Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: Anatomical aspects

O'Brien, Michael K.; Landmesser, Lynn T.; Oppenheim, Ronald W.

doi:10.1002/neu.480210207

Cited by 46 publications

(29 citation statements)

References 51 publications

(44 reference statements)

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“…This is not surprising, because thoracic spinal cord contains only medial motor column, but not LMC, motoneurons. Together, these findings are consistent with previous studies showing that the phenotype and target specificity of sensory neurons are more plastic than motoneurons (McMahon and Gibson, 1987;Wenner and Frank, 1995;Scott, 1999, 2002) and that innervation of limb muscles does not convert thoracic motoneurons to LMC neurons (O'Brien and Oppenheim, 1990;Turney et al, 2003).…”

Section: Regulation Of Er81 In Sensory Neurons and Thoracic Motoneuronssupporting

confidence: 92%

An Early Broad Competence of Motoneurons to ExpressER81Is Later Sculpted by the Periphery

Wang¹,

Scott²

2004

J. Neurosci.

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The ETS transcription factor ER81 is expressed in sensory neurons and motoneurons that innervate the adductor and femorotibialis muscles in chick hindlimb and is essential for the development of monosynaptic connections between these two populations of neurons. Neurons need a signal(s) from limb bud mesoderm to initiate ER81 expression. It is not known whether the mature expression pattern arises because adductor and femorotibialis motoneurons are uniquely competent to respond to peripheral signals and express ER81, or whether all motoneurons are competent to express ER81, but normally only adductor and femorotibialis motoneurons are exposed to the requisite activating signal. To investigate these possibilities, we examined ER81 expression in motoneurons that encountered limb tissue surgically mismatched with their target identity at stages after motor pool identities are established. We found that ER81 expression was not invariably linked to motor pool identity or target innervation and was more malleable in later-born femorotibialis motoneurons than in earlier-born adductor motoneurons. We also found that ER81 expression is regulated differently in sensory neurons and motoneurons. Most striking was the observation that motoneurons caudal to the normal adductor and femorotibialis pools could express ER81 when exposed to the appropriate peripheral signals, although this competence did not extend through the entire lumbosacral (LS) region. Thus, it appears that a prepattern of competence to express ER81 is established in early LS motoneurons, most likely in concert with their target identity, and that the expression domains of motoneurons are subsequently refined by peripheral signals at later stages.

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Section: Regulation Of Er81 In Sensory Neurons and Thoracic Motoneuronssupporting

confidence: 92%

An Early Broad Competence of Motoneurons to ExpressER81Is Later Sculpted by the Periphery

Wang¹,

Scott²

2004

J. Neurosci.

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“…at later stages a chemically-mediated mismatch between nerve and muscle involving cell-cell interactions and the loss of synaptic stability may result in an uncoupling that leads to the observed regression of both nerve and muscle. Alternatively, owing to differences in number or type, thoracic motoneurons may be unable to provide sufficient innervation or trophic support to sustain the development of the rapidly developing limb muscles during the last half of the incubation period (cf., O'Brien and Oppenheim, 1990). Another possibility that we do not favor, but cannot exclude, is that eventually limb muscles fail to provide appropriate trophic support for nonlimb motoneurons resulting in motoneuron regression which in turn leads to muscle degeneration.…”

Section: Discussionmentioning

confidence: 91%

Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: Functional aspects

1990

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SUMMARYFollowing heterotopic transplantation of the thoracic neural tube to the lumbar region on embryonic day (E) 2, the transplanted cord differentiates normally and estdblishes neuroanatomical connections with the host central nervous system and hindlimb muscles. Beginning on about E12, however, the neuromuscular system begins to undergo regressive changes resulting in motoneuron degeneration and muscle atrophy (O'Brien and Oppenheim, 1990). In the present paper, we have examined the development of neuromuscular function in thoracic transplant embryos from E6 to the time of hatching on E20-21. The onset of hindlimb movements and reflexes occurred a t the same time (E6-ES) in both control and thoracic transplant embryos. Further, both the nature (pattern) and frequency of these movements appeared normal in the thoracic transplants up to ElO-El2, after which there was a gradual and marked reduction in the frequency, and an alteration in the pattern, of both spontaneous and reflex-evoked hindlimb movements. After El6 normal movements were virtually absent in many of the thoracic transplant cases. By contrast, movements of the head, trunk and wings were normal in these embryos throughout the observation period. Hindlimbs innervated partly by the thoracic transplant and partly by remaining host lumbar cord did not exhibit the regressive changes in function after El0 that occurred in hindlimbs innervated exclusively by the thoracic transplant. EMG recordings from specific hindlimb muscles innervated solely by thoracic motoneurons demonstrated that the activation pattern of both flexon and extensors was similar to the repetitive pattern observed in normal thoracically innervated intercostal muscles (i.e., extensorlike). Muscles did not show distinguishable EMG burst patterns with inhibitory periods as do control lumbar innervated muscles. W e conclude that the development of the pattern generating circuitry in the transplanted thoracic cord was similar to normal thoracic cord and thus appeared to be uninfluenced by having contacted the foreign hindlimb muscle targets early in development. Activity blockade with curare from E6 to El4 suppressed the loss of motoneurons that occurs in the thoracic transplant after E10. Thus, the abnormal thoracic-like activation pattern of thoracically innervated hindlimbs may be a critical signal in the initiation of the neuromuscular regression that occurs after El0 in these preparations. Finally, although the innervation and formation of neuromuscular endplates in thoracic transplants appeared normal up to E12, by El4 both the intramuscular nerves and the endplates exhibited signs of degeneration and regression. Thoracic motoneurons are initially able to innervate and functionally activate hindlimb muscles in a manner similar to that of thoracically innervated intercostal muscles. Eventually, however, even this abnormal activation pattern disappears and the entire neuromuscular system breaks down, As described in more detail in the preceding cornhave used heterotopic transplantation ...

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“…Manipulations of motor neuronal positioning, through inversions or rostrocaudal shifts of the neural tube (Lance-Jones and Landmesser, 1980Landmesser, , 1981bO'Brien and Oppenheim, 1989), or of limb targets, through transplant of supernumerary limbs Whitelaw and Hollyday, 1983a), limb bud rotations (Ferns and Hollyday, 1993;Whitelaw and Hollyday, 1983b) and limb bud ablations (Shorrey, 1909;Barron, 1948;Hamburger and O'Keefe, 1944;Whitelaw and Hollyday, 1983c;Tosney and Landmesser, 1984), have revealed that there are both permissive and instructive signals in the periphery that motor axons use to be guided to their correct targets. These experiments have yielded the model that local guidepost signals within the limb mesenchyme are used by motor axons to navigate.…”

Section: Specification Of Motor Axon Pathfindingmentioning

confidence: 98%

The generation and diversification of spinal motor neurons: signals and responses

Price

Briscoe²

2004

Mechanisms of Development

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Motor neurons are probably the best characterised neuronal class in the vertebrate central nervous system and have become a paradigm for understanding the mechanisms that control the development of vertebrate neurons. For many investigators working on this problem the chick embryo is the model system of choice and from these studies a picture of the steps involved in motor neuron generation has begun to emerge. These findings suggest that motor neuron generation is shaped by extracellular signals that regulate intrinsic, cell-autonomous determinants at sequential steps during development. The chick embryo has played a prominent role in identifying the sources of these signals, defining their molecular identities and determining the cell intrinsic programs they regulate.

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Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: Anatomical aspects

Cited by 46 publications

References 51 publications

An Early Broad Competence of Motoneurons to ExpressER81Is Later Sculpted by the Periphery

An Early Broad Competence of Motoneurons to ExpressER81Is Later Sculpted by the Periphery

Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: Functional aspects

The generation and diversification of spinal motor neurons: signals and responses

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