne.10634
114. Yip YP, Rinaman L, Capriotti C, Yip JW (2003b) Ectopic sympathetic preganglionic neurons maintain proper connectivity in the reeler mutant mouse. Neuroscience 118(2):439-450
115. Yip YP, Capriotti C, Magdaleno S, Benhayon D, Curran T, Nakajima K, Yip JW (2004) Components of the Reelin signaling pathway are expressed in the spinal cord. J Comp Neurol 470(2):210-219. doi:10.1002/cne.20001
116. Yip YP, Mehta N, Magdaleno S, Curran T, Yip JW (2009) Ectopic expression of Reelin alters migration of sympathetic preganglionic neurons in the spinal cord. J Comp Neurol 515(2):260-268. doi:10.1002/cne.22044