The acquisition of motoneuron subtype identity and motor circuit formation
Corresponding Author
Lynn T. Landmesser
Department of Neurosciences, Case Western Reserve University, School of Medicine, 10900 Euclid Ave., Cleveland, OH, 44106-4975 USA
Tel.: +1-216-3683996; fax: +1-216-3684650
E-mail address: [email protected] (L.T. Landmesser).
Search for more papers by this authorCorresponding Author
Lynn T. Landmesser
Department of Neurosciences, Case Western Reserve University, School of Medicine, 10900 Euclid Ave., Cleveland, OH, 44106-4975 USA
Tel.: +1-216-3683996; fax: +1-216-3684650
E-mail address: [email protected] (L.T. Landmesser).
Search for more papers by this authorAbstract
Experiments in chick embryos using classical transplantation techniques introduced by Viktor Hamburger are reviewed; these demonstrated that chick-limb innervating motoneurons become specified by extrinsic signals prior to axon outgrowth and that they selectively grow to appropriate muscles by actively responding to guidance cues within the limb. More recent experiments reveal that fast/slow and flexor/extensor subclasses of motoneurons are distinct by E4–5 and that they exhibit patterned spontaneous activity while still growing to their targets. These observations are then related to the combinatorial code of LIM transcription factor expression, which has been hypothesized to specify motoneuron subtypes.
References
- S. Arber, B. Han, M. Mendelsohn, M. Smith, T.M. Jesell, S. Sockanathan. Requirement for the homeobox gene Hb9 in the consolidation of motoneuron identity. Neuron. 23: 1999; 659–674
- A. Bekoff. Ontogeny of leg motor output in the chick embryo: a neural analysis. Brain Res. 106: 1976; 271–291
- F. Bladt, D. Rietmacher, S. Isenmann, A. Aguzzi, C. Birchmeier. Essential role of the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature. 376: 1995; 768–771
- J. Briscoe, A. Pierani, T.M. Jessell, J. Ericson. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell. 101: 2000; 435–445
- J. Butler, E. Cosmos, J. Brierley. Differentiation of muscle fiber types in aneurogenic brachial muscles of the chick embryo. J. Exp. Zool. 224: 1982; 65–80
- L.M. Dahm, L.T. Landmesser. The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev. Biol. 130: 1988; 621–644
- A. Ebens, K. Brose, E.D. Leonardo, M.G. Hanson, F. Bladt, C. Birchmeier, B.A. Barres, M. Tessier-Lavigne. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron. 17: 1996; 1157–1172
- J. Eberhart, M. Swartz, S.A. Koblar, E.B. Pasquale, H. Tanaka, C.E. Krull. Expression of EphA4, ephrin-A2 and ephrin A5 during axon outgrowth to the hindlimb indicates potential roles in pathfinding. Dev. Neurosci. 22: 2000; 237–250
- M. Ensini, T.N. Tsuchida, H.G. Belting, T.M. Jessell. The control of rostrocaudal pattern in the developing spinal cord: specification of motor neuron subtype identity is initiated by signals from the paraxial mesoderm. Development. 125: 1998; 969–982
- B. Fedirchuk, P. Wenner, P.J. Whelan, S. Ho, J. Tabak, M.J. O'Donovan. Spontaneous network activity transiently depresses synaptic transmission in the embryonic chick spinal cord. J. Neurosci. 19: 1999; 2102–2112
- B. Ferguson. Development of motor innervation of the chick following dorso-ventral limb bud rotations. J. Neurosci. 3: 1983; 1760–1772
- B.J. Fredette, L. Landmesser. A reevaluation of the role of innervation in primary and secondary myogenesis in developing chick muscles. Dev. Biol. 143: 1991; 19–35
- V. Hamburger. The development and innervation of transplanted limb primordia of chick embryos. J. Exp. Zool. 80: 1939; 347–389
- F. Helmbacher, S. Schneider-Maunoury, P. Topilko, L. Tiret, P. Charnay. Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development. 127: 2000; 3313–3324
- M. Hollyday, V. Hamburger. An autoradiographic study of the formation of the lateral motor column of the chick embryo. Brain Res. 132: 1977; 197–208
- M. Hollyday. Organization of motor pools in the chick lumbar lateral motor column. J. Comp. Neurol. 194: 1980; 143–170
- L.W. Jurata, J.B. Thomas, S.L. Pfaff. Transcriptional mechanisms in the development of motor control. Curr. Opin. Neurobiol. 10: 2000; 72–79
- A. Kania, R.L. Johnson, T.M. Jessell. Coordinate roles of LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell. 102: 2000; 161–173
- R.J. Keynes, R.V. Stirling, C. Stern, D. Summerbell. The specificity of motor innervation of the chick wing does not depend on the segmental origin of muscles. Development. 99: 1987; 565–575
- T. Kitsukawa, M. Shimizu, M. Sanbo, T. Hirata, M. Taniguchi, Y. Bekku, T. Yagi, H. Fujisawa. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron. 19: 1997; 995–1005
- C. Lance-Jones. The effect of somite manipulation on the development of motoneuron projection patterns in the embryonic chick hindlimb. Dev. Biol. 126: 1988; 408–419
- C. Lance-Jones, M. Dias. The influence of presumptive limb connective tissue on motoneuron axon guidance. Dev. Biol. 143: 1991; 93–110
- C. Lance-Jones, L. Landmesser. Motoneuron projection patterns in the chick hind limb following early partial reversals of the spinal cord. J. Physiol. (Lond.). 302: 1980; 581–602
- C. Lance-Jones, L. Landmesser. Pathway selection by embryonic chick lumbosacral motoneurons during normal development. Proc. R. Soc. Lond. B. 214: 1981; 1–18
- C. Lance-Jones, L. Landmesser. Pathway selection by embryonic chick motoneurons in an experimentally altered environment. Proc. R. Soc. Lond. B. 214: 1981; 119–152
- L.T. Landmesser, M.J. O'Donovan. The activation patterns of embryonic chick motoneurons projecting to inappropriate muscles. J. Physiol. Lond. 347: 1984; 189–204
- L. Landmesser. The distribution of motoneurons supplying chick hindlimb muscles. J. Physiol. Lond. 284: 1978; 371–389
- L. Landmesser. the development of motor projection patterns in the embryonic chick hindlimb. J. Physiol. Lond. 284: 1978; 391–414
- M. Lee, M.J. O'Donovan. Organization of hindlimb muscle afferent projections to lumbosacral motoneurons in the chick embryo. J. Neurosci. 11: 1991; 2564–2573
- J.H. Lin, T. Saito, D.J. Anderson, C. Lance-Jones, T.M. Jessell, S. Arber. Functionally related motor neuron pool and sensory afferent subtypes defined by coordinate ETS gene expression. Cell. 95: 1998; 393–402
- M.P. Matise, C. Lance Jones. A critical period for the specification of motor pools in the chick embryo. Development. 122: 1996; 659–669
- S.C. Mears, E. nd Frank. Formation of specific synaptic connections between muscle spindle afferents and motoenruons in the mouse. J. Neurosci. 17: 1997; 3128–3195
- L.D. Milner, L.T. Landmesser. Cholinergic and GABAergic inputs drive patterned spontaneous motonneuron activity before target contact. J. Neurosci. 19: 1999; 3007–3022
- L.D. Milner, V.F. Rafuse, L.T. Landmesser. Selective fasciculation and divergent pathfinding decisions of embryonic chick motor axons projecting to fast and slow muscle regions. J. Neurosci. 18: 1998; 3297–3313
- M.J. O'Donovan. Motor activity in the isolated spinal cord of the chick embryo: synaptic drive and firing pattern of single motoneurons. J. Neurosci. 9: 1989; 943–958
- A.A. Penn, P.A. Riquelme, M.B. Feller, C.J. Shatz. Competition in retinogeniculate patterning driven by spontaneous activity. Science. 279: 1998; 2108–2112
- K. Phelan, M. Hollyday. Axon guidance in muscleless chick wings: the role of muscle cells in motoneuron pathway selection and muscle nerve formation. J. Neurosci. 10: 1990; 2699–2716
- V.F. Rafuse, L.D. Milner, L.T. Landmesser. Selective innervation of fast and slow muscle regions during early chick neuromuscular development. J. Neurosci. 16: 1996; 6864–6877
- H. Roelink, A. Augsberger, J. Heemkerk, V. Korzh, S. Norlin, A. Ruiz i Atalba, Y. Tanabe, M. Placzek, T. Edlund, T.M. Jessell. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notocord. Cell. 76: 1994; 761–775
- K. Sharma, A.E. Leonard, K. Lettieri, S.L. Pfaff. Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature. 406: 2000; 515–519
- S. Sockanathan, T.M. Jessell. Motor neuron-derived retinoid signaling specifies the subtype identity of motoneurons. Cell. 94: 1998; 503–514
- D. Summerbell, R.V. Stirling. The innervation of dorsoventrally reversed chick wings: evidence that motor axons do not actively seek out their appropriate targets. J. Embryol. Exp. Morph. 61: 1981; 233–247
- J. Tang, U. Rutishauser, L. Landmesser. Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron. 13: 1994; 405–414
- M. Tessier-Lavigne, C.S. Goodman. The molecular biology of axon guidance. Science. 274: 1996; 1123–1132
- J. Thaler, K. Harrison, K. Sharma, K. Lettieri, J. Kehrl, S.L. Pfaff. Active supresssion of inteneuron programs within developing motor neurons revealed by analysis of homeodomain factor Hb9. Neuron. 23: 1999; 675–687
- W.J. Thompson, L.C. Soileau, R.J. Balice-Gordon, L.A. Sutton. Selective innervation of types of fibers in developing rat muscles. J. Exp. Biol. 132: 1987; 249–263
- T. Tsuchida, M. Ensini, S.B. Morton, M. Baldassare, T. Edlund, T.M. Jessell, S.L. Pfaff. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell. 79: 1994; 957–970
- M.W. Vogel. Activation patterns of embryonic chick lumbosacral motoneurons following large spinal cord reversals. J. Physiol. Lond. 389: 1987; 491–512
- V. Whitelaw, M. Hollyday. Neural pathway constraints in the motor innervation of the chick hindlimb following dorsoventral rotations of distal limb segments. J. Neurosci. 3: 1983; 1226–1233