A hierarchy of determining factors controls motoneuron innervation - Experimental studies on the development of the plantaris muscle (PL) in avian chimeras

M. Grim, K. Nensa, B. Christ, H. J. Jacob, Kathryn Tosney

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Quail leg buds were grafted in place of chick leg buds or chick wing buds and vice versa at stages 18 to 21 after colonization by muscle precursor cells had been completed. Motor endplate pattern in the plantaris muscle of the grafts was analyzed before hatching by means of esterase and acetylcholinesterase staining techniques. Muscle fibre types were made visual using the myosin ATPase reaction. Investigations are based on the species-specific endplate pattern of the plantaris muscle: multiply innervated fibres in the chick and focally innervated fibres in the quail. Muscle pieces isolated from the adjacent medial gastrocnemius muscle of the grafted legs were histologically examined to judge their species-specific composition. Horseradish peroxidase was injected into the plantaris muscles of both the grafted and the opposite leg as well as in the plantaris muscle of normal quail embryos, in order to be sure that the plantaris muscle of the graft is innervated by appropriate motoneurons. This procedural design offers for the first time a possibility to test experimentally the influences of motoneurons on endplate pattern formation under conditions corresponding to those in normal ontogenesis. It is shown that such appropriate motoneurons of one species which project to the plantaris muscle of the other species dictate the endplate pattern. When the plantaris muscle is innervated by inappropriate motoneurons, the endplate pattern inherent in the muscle primordium itself becomes realized. A sequence of hierarchically acting factors is proposed to bring different results in line. According to this, the neuronally set programme has priority compared with that set in the muscle. This is true for the normal development and might generate the high neuro-muscular specificity. If under experimental conditions the neuronal programme and the peripheral programme differ, the axons and muscle fibres selectively interact with respect to their inherent characteristics and the muscle-specific programme becomes expressed. If there is a lack of a certain axon type, muscle fibres might become innervated by non-corresponding motoneurons which alter the muscle fibre type.

Original languageEnglish
Pages (from-to)179-189
Number of pages11
JournalAnatomy and Embryology
Volume180
Issue number2
DOIs
StatePublished - Jul 1 1989
Externally publishedYes

Fingerprint

Motor Neurons
Skeletal Muscle
Muscles
Quail
Leg
Axons
Motor Endplate
Transplants
Myoblasts
Esterases
Horseradish Peroxidase
Myosins
Acetylcholinesterase
Embryonic Structures
Staining and Labeling

Keywords

  • Endplate pattern formation
  • Hierarchy of controlling factors
  • Muscle fibre types
  • Muscle innervation
  • Plantaris muscle
  • Quail-chick chimeras

ASJC Scopus subject areas

  • Embryology
  • Anatomy
  • Developmental Biology
  • Cell Biology

Cite this

A hierarchy of determining factors controls motoneuron innervation - Experimental studies on the development of the plantaris muscle (PL) in avian chimeras. / Grim, M.; Nensa, K.; Christ, B.; Jacob, H. J.; Tosney, Kathryn.

In: Anatomy and Embryology, Vol. 180, No. 2, 01.07.1989, p. 179-189.

Research output: Contribution to journalArticle

@article{78969a182f324dd5b5ec51933e3bfa69,
title = "A hierarchy of determining factors controls motoneuron innervation - Experimental studies on the development of the plantaris muscle (PL) in avian chimeras",
abstract = "Quail leg buds were grafted in place of chick leg buds or chick wing buds and vice versa at stages 18 to 21 after colonization by muscle precursor cells had been completed. Motor endplate pattern in the plantaris muscle of the grafts was analyzed before hatching by means of esterase and acetylcholinesterase staining techniques. Muscle fibre types were made visual using the myosin ATPase reaction. Investigations are based on the species-specific endplate pattern of the plantaris muscle: multiply innervated fibres in the chick and focally innervated fibres in the quail. Muscle pieces isolated from the adjacent medial gastrocnemius muscle of the grafted legs were histologically examined to judge their species-specific composition. Horseradish peroxidase was injected into the plantaris muscles of both the grafted and the opposite leg as well as in the plantaris muscle of normal quail embryos, in order to be sure that the plantaris muscle of the graft is innervated by appropriate motoneurons. This procedural design offers for the first time a possibility to test experimentally the influences of motoneurons on endplate pattern formation under conditions corresponding to those in normal ontogenesis. It is shown that such appropriate motoneurons of one species which project to the plantaris muscle of the other species dictate the endplate pattern. When the plantaris muscle is innervated by inappropriate motoneurons, the endplate pattern inherent in the muscle primordium itself becomes realized. A sequence of hierarchically acting factors is proposed to bring different results in line. According to this, the neuronally set programme has priority compared with that set in the muscle. This is true for the normal development and might generate the high neuro-muscular specificity. If under experimental conditions the neuronal programme and the peripheral programme differ, the axons and muscle fibres selectively interact with respect to their inherent characteristics and the muscle-specific programme becomes expressed. If there is a lack of a certain axon type, muscle fibres might become innervated by non-corresponding motoneurons which alter the muscle fibre type.",
keywords = "Endplate pattern formation, Hierarchy of controlling factors, Muscle fibre types, Muscle innervation, Plantaris muscle, Quail-chick chimeras",
author = "M. Grim and K. Nensa and B. Christ and Jacob, {H. J.} and Kathryn Tosney",
year = "1989",
month = "7",
day = "1",
doi = "10.1007/BF00309770",
language = "English",
volume = "180",
pages = "179--189",
journal = "Referate und Beiträge zur Anatomie und Entwickelungsgeschichte",
issn = "0177-5154",
publisher = "Springer Verlag",
number = "2",

}

TY - JOUR

T1 - A hierarchy of determining factors controls motoneuron innervation - Experimental studies on the development of the plantaris muscle (PL) in avian chimeras

AU - Grim, M.

AU - Nensa, K.

AU - Christ, B.

AU - Jacob, H. J.

AU - Tosney, Kathryn

PY - 1989/7/1

Y1 - 1989/7/1

N2 - Quail leg buds were grafted in place of chick leg buds or chick wing buds and vice versa at stages 18 to 21 after colonization by muscle precursor cells had been completed. Motor endplate pattern in the plantaris muscle of the grafts was analyzed before hatching by means of esterase and acetylcholinesterase staining techniques. Muscle fibre types were made visual using the myosin ATPase reaction. Investigations are based on the species-specific endplate pattern of the plantaris muscle: multiply innervated fibres in the chick and focally innervated fibres in the quail. Muscle pieces isolated from the adjacent medial gastrocnemius muscle of the grafted legs were histologically examined to judge their species-specific composition. Horseradish peroxidase was injected into the plantaris muscles of both the grafted and the opposite leg as well as in the plantaris muscle of normal quail embryos, in order to be sure that the plantaris muscle of the graft is innervated by appropriate motoneurons. This procedural design offers for the first time a possibility to test experimentally the influences of motoneurons on endplate pattern formation under conditions corresponding to those in normal ontogenesis. It is shown that such appropriate motoneurons of one species which project to the plantaris muscle of the other species dictate the endplate pattern. When the plantaris muscle is innervated by inappropriate motoneurons, the endplate pattern inherent in the muscle primordium itself becomes realized. A sequence of hierarchically acting factors is proposed to bring different results in line. According to this, the neuronally set programme has priority compared with that set in the muscle. This is true for the normal development and might generate the high neuro-muscular specificity. If under experimental conditions the neuronal programme and the peripheral programme differ, the axons and muscle fibres selectively interact with respect to their inherent characteristics and the muscle-specific programme becomes expressed. If there is a lack of a certain axon type, muscle fibres might become innervated by non-corresponding motoneurons which alter the muscle fibre type.

AB - Quail leg buds were grafted in place of chick leg buds or chick wing buds and vice versa at stages 18 to 21 after colonization by muscle precursor cells had been completed. Motor endplate pattern in the plantaris muscle of the grafts was analyzed before hatching by means of esterase and acetylcholinesterase staining techniques. Muscle fibre types were made visual using the myosin ATPase reaction. Investigations are based on the species-specific endplate pattern of the plantaris muscle: multiply innervated fibres in the chick and focally innervated fibres in the quail. Muscle pieces isolated from the adjacent medial gastrocnemius muscle of the grafted legs were histologically examined to judge their species-specific composition. Horseradish peroxidase was injected into the plantaris muscles of both the grafted and the opposite leg as well as in the plantaris muscle of normal quail embryos, in order to be sure that the plantaris muscle of the graft is innervated by appropriate motoneurons. This procedural design offers for the first time a possibility to test experimentally the influences of motoneurons on endplate pattern formation under conditions corresponding to those in normal ontogenesis. It is shown that such appropriate motoneurons of one species which project to the plantaris muscle of the other species dictate the endplate pattern. When the plantaris muscle is innervated by inappropriate motoneurons, the endplate pattern inherent in the muscle primordium itself becomes realized. A sequence of hierarchically acting factors is proposed to bring different results in line. According to this, the neuronally set programme has priority compared with that set in the muscle. This is true for the normal development and might generate the high neuro-muscular specificity. If under experimental conditions the neuronal programme and the peripheral programme differ, the axons and muscle fibres selectively interact with respect to their inherent characteristics and the muscle-specific programme becomes expressed. If there is a lack of a certain axon type, muscle fibres might become innervated by non-corresponding motoneurons which alter the muscle fibre type.

KW - Endplate pattern formation

KW - Hierarchy of controlling factors

KW - Muscle fibre types

KW - Muscle innervation

KW - Plantaris muscle

KW - Quail-chick chimeras

UR - http://www.scopus.com/inward/record.url?scp=0024375403&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0024375403&partnerID=8YFLogxK

U2 - 10.1007/BF00309770

DO - 10.1007/BF00309770

M3 - Article

C2 - 2802182

AN - SCOPUS:0024375403

VL - 180

SP - 179

EP - 189

JO - Referate und Beiträge zur Anatomie und Entwickelungsgeschichte

JF - Referate und Beiträge zur Anatomie und Entwickelungsgeschichte

SN - 0177-5154

IS - 2

ER -