Development of cerebral arterial innervation: synchronous development of neuropeptide Y (NPY)- and vasoactive intestinal polypeptide (VIP)-containing fibers and some observations on growth cones

Shin Han Tsai, John M. Tew, Michael T. Shipley

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

The pre- and postnatal development of sympathetic fibers containing neuropeptide Y (NPY) and parasympathetic fibers containing vasoactive intestinal polypeptide (VIP) supplying the cerebral arteries were studied with immunohistochemistry in rats. The innervation patterns and densities of NPY and VIP fibers were similar at all stages of development and similar to that previously reported for norepinephrine (NE). There was a striking reorganization of the innervation pattern of all three fiber systems between the first and second postnatal weeks. At all stages of development prior to the first postnatal week, growth cones were present on individual fibers at the distal part of major cerebral arteries and the middle segment of the basilar artery. The growth cones had a range of shapes from blunt to stellate, lanceolate or filiform. NPY and VIP immunoreactive granules were commonly present. The present results taken with our earlier developmental study of NE (fibers) (J. Comp. Neurol., 271 (1988) 435-444), demonstrate that: (1) both sympathetic and parasympathetic perivascular nerves on immature cerebral vessels develop with similar sequences: first longitudinal fibers and fiber bundles are present; these transform to a meshwork pattern and finally transform again into the mature, predominantly circumferential pattern; (2) both the classical (NE) and peptidergic transmitters (NPY) within the sympathetic system appear to develop identically in terms of time of appearance, innervation patterns, densities and reorganization. This suggests that NE and NPY are largely co-localized and coordinately regulated in cerebrovascular sympathetic fibers; (3) the development of parasympathetic VIP fibers is remarkably similar to that of the sympathetic system in time of appearance, sequence, transformation of innervation patterns and progressive increases in innervation density at all developmental stages; (4) the development of both sympathetic and parasympathetic fibers into the mature circumferential pattern begins abruptly and takes place in a relatively short period from the first to the second postnatal week. Growth cones on all fiber types were abundant up to the first postnatal week but were not evident when those fiber systems underwent their final reorganization. This suggests that growth cones play a role in initial axon guidance but not in local remodelling. Taken together, these findings show that the sympathetic (vasoconstrictive) and parasymphatetic (vasodilative) neurovascular systems are highly synchronized at all stages of development. This remarkable synchrony suggests that there is a tightly regulated balance between vasoconstriction and vasodilation of cerebral vessels throughout development. The developmental synchrony of sympthetic innervation may be achieved by interactions among the fibers, coordinate expression of target secreted tropic factors, or both.

Original languageEnglish
Pages (from-to)77-83
Number of pages7
JournalDevelopmental Brain Research
Volume69
Issue number1
DOIs
Publication statusPublished - Sep 18 1992
Externally publishedYes

Fingerprint

Growth Cones
Neuropeptide Y
Vasoactive Intestinal Peptide
Adrenergic Fibers
Norepinephrine
Basilar Artery
Cerebral Arteries
Middle Cerebral Artery
Vasoconstriction
Vasodilation
Immunohistochemistry

Keywords

  • Cerebral artery
  • Neuropeptide Y
  • Perivascular innervation
  • Rat
  • Vasoactive intestinal polypeptide

ASJC Scopus subject areas

  • Developmental Biology
  • Developmental Neuroscience

Cite this

@article{2bba4586b3b1457fa1e46719eeba75d2,
title = "Development of cerebral arterial innervation: synchronous development of neuropeptide Y (NPY)- and vasoactive intestinal polypeptide (VIP)-containing fibers and some observations on growth cones",
abstract = "The pre- and postnatal development of sympathetic fibers containing neuropeptide Y (NPY) and parasympathetic fibers containing vasoactive intestinal polypeptide (VIP) supplying the cerebral arteries were studied with immunohistochemistry in rats. The innervation patterns and densities of NPY and VIP fibers were similar at all stages of development and similar to that previously reported for norepinephrine (NE). There was a striking reorganization of the innervation pattern of all three fiber systems between the first and second postnatal weeks. At all stages of development prior to the first postnatal week, growth cones were present on individual fibers at the distal part of major cerebral arteries and the middle segment of the basilar artery. The growth cones had a range of shapes from blunt to stellate, lanceolate or filiform. NPY and VIP immunoreactive granules were commonly present. The present results taken with our earlier developmental study of NE (fibers) (J. Comp. Neurol., 271 (1988) 435-444), demonstrate that: (1) both sympathetic and parasympathetic perivascular nerves on immature cerebral vessels develop with similar sequences: first longitudinal fibers and fiber bundles are present; these transform to a meshwork pattern and finally transform again into the mature, predominantly circumferential pattern; (2) both the classical (NE) and peptidergic transmitters (NPY) within the sympathetic system appear to develop identically in terms of time of appearance, innervation patterns, densities and reorganization. This suggests that NE and NPY are largely co-localized and coordinately regulated in cerebrovascular sympathetic fibers; (3) the development of parasympathetic VIP fibers is remarkably similar to that of the sympathetic system in time of appearance, sequence, transformation of innervation patterns and progressive increases in innervation density at all developmental stages; (4) the development of both sympathetic and parasympathetic fibers into the mature circumferential pattern begins abruptly and takes place in a relatively short period from the first to the second postnatal week. Growth cones on all fiber types were abundant up to the first postnatal week but were not evident when those fiber systems underwent their final reorganization. This suggests that growth cones play a role in initial axon guidance but not in local remodelling. Taken together, these findings show that the sympathetic (vasoconstrictive) and parasymphatetic (vasodilative) neurovascular systems are highly synchronized at all stages of development. This remarkable synchrony suggests that there is a tightly regulated balance between vasoconstriction and vasodilation of cerebral vessels throughout development. The developmental synchrony of sympthetic innervation may be achieved by interactions among the fibers, coordinate expression of target secreted tropic factors, or both.",
keywords = "Cerebral artery, Neuropeptide Y, Perivascular innervation, Rat, Vasoactive intestinal polypeptide",
author = "Tsai, {Shin Han} and Tew, {John M.} and Shipley, {Michael T.}",
year = "1992",
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TY - JOUR

T1 - Development of cerebral arterial innervation

T2 - synchronous development of neuropeptide Y (NPY)- and vasoactive intestinal polypeptide (VIP)-containing fibers and some observations on growth cones

AU - Tsai, Shin Han

AU - Tew, John M.

AU - Shipley, Michael T.

PY - 1992/9/18

Y1 - 1992/9/18

N2 - The pre- and postnatal development of sympathetic fibers containing neuropeptide Y (NPY) and parasympathetic fibers containing vasoactive intestinal polypeptide (VIP) supplying the cerebral arteries were studied with immunohistochemistry in rats. The innervation patterns and densities of NPY and VIP fibers were similar at all stages of development and similar to that previously reported for norepinephrine (NE). There was a striking reorganization of the innervation pattern of all three fiber systems between the first and second postnatal weeks. At all stages of development prior to the first postnatal week, growth cones were present on individual fibers at the distal part of major cerebral arteries and the middle segment of the basilar artery. The growth cones had a range of shapes from blunt to stellate, lanceolate or filiform. NPY and VIP immunoreactive granules were commonly present. The present results taken with our earlier developmental study of NE (fibers) (J. Comp. Neurol., 271 (1988) 435-444), demonstrate that: (1) both sympathetic and parasympathetic perivascular nerves on immature cerebral vessels develop with similar sequences: first longitudinal fibers and fiber bundles are present; these transform to a meshwork pattern and finally transform again into the mature, predominantly circumferential pattern; (2) both the classical (NE) and peptidergic transmitters (NPY) within the sympathetic system appear to develop identically in terms of time of appearance, innervation patterns, densities and reorganization. This suggests that NE and NPY are largely co-localized and coordinately regulated in cerebrovascular sympathetic fibers; (3) the development of parasympathetic VIP fibers is remarkably similar to that of the sympathetic system in time of appearance, sequence, transformation of innervation patterns and progressive increases in innervation density at all developmental stages; (4) the development of both sympathetic and parasympathetic fibers into the mature circumferential pattern begins abruptly and takes place in a relatively short period from the first to the second postnatal week. Growth cones on all fiber types were abundant up to the first postnatal week but were not evident when those fiber systems underwent their final reorganization. This suggests that growth cones play a role in initial axon guidance but not in local remodelling. Taken together, these findings show that the sympathetic (vasoconstrictive) and parasymphatetic (vasodilative) neurovascular systems are highly synchronized at all stages of development. This remarkable synchrony suggests that there is a tightly regulated balance between vasoconstriction and vasodilation of cerebral vessels throughout development. The developmental synchrony of sympthetic innervation may be achieved by interactions among the fibers, coordinate expression of target secreted tropic factors, or both.

AB - The pre- and postnatal development of sympathetic fibers containing neuropeptide Y (NPY) and parasympathetic fibers containing vasoactive intestinal polypeptide (VIP) supplying the cerebral arteries were studied with immunohistochemistry in rats. The innervation patterns and densities of NPY and VIP fibers were similar at all stages of development and similar to that previously reported for norepinephrine (NE). There was a striking reorganization of the innervation pattern of all three fiber systems between the first and second postnatal weeks. At all stages of development prior to the first postnatal week, growth cones were present on individual fibers at the distal part of major cerebral arteries and the middle segment of the basilar artery. The growth cones had a range of shapes from blunt to stellate, lanceolate or filiform. NPY and VIP immunoreactive granules were commonly present. The present results taken with our earlier developmental study of NE (fibers) (J. Comp. Neurol., 271 (1988) 435-444), demonstrate that: (1) both sympathetic and parasympathetic perivascular nerves on immature cerebral vessels develop with similar sequences: first longitudinal fibers and fiber bundles are present; these transform to a meshwork pattern and finally transform again into the mature, predominantly circumferential pattern; (2) both the classical (NE) and peptidergic transmitters (NPY) within the sympathetic system appear to develop identically in terms of time of appearance, innervation patterns, densities and reorganization. This suggests that NE and NPY are largely co-localized and coordinately regulated in cerebrovascular sympathetic fibers; (3) the development of parasympathetic VIP fibers is remarkably similar to that of the sympathetic system in time of appearance, sequence, transformation of innervation patterns and progressive increases in innervation density at all developmental stages; (4) the development of both sympathetic and parasympathetic fibers into the mature circumferential pattern begins abruptly and takes place in a relatively short period from the first to the second postnatal week. Growth cones on all fiber types were abundant up to the first postnatal week but were not evident when those fiber systems underwent their final reorganization. This suggests that growth cones play a role in initial axon guidance but not in local remodelling. Taken together, these findings show that the sympathetic (vasoconstrictive) and parasymphatetic (vasodilative) neurovascular systems are highly synchronized at all stages of development. This remarkable synchrony suggests that there is a tightly regulated balance between vasoconstriction and vasodilation of cerebral vessels throughout development. The developmental synchrony of sympthetic innervation may be achieved by interactions among the fibers, coordinate expression of target secreted tropic factors, or both.

KW - Cerebral artery

KW - Neuropeptide Y

KW - Perivascular innervation

KW - Rat

KW - Vasoactive intestinal polypeptide

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