Elsevier

Brain Research

Volume 541, Issue 2, 15 February 1991, Pages 241-251
Brain Research

Light and electron microscopic analyses of intraspinal axon collaterals of sympathetic preganglionic neurons

https://doi.org/10.1016/0006-8993(91)91024-UGet rights and content

Abstract

Experiments were performed in pigeons (Columba livia). Sympathetic preganglionic neurons (SPNs) in the first thoracic spinal cord segment (T1) were identified electrophysiologically using antidromic activation and collision techniques and then intracellularly labeled with horseradish peroxidase (HRP). In 6 of 10 HRP-labeled SPNs, the site of axon origin and intraspinal axonal trajectory could be specified. In 2 of the 6 HRP-labeled axons, the peripherally projecting process branched intraspinally. The presence or absence of SPN intraspinal axonal collateralization did not correlate with parent perikaryal subnuclear location or dendritic alignment. None of the collaterals were recurrent onto the SPN of origin. Light microscopically, the collateral branches appeared to end with punctate, bulbous swellings. The spinal regions of the terminal end swellings for the two axons did not overlap one another. In one instance the entire terminal field was confined within the principal preganglionic cell column (column of Terni). The other axon had collateral branches which terminated in the lateral white matter and in a ventrolateral region of lamina VII. A serial section, electron microscopic reconstructive analysis of the entire intraspinal collateral terminal field within the column of Terni revealed that: (a) the primary collateral process was unmyelinated and arose at a node of Ranvier; (b) after issuance of the collateral branch, the myelinated parent axon continued to increase its myelin wrapping throughout the spinal gray; (c) the bulbous swellings observed light microscopically corresponded to axon terminal boutons and regions of synaptic contact; (d) the axon collateral terminals were exclusively presynaptic to small caliber dendrites and formed only asymmetric specializations; and (e) the collateral terminals contained numerous mitochondria, and densely packed, electron-lucent, spherical vesicles.

References (41)

  • BarmanS.M.

    Spinal cord control of the cardiovascular system

  • BerodA. et al.

    Importance of fixation in immunohistochemistry: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase

    J. Histochem. Cytochem.

    (1981)
  • BurkeR.E. et al.

    Spinal neurons and synapses

  • CabotJ.B.

    Sympathetic preganglionic neurons: cytoarchitecture, ultrastructure, and biophysical properties

  • CabotJ.B. et al.

    Somatic and dendritic morphology of intracellularly labeled sympathetic preganglionic neurons

    Soc. Neurosci. Abstr.

    (1985)
  • CabotJ.B. et al.

    Evidence for glycine-like immunoreactive input onto retrogradely labeled sympathetic preganglionic neurons in the rat and pigeon

    Soc. Neurosci. Abstr.

    (1990)
  • CooteJ.H.

    The organisation of cardiovascular neurons in the spinal cord

    Rev. Physiol. Biochem. Pharmacol.

    (1988)
  • DeGroatW.C.

    Mechanisms underlying recurrent inhibition in the sacral parasympathetic outflow to the urinary bladder

    J. Physiol.

    (1976)
  • DembowskyK. et al.

    Morphology of sympathetic preganglionic neurons in the thoracic spinal cord of the cat: an intracellular horseradish peroxidase study

    J. Comp. Neurol.

    (1985)
  • DembowskyK. et al.

    Three types of sympathetic preganglionic neurones with different electrophysiological properties are identified by intracellular recordings in the cat

    Pflu¨gers Arch.

    (1986)
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