The development of catecholaminergic innervation in chick spinal cord

doi:10.1016/0006-8993(80)91291-3

Brain Research

Volume 191, Issue 2, 9 June 1980, Pages 417-428

https://doi.org/10.1016/0006-8993(80)91291-3 Get rights and content

Abstract

This combined biochemical and histofluorescent study of the embryonic chick was designed to investigate the temporal and spatial development of noradrenergic pathways in the spinal cord. The sequence of catecholaminergic innervation was analyzed by measuring the specific uptake of [³H]norepinephrine, the levels of endogenous norepinephrine, and the distribution of catecholamine histofluorescence. Uptake studies showed early axons present in all levels of spinal cord by 10 days incubation with subsequent increases of uptake activity appearing in a rostrocaudal fashion. Endogenous norepinephrine values were low until day 14, at which time transmitter levels began to increase, approaching hatched values on incubation day 17. Morphologic studies demonstrated catecholaminergic terminals first in the intermediate gray matter and later concentrated in the ventral and dorsal horns. These observations were interpreted to indicate that: (1) noradrenergic axons are an early descending supraspinal pathway; (2) arborization of this system occurs in a rostral-caudal sequence; and (3) monoaminergic uptake mechanisms develop prior to and independent of neurotransmitter synthesis and storage. The development of this noradrenergic system parallels alteration in spinal cord physiology and refinements in the motility of the embryo.

Reference (38)

BekoffA.
Ontogeny of leg motor output in the chick embryo: a neural analysis
Brain Research
(1976)
CasertaM. et al.
Biochemical and morphological studies of synaptogenesis in the avian sympathetic cell column
Brain Research
(1978)
CoyleJ.T.
Biochemical aspects of neurotransmission in the developing brain
DescarriesL. et al.
Serotonin nerve terminals in adult rat neocortex
Brain Research
(1975)
IkedaH. et al.
Distribution of monoamine containing cells in the central nervous system of the chicken
Jap. J. Pharmacol.
(1971)
IkedaH. et al.
Distribution of monoamine containing terminals and fibers in the central nervous system of the chicken
Jap. J. Pharmacol.
(1974)
KopinI.J. et al.
Quantitative relationship of catecholamine content and histofluorescence in brain of rats
Brain Research
(1974)
LowryO.H. et al.
Protein measurement with the Folin phenol reagent
J. biol. Chem.
(1951)
MaedaT. et al.
Modification of postnatal development of neocortex in rat brain with experimental deprivation of locus coeruleus
Brain Research
(1974)
NygrenL.G. et al.
A new major projection from locus coeruleus: the main source of noradrenergic nerve terminals in the ventral and dorsal columns of the spinal cord
Brain Research
(1977)

SohalG.S.

Effects of reciprocal forebrain transplantation on motility and hatching in chick and duck embryos

Brain Research

(1976)

StokesB.T. et al.

The emergence of inhibition in the chick embryo spinal cord

Brain Research

(1974)

TennysonV.M. et al.

5-Hydroxydopamine ‘tagged’ neuronal boutons in rabbit neostriatum: interrelationship between vesicles and axonal membrane

Brain Research

(1974)

WendlandtS. et al.

The involvement of the noradrenergic system arising from the locus coeruleus in the postnatal development of the cortex in rat brain

Brain Research

(1977)

ZivinJ.A. et al.

Quantitative localization of biogenic amines in the spinal cord

Brain Research

(1975)

CarlssonA. et al.

Cellular localization of monoamine in the spinal cord

Acta physiol. scand.

(1964)

CoghillG.E.

Anatomy and the Problem of Behavior

(1929)

CoyleJ.T. et al.

Development of the uptake and storage ofl-[³H]norepinephrine in the rat brain

J. Neurochem.

(1971)

CoyleJ.T. et al.

Catecholamines in fetal and newborn rat brain

J. Neurochem.

(1973)

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The development of catecholaminergic innervation in chick spinal cord

Abstract

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Development of the uptake and storage ofl-[³H]norepinephrine in the rat brain