Cercal sensory development following laser microlesions of embryonic apical cells in Acheta domesticus

Edwards, JS; Sw, Chen; Berns, Michael W.

doi:10.1523/jneurosci.01-03-00250.1981

Cited by 60 publications

(13 citation statements)

References 8 publications

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“…Guidance by heterologous axons has been reported for other developing systems (e.g., Edwards et al, 1981;Bentley and Keshishian, 1982;Ho and Goodman, 1982;Moody and Heaton, 1983a,b), with destruction of the guide neurons leading to aberrant projections by the follower axons (Edwards et al, 1981;Moody and Heaton, 1983a;Raper et al, 1984).…”

Section: Discussionmentioning

confidence: 84%

Skin sensory innervation patterns in embryonic chick hindlimb following dorsal root ganglion reversals

Scott

1986

J. Neurobiol.

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During embryonic development skin sensory neurons in lumbosacral dorsal root ganglia (DRGs) establish their dermatomes and axonal projections in a precise, orderly fashion in the chick. To investigate mechanisms responsible for this specific outgrowth, the rostrocaudal order of DRGs T7-LS3 was reversed by rotating the corresponding segments of neural crest, either alone or together with the underlying neural tube in St.15-16 embryos. The resulting skin sensory innervation patterns, mapped physiologically or anatomically at St.29-40, differed between the two experimental groups. Following neural tube rotations DRGs tended to establish innervation patterns that were consonant with their original position in the embryo. Axons from these rotated DRGs generally projected into the appropriate pathways and innervated the appropriate region of skin. Neural crest rotations left the ventral neural tube (including the motor neuron precursors) largely intact. In this case rotated DRGs tended to establish innervation patterns in accordance with their new position in the embryo, almost as if no rotation had been made. These results cannot be explained solely by the inherent specificity of sensory neurons. Instead, the results are largely consistent with the suggestion (Honig et al., 1986; Landmesser and Honig, 1986) that motor axons can direct the outgrowth of sensory axons and thereby influence the establishment of sensory innervation patterns. Other mechanisms that may also affect the development of sensory innervation patterns are discussed.

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Section: Discussionmentioning

confidence: 84%

Skin sensory innervation patterns in embryonic chick hindlimb following dorsal root ganglion reversals

Scott

1986

J. Neurobiol.

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“…For example, peripheral axonal pathways in the antenna, the leg, and the cerci are established by pairs of early differentiating axons called pioneers, which extend along stereotyped pathways into the CNS (Bate 1976;Edwards 1977;Keshishian 1980). These pioneers are necessary for the normal pathfinding of subsequently growing axons (Edwards et al 1981;Klose and Bentley 1989). Reproducible deflections in pioneer trajectories within the leg correlate with the locations of specific early differentiating sensory cells, and deletion of these cells induce abnormal pioneer pathfinding (Bentley and Caudy 1983).…”

Section: Pioneer Neuronsmentioning

confidence: 99%

“…Their ablation often perturbs the guidance of subsequent follower axons, either by delaying or misrouting them, but does not necessarily prevent followers from extending and locating their appropriate targets (Durbin 1987;Edwards et al 1981;Pike et al 1992;Hutter 2003). As a rule pioneers contribute guidance information and a suitable substratum for extension to their followers, but only in rare cases are they essential for followers to reach their targets (Whitlock and Westerfield 1998;Pittman et al 2008).…”

Section: Pioneer Neuronsmentioning

confidence: 99%

Cellular Strategies of Axonal Pathfinding

Raper

Mason

2010

Cold Spring Harbor Perspectives in Biology

157

130

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Axons follow highly stereotyped and reproducible trajectories to their targets. In this review we address the properties of the first pioneer neurons to grow in the developing nervous system and what has been learned over the past several decades about the extracellular and cell surface substrata on which axons grow. We then discuss the types of guidance cues and their receptors that influence axon extension, what determines where cues are expressed, and how axons respond to the cues they encounter in their environment.T his article provides an overview of how growth cones respond to the cellular substrata and molecular cues they encounter as they extend through the developing nervous system. It elaborates on the primer by Kolodkin and TessierLavigne (2010) and touches on many of the topics covered in greater detail in the articles that follow. The first sections describe how axons extend in a directed manner, the substrata on which they grow, interactions between pioneer and follower axons, and growth cone behaviors in emerging tracts and at decision points. The subsequent sections discuss examples of specific cues, their distributions, how their distributions are determined, and how growth cones integrate multiple cues during pathfinding. AXONS EXTEND IN VIVO IN A DIRECTED MANNERThe first person to visualize the growing tips of axons, Ramon y Cajal, recognized that axons for the most part grow very efficiently towards their ultimate targets. He was a strong advocate for axons finding their way in response to chemotactic cues:"If one admits that neuroblasts are endowed with chemotactic properties, then one might also imagine that they are capable of ameboid movements, initiated by factors secreted from epithelial, neural, or mesodermal elements. As a result, their processes may be oriented in the direction of chemical gradients, and thus guided to the secreting cells" (Ramon y Cajal 1892; trans. English, 1995).This surprisingly modern outlook emphasizing directed guidance was temporarily derailed by the views of Weiss during the 1920s and 1930s. He first argued that functional specificity did not arise as a consequence of specific axonal connections (Weiss 1936), and later argued that nonspecific mechanical guidance cues play a predominant role in guiding axons and organizing them into nerves and tracts

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“…This is possible because of the spectral purity and short exposure time of a laser beam that is focused to a diffraction-limited spot by a high numerical aperture (NA ¼ 1.3 -1.4) microscope objective [1 -3]. Such systems have been used to perform nanosurgery on neurons in organisms such as Caenorhabditis elegans [4,5] and cricket larvae [6], as well as in individual neurons growing in culture [7,8]. Through precise control of the laser parameters, it is possible to cause either complete transection of neurites extending from neurons in culture or localized subaxotomy damage from which the neurites recover [8].…”

Section: Introductionmentioning

confidence: 99%

Neuronal growth cones respond to laser-induced axonal damage

Mohanty

Gomez-Godinez

et al. 2011

J. R. Soc. Interface.

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Although it is well known that damage to neurons results in release of substances that inhibit axonal growth, release of chemical signals from damaged axons that attract axon growth cones has not been observed. In this study, a 532 nm 12 ns laser was focused to a diffraction-limited spot to produce site-specific damage to single goldfish axons in vitro. The axons underwent a localized decrease in thickness ('thinning') within seconds. Analysis by fluorescence and transmission electron microscopy indicated that there was no gross rupture of the cell membrane. Mitochondrial transport along the axonal cytoskeleton immediately stopped at the damage site, but recovered over several minutes. Within seconds of damage nearby growth cones extended filopodia towards the injury and were often observed to contact the damaged site. Turning of the growth cone towards the injured axon also was observed. Repair of the laser-induced damage was evidenced by recovery of the axon thickness as well as restoration of mitochondrial movement. We describe a new process of growth cone response to damaged axons. This has been possible through the interface of optics (laser subcellular surgery), fluorescence and electron microscopy, and a goldfish retinal ganglion cell culture model.

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Cercal sensory development following laser microlesions of embryonic apical cells in Acheta domesticus

Cited by 60 publications

References 8 publications

Skin sensory innervation patterns in embryonic chick hindlimb following dorsal root ganglion reversals

Skin sensory innervation patterns in embryonic chick hindlimb following dorsal root ganglion reversals

Cellular Strategies of Axonal Pathfinding

Neuronal growth cones respond to laser-induced axonal damage

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