Contact-mediated mechanisms of motor axon segmentation

Robert A. Oakley, Kathryn Tosney

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

In the chick embryo, the segmental pattern of motor outgrowth depends on guidance cues provided by sclerotome cells. Motor axons preferentially invade the anterior sclerotome but avoid the posterior sclerotome. To determine how motor growth cone motility is influenced by these cells, we used videomicroscopy to analyze the behavior of motor growth cones as they confronted identified sclerotome cells in vitro. After contact, motor growth cones invariably avoided posterior sclerotome cells by either branching or turning. Both types of avoidance behavior were initiated by a local inhibition of veil protrusion: veils failed to progress along the contacting filopodia. This inhibition was specific to veils since contact failed to alter the number of filopodia protruded. Moreover, motor growth cones turned away from posterior cells despite more persistent filopodial contacts with these cells than with the laminin substratum. In no case did contact with posterior cells cause a complete loss of growth cone motility or a complete collapse of growth cone structure. In contrast, motor growth cones exhibited a selective affinity for anterior cells, preferring the surfaces of these cells to the laminin substratum. Contact with anterior cells stimulated a generalized increase in protrusive activity: contact caused a net increase in the extension of veils and filopodia both locally and at sites distant from the site of contact. Contact also elicited a localized thickening of contacting processes, suggesting that contact with anterior cells promotes neunte consolidation. This behavior of motor growth cones in vitro suggests that both an inhibition of veil formation by posterior cells and an enhancement of motility and axon consolidation by anterior cells contribute to the preferential advance of motor axons into anterior sclerotome in vivo. We suggest that patterned outgrowth results from the juxtaposition of two contrasting environments that differentially influence growth cone motility.

Original languageEnglish
Pages (from-to)3773-3792
Number of pages20
JournalJournal of Neuroscience
Volume13
Issue number9
StatePublished - Dec 1 1993
Externally publishedYes

Fingerprint

Growth Cones
Axons
Pseudopodia
Laminin
Avoidance Learning
Video Microscopy
Chick Embryo
Cell Movement
Cues

Keywords

  • Axon guidance
  • Cell motility
  • Growth cones
  • Inhibition
  • Motoneurons
  • Segmentation

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Contact-mediated mechanisms of motor axon segmentation. / Oakley, Robert A.; Tosney, Kathryn.

In: Journal of Neuroscience, Vol. 13, No. 9, 01.12.1993, p. 3773-3792.

Research output: Contribution to journalArticle

Oakley, Robert A. ; Tosney, Kathryn. / Contact-mediated mechanisms of motor axon segmentation. In: Journal of Neuroscience. 1993 ; Vol. 13, No. 9. pp. 3773-3792.
@article{b9a197e5084f440fb15799827a910566,
title = "Contact-mediated mechanisms of motor axon segmentation",
abstract = "In the chick embryo, the segmental pattern of motor outgrowth depends on guidance cues provided by sclerotome cells. Motor axons preferentially invade the anterior sclerotome but avoid the posterior sclerotome. To determine how motor growth cone motility is influenced by these cells, we used videomicroscopy to analyze the behavior of motor growth cones as they confronted identified sclerotome cells in vitro. After contact, motor growth cones invariably avoided posterior sclerotome cells by either branching or turning. Both types of avoidance behavior were initiated by a local inhibition of veil protrusion: veils failed to progress along the contacting filopodia. This inhibition was specific to veils since contact failed to alter the number of filopodia protruded. Moreover, motor growth cones turned away from posterior cells despite more persistent filopodial contacts with these cells than with the laminin substratum. In no case did contact with posterior cells cause a complete loss of growth cone motility or a complete collapse of growth cone structure. In contrast, motor growth cones exhibited a selective affinity for anterior cells, preferring the surfaces of these cells to the laminin substratum. Contact with anterior cells stimulated a generalized increase in protrusive activity: contact caused a net increase in the extension of veils and filopodia both locally and at sites distant from the site of contact. Contact also elicited a localized thickening of contacting processes, suggesting that contact with anterior cells promotes neunte consolidation. This behavior of motor growth cones in vitro suggests that both an inhibition of veil formation by posterior cells and an enhancement of motility and axon consolidation by anterior cells contribute to the preferential advance of motor axons into anterior sclerotome in vivo. We suggest that patterned outgrowth results from the juxtaposition of two contrasting environments that differentially influence growth cone motility.",
keywords = "Axon guidance, Cell motility, Growth cones, Inhibition, Motoneurons, Segmentation",
author = "Oakley, {Robert A.} and Kathryn Tosney",
year = "1993",
month = "12",
day = "1",
language = "English",
volume = "13",
pages = "3773--3792",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "9",

}

TY - JOUR

T1 - Contact-mediated mechanisms of motor axon segmentation

AU - Oakley, Robert A.

AU - Tosney, Kathryn

PY - 1993/12/1

Y1 - 1993/12/1

N2 - In the chick embryo, the segmental pattern of motor outgrowth depends on guidance cues provided by sclerotome cells. Motor axons preferentially invade the anterior sclerotome but avoid the posterior sclerotome. To determine how motor growth cone motility is influenced by these cells, we used videomicroscopy to analyze the behavior of motor growth cones as they confronted identified sclerotome cells in vitro. After contact, motor growth cones invariably avoided posterior sclerotome cells by either branching or turning. Both types of avoidance behavior were initiated by a local inhibition of veil protrusion: veils failed to progress along the contacting filopodia. This inhibition was specific to veils since contact failed to alter the number of filopodia protruded. Moreover, motor growth cones turned away from posterior cells despite more persistent filopodial contacts with these cells than with the laminin substratum. In no case did contact with posterior cells cause a complete loss of growth cone motility or a complete collapse of growth cone structure. In contrast, motor growth cones exhibited a selective affinity for anterior cells, preferring the surfaces of these cells to the laminin substratum. Contact with anterior cells stimulated a generalized increase in protrusive activity: contact caused a net increase in the extension of veils and filopodia both locally and at sites distant from the site of contact. Contact also elicited a localized thickening of contacting processes, suggesting that contact with anterior cells promotes neunte consolidation. This behavior of motor growth cones in vitro suggests that both an inhibition of veil formation by posterior cells and an enhancement of motility and axon consolidation by anterior cells contribute to the preferential advance of motor axons into anterior sclerotome in vivo. We suggest that patterned outgrowth results from the juxtaposition of two contrasting environments that differentially influence growth cone motility.

AB - In the chick embryo, the segmental pattern of motor outgrowth depends on guidance cues provided by sclerotome cells. Motor axons preferentially invade the anterior sclerotome but avoid the posterior sclerotome. To determine how motor growth cone motility is influenced by these cells, we used videomicroscopy to analyze the behavior of motor growth cones as they confronted identified sclerotome cells in vitro. After contact, motor growth cones invariably avoided posterior sclerotome cells by either branching or turning. Both types of avoidance behavior were initiated by a local inhibition of veil protrusion: veils failed to progress along the contacting filopodia. This inhibition was specific to veils since contact failed to alter the number of filopodia protruded. Moreover, motor growth cones turned away from posterior cells despite more persistent filopodial contacts with these cells than with the laminin substratum. In no case did contact with posterior cells cause a complete loss of growth cone motility or a complete collapse of growth cone structure. In contrast, motor growth cones exhibited a selective affinity for anterior cells, preferring the surfaces of these cells to the laminin substratum. Contact with anterior cells stimulated a generalized increase in protrusive activity: contact caused a net increase in the extension of veils and filopodia both locally and at sites distant from the site of contact. Contact also elicited a localized thickening of contacting processes, suggesting that contact with anterior cells promotes neunte consolidation. This behavior of motor growth cones in vitro suggests that both an inhibition of veil formation by posterior cells and an enhancement of motility and axon consolidation by anterior cells contribute to the preferential advance of motor axons into anterior sclerotome in vivo. We suggest that patterned outgrowth results from the juxtaposition of two contrasting environments that differentially influence growth cone motility.

KW - Axon guidance

KW - Cell motility

KW - Growth cones

KW - Inhibition

KW - Motoneurons

KW - Segmentation

UR - http://www.scopus.com/inward/record.url?scp=0027265529&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0027265529&partnerID=8YFLogxK

M3 - Article

C2 - 8366345

AN - SCOPUS:0027265529

VL - 13

SP - 3773

EP - 3792

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 9

ER -