The spatial relationships among cutaneous, muscle sensory and motoneuron axone during development of the chick hindlimb

Marcia Honig, Priscilla A. Frase, Suzanne J. Camilli

Research output: Contribution to journalArticle

47 Citations (Scopus)

Abstract

Previous studies have suggested that interactions with other axons are important in sensory axon pathfinding in the developing chick hindlimb. Yet the nature of these interactions remains unknown, in part because information about the spatial relationships among the different kinds of axons is lacking. To obtain this information, we combined retrograde axonal tracing with an immunofluorescent labelling approach that distinguishes between sensory and motoneuron axons. This allowed us to follow the trajectories of sensory axons having a known destination, while also identifying their neighbors. We found that as sensory and motoneuron axons meet in the spinal nerves and travel into the limb, sensory axons remain bundled together. The large bundles that are present proximally gradually split into smaller bundles as the axons course distally in the spinal nerves; more distally, some bundles join to again form large bundles. Younger, later-growing sensory axons appear to grow primarily along bundles of older sensory axons that grew out earlier. Starting from very proximal levels, axons projecting along an individual cutaneous nerve are found together in bundles that are situated in characteristic regions of each spinal nerve. Some of these bundles are initially interspersed with bundles of axons projecting along other nerves, thereby indicating that the initial position of a cutaneous axon in the spinal nerves does not strictly determine its subsequent trajectory. As they travel distally, bundles of axons projecting along one cutaneous nerve gradually join one another, becoming increasingly separated from axons having different destinations. In contrast, muscle sensory axons are situated adjacent to motoneuron axons innervating the same muscle for much of their course. This suggests that muscle sensory axons may be guided to the appropriate muscles by fasciculating along motoneuron axons. Taken together, the results show that sensory axons projecting along different nerves are different from one another and respond to cues in their environment to navigate through the spinal nerves and plexus. Thus, sensory neurons must be intrinsically specified with respect to their peripheral targets. Sensory axons appear to respond differentially to the axons they encounter, segregating from axons that project along different nerves and often growing with axons destined for the same nerve, suggesting that fasciculation may aid pathfinding.

Original languageEnglish (US)
Pages (from-to)995-1004
Number of pages10
JournalDevelopment
Volume125
Issue number6
StatePublished - 1998

Fingerprint

Motor Neurons
Hindlimb
Axons
Muscles
Skin
Spinal Nerves
Fasciculation

All Science Journal Classification (ASJC) codes

  • Anatomy
  • Cell Biology

Cite this

The spatial relationships among cutaneous, muscle sensory and motoneuron axone during development of the chick hindlimb. / Honig, Marcia; Frase, Priscilla A.; Camilli, Suzanne J.

In: Development, Vol. 125, No. 6, 1998, p. 995-1004.

Research output: Contribution to journalArticle

@article{5812d67717474b6dbf53c69e762f0593,
title = "The spatial relationships among cutaneous, muscle sensory and motoneuron axone during development of the chick hindlimb",
abstract = "Previous studies have suggested that interactions with other axons are important in sensory axon pathfinding in the developing chick hindlimb. Yet the nature of these interactions remains unknown, in part because information about the spatial relationships among the different kinds of axons is lacking. To obtain this information, we combined retrograde axonal tracing with an immunofluorescent labelling approach that distinguishes between sensory and motoneuron axons. This allowed us to follow the trajectories of sensory axons having a known destination, while also identifying their neighbors. We found that as sensory and motoneuron axons meet in the spinal nerves and travel into the limb, sensory axons remain bundled together. The large bundles that are present proximally gradually split into smaller bundles as the axons course distally in the spinal nerves; more distally, some bundles join to again form large bundles. Younger, later-growing sensory axons appear to grow primarily along bundles of older sensory axons that grew out earlier. Starting from very proximal levels, axons projecting along an individual cutaneous nerve are found together in bundles that are situated in characteristic regions of each spinal nerve. Some of these bundles are initially interspersed with bundles of axons projecting along other nerves, thereby indicating that the initial position of a cutaneous axon in the spinal nerves does not strictly determine its subsequent trajectory. As they travel distally, bundles of axons projecting along one cutaneous nerve gradually join one another, becoming increasingly separated from axons having different destinations. In contrast, muscle sensory axons are situated adjacent to motoneuron axons innervating the same muscle for much of their course. This suggests that muscle sensory axons may be guided to the appropriate muscles by fasciculating along motoneuron axons. Taken together, the results show that sensory axons projecting along different nerves are different from one another and respond to cues in their environment to navigate through the spinal nerves and plexus. Thus, sensory neurons must be intrinsically specified with respect to their peripheral targets. Sensory axons appear to respond differentially to the axons they encounter, segregating from axons that project along different nerves and often growing with axons destined for the same nerve, suggesting that fasciculation may aid pathfinding.",
author = "Marcia Honig and Frase, {Priscilla A.} and Camilli, {Suzanne J.}",
year = "1998",
language = "English (US)",
volume = "125",
pages = "995--1004",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "6",

}

TY - JOUR

T1 - The spatial relationships among cutaneous, muscle sensory and motoneuron axone during development of the chick hindlimb

AU - Honig, Marcia

AU - Frase, Priscilla A.

AU - Camilli, Suzanne J.

PY - 1998

Y1 - 1998

N2 - Previous studies have suggested that interactions with other axons are important in sensory axon pathfinding in the developing chick hindlimb. Yet the nature of these interactions remains unknown, in part because information about the spatial relationships among the different kinds of axons is lacking. To obtain this information, we combined retrograde axonal tracing with an immunofluorescent labelling approach that distinguishes between sensory and motoneuron axons. This allowed us to follow the trajectories of sensory axons having a known destination, while also identifying their neighbors. We found that as sensory and motoneuron axons meet in the spinal nerves and travel into the limb, sensory axons remain bundled together. The large bundles that are present proximally gradually split into smaller bundles as the axons course distally in the spinal nerves; more distally, some bundles join to again form large bundles. Younger, later-growing sensory axons appear to grow primarily along bundles of older sensory axons that grew out earlier. Starting from very proximal levels, axons projecting along an individual cutaneous nerve are found together in bundles that are situated in characteristic regions of each spinal nerve. Some of these bundles are initially interspersed with bundles of axons projecting along other nerves, thereby indicating that the initial position of a cutaneous axon in the spinal nerves does not strictly determine its subsequent trajectory. As they travel distally, bundles of axons projecting along one cutaneous nerve gradually join one another, becoming increasingly separated from axons having different destinations. In contrast, muscle sensory axons are situated adjacent to motoneuron axons innervating the same muscle for much of their course. This suggests that muscle sensory axons may be guided to the appropriate muscles by fasciculating along motoneuron axons. Taken together, the results show that sensory axons projecting along different nerves are different from one another and respond to cues in their environment to navigate through the spinal nerves and plexus. Thus, sensory neurons must be intrinsically specified with respect to their peripheral targets. Sensory axons appear to respond differentially to the axons they encounter, segregating from axons that project along different nerves and often growing with axons destined for the same nerve, suggesting that fasciculation may aid pathfinding.

AB - Previous studies have suggested that interactions with other axons are important in sensory axon pathfinding in the developing chick hindlimb. Yet the nature of these interactions remains unknown, in part because information about the spatial relationships among the different kinds of axons is lacking. To obtain this information, we combined retrograde axonal tracing with an immunofluorescent labelling approach that distinguishes between sensory and motoneuron axons. This allowed us to follow the trajectories of sensory axons having a known destination, while also identifying their neighbors. We found that as sensory and motoneuron axons meet in the spinal nerves and travel into the limb, sensory axons remain bundled together. The large bundles that are present proximally gradually split into smaller bundles as the axons course distally in the spinal nerves; more distally, some bundles join to again form large bundles. Younger, later-growing sensory axons appear to grow primarily along bundles of older sensory axons that grew out earlier. Starting from very proximal levels, axons projecting along an individual cutaneous nerve are found together in bundles that are situated in characteristic regions of each spinal nerve. Some of these bundles are initially interspersed with bundles of axons projecting along other nerves, thereby indicating that the initial position of a cutaneous axon in the spinal nerves does not strictly determine its subsequent trajectory. As they travel distally, bundles of axons projecting along one cutaneous nerve gradually join one another, becoming increasingly separated from axons having different destinations. In contrast, muscle sensory axons are situated adjacent to motoneuron axons innervating the same muscle for much of their course. This suggests that muscle sensory axons may be guided to the appropriate muscles by fasciculating along motoneuron axons. Taken together, the results show that sensory axons projecting along different nerves are different from one another and respond to cues in their environment to navigate through the spinal nerves and plexus. Thus, sensory neurons must be intrinsically specified with respect to their peripheral targets. Sensory axons appear to respond differentially to the axons they encounter, segregating from axons that project along different nerves and often growing with axons destined for the same nerve, suggesting that fasciculation may aid pathfinding.

UR - http://www.scopus.com/inward/record.url?scp=0031953280&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0031953280&partnerID=8YFLogxK

M3 - Article

VL - 125

SP - 995

EP - 1004

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 6

ER -