The development of sensory projection patterns in embryonic chick hind limb.

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Abstract

1. The distribution within individual dorsal root ganglia (d.r.g.s) of sensory neurones projecting to different targets in the embryonic chick hind limb was determined using the retrograde transport of horseradish peroxidase (HRP). The segmental pattern of sensory neurone projections was also defined, using retrograde and orthograde HRP labelling and electrophysiological techniques, from the onset of axonal outgrowth into the limb until after the period of sensory cell death. 2. At stage (St.) 29‐30, shortly after initial axonal outgrowth into the limb, the large lateroventral neurones in the d.r.g.s projected both to skin and to muscle. At St. 36‐37, after cell death in the d.r.g.s, cells from both the lateroventral and mediodorsal populations projected both to skin and to muscle. Thus these two cell populations do not correspond to cutaneous and proprioceptive afferents, respectively. 3. The cells projecting along individual cutaneous nerves or to individual muscles were always widely distributed throughout the ganglia. Thus, sensory neurones cannot be specified to project to particular peripheral targets as a result of their position in the d.r.g. Nevertheless, small clusters of cells were frequently found to project along the same peripheral nerve. 4. Since there is a correlation between position in the d.r.g. and time of origin, neurones projecting to each target have a wide range of birthdates, and, therefore, sensory neurones cannot be specified as a result of their birthdate. 5. At St. 36‐38, after cell death, afferents to a given muscle or cutaneous nerve arise primarily from two or three adjacent segments out of the eight lumbosacral segments. For muscles these are the same segments that supply the motoneurones to that muscle. Each d.r.g. sends a characteristic proportion of axons down each of several peripheral nerves in a consistent and orderly pattern. 6. During initial outgrowth, the segmental projection pattern is similar to the pattern found in mature embryos. Thus, extensive projection ‘errors’ are not made and neither cell death nor retraction of axons is necessary for establishing the appropriate connectivity pattern. The majority of neurones do not send branches down more than one peripheral nerve. 7. Axons projecting to the same target are initially dispersed in the spinal nerves, and gradually segregate out in the plexus region, ultimately to form a separate nerve trunk. Axons projecting to different targets cross each other. Cutaneous and muscle nerves first form at the same stages. Therefore, the particular pathways axons take do not depend in any simple way on either axonal position in the plexus or time of arrival at the base of the limb. Simple timed outgrowth mechanisms and models in which axons maintain constant topographical relationships with each other therefore cannot generate the observed projection pattern. 8...

Original languageEnglish (US)
Pages (from-to)175-202
Number of pages28
JournalThe Journal of Physiology
Volume330
Issue number1
DOIs
StatePublished - Sep 1 1982

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Extremities
Axons
Muscles
Sensory Receptor Cells
Skin
Cell Death
Peripheral Nerves
Horseradish Peroxidase
Neurons
Spinal Nerves
Spinal Ganglia
Motor Neurons
Ganglia
Population
Embryonic Structures

All Science Journal Classification (ASJC) codes

  • Physiology

Cite this

The development of sensory projection patterns in embryonic chick hind limb. / Honig, Marcia.

In: The Journal of Physiology, Vol. 330, No. 1, 01.09.1982, p. 175-202.

Research output: Contribution to journalArticle

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title = "The development of sensory projection patterns in embryonic chick hind limb.",
abstract = "1. The distribution within individual dorsal root ganglia (d.r.g.s) of sensory neurones projecting to different targets in the embryonic chick hind limb was determined using the retrograde transport of horseradish peroxidase (HRP). The segmental pattern of sensory neurone projections was also defined, using retrograde and orthograde HRP labelling and electrophysiological techniques, from the onset of axonal outgrowth into the limb until after the period of sensory cell death. 2. At stage (St.) 29‐30, shortly after initial axonal outgrowth into the limb, the large lateroventral neurones in the d.r.g.s projected both to skin and to muscle. At St. 36‐37, after cell death in the d.r.g.s, cells from both the lateroventral and mediodorsal populations projected both to skin and to muscle. Thus these two cell populations do not correspond to cutaneous and proprioceptive afferents, respectively. 3. The cells projecting along individual cutaneous nerves or to individual muscles were always widely distributed throughout the ganglia. Thus, sensory neurones cannot be specified to project to particular peripheral targets as a result of their position in the d.r.g. Nevertheless, small clusters of cells were frequently found to project along the same peripheral nerve. 4. Since there is a correlation between position in the d.r.g. and time of origin, neurones projecting to each target have a wide range of birthdates, and, therefore, sensory neurones cannot be specified as a result of their birthdate. 5. At St. 36‐38, after cell death, afferents to a given muscle or cutaneous nerve arise primarily from two or three adjacent segments out of the eight lumbosacral segments. For muscles these are the same segments that supply the motoneurones to that muscle. Each d.r.g. sends a characteristic proportion of axons down each of several peripheral nerves in a consistent and orderly pattern. 6. During initial outgrowth, the segmental projection pattern is similar to the pattern found in mature embryos. Thus, extensive projection ‘errors’ are not made and neither cell death nor retraction of axons is necessary for establishing the appropriate connectivity pattern. The majority of neurones do not send branches down more than one peripheral nerve. 7. Axons projecting to the same target are initially dispersed in the spinal nerves, and gradually segregate out in the plexus region, ultimately to form a separate nerve trunk. Axons projecting to different targets cross each other. Cutaneous and muscle nerves first form at the same stages. Therefore, the particular pathways axons take do not depend in any simple way on either axonal position in the plexus or time of arrival at the base of the limb. Simple timed outgrowth mechanisms and models in which axons maintain constant topographical relationships with each other therefore cannot generate the observed projection pattern. 8...",
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AB - 1. The distribution within individual dorsal root ganglia (d.r.g.s) of sensory neurones projecting to different targets in the embryonic chick hind limb was determined using the retrograde transport of horseradish peroxidase (HRP). The segmental pattern of sensory neurone projections was also defined, using retrograde and orthograde HRP labelling and electrophysiological techniques, from the onset of axonal outgrowth into the limb until after the period of sensory cell death. 2. At stage (St.) 29‐30, shortly after initial axonal outgrowth into the limb, the large lateroventral neurones in the d.r.g.s projected both to skin and to muscle. At St. 36‐37, after cell death in the d.r.g.s, cells from both the lateroventral and mediodorsal populations projected both to skin and to muscle. Thus these two cell populations do not correspond to cutaneous and proprioceptive afferents, respectively. 3. The cells projecting along individual cutaneous nerves or to individual muscles were always widely distributed throughout the ganglia. Thus, sensory neurones cannot be specified to project to particular peripheral targets as a result of their position in the d.r.g. Nevertheless, small clusters of cells were frequently found to project along the same peripheral nerve. 4. Since there is a correlation between position in the d.r.g. and time of origin, neurones projecting to each target have a wide range of birthdates, and, therefore, sensory neurones cannot be specified as a result of their birthdate. 5. At St. 36‐38, after cell death, afferents to a given muscle or cutaneous nerve arise primarily from two or three adjacent segments out of the eight lumbosacral segments. For muscles these are the same segments that supply the motoneurones to that muscle. Each d.r.g. sends a characteristic proportion of axons down each of several peripheral nerves in a consistent and orderly pattern. 6. During initial outgrowth, the segmental projection pattern is similar to the pattern found in mature embryos. Thus, extensive projection ‘errors’ are not made and neither cell death nor retraction of axons is necessary for establishing the appropriate connectivity pattern. The majority of neurones do not send branches down more than one peripheral nerve. 7. Axons projecting to the same target are initially dispersed in the spinal nerves, and gradually segregate out in the plexus region, ultimately to form a separate nerve trunk. Axons projecting to different targets cross each other. Cutaneous and muscle nerves first form at the same stages. Therefore, the particular pathways axons take do not depend in any simple way on either axonal position in the plexus or time of arrival at the base of the limb. Simple timed outgrowth mechanisms and models in which axons maintain constant topographical relationships with each other therefore cannot generate the observed projection pattern. 8...

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