I. Spinal organization of parasympathetic and sympathetic reflexes
Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine

https://doi.org/10.1016/0165-1838(81)90059-XGet rights and content

Abstract

Electrophysiological and horseradish peroxidase (HRP) techniques have provided new insights into the organization of the sacral parasympathetic reflex pathways to the large intestine and urinary bladder. The innervation of the two organs arises from separate groups of sacral preganglionic cells: (1) a dorsal band of cells in laminae V and VI providing an input to the intestine; and (2) a lateral band of cells in lamina VII providing an input to the bladder. These two groups of cells were separated by an interband region containing tract cells and interneurons. Neurons in the interband region received a visceral afferent input and exhibited firing correlated with the activity of intestine and urinary bladder. It seems reasonable therefore to consider the interband region as a third component of the sacral parasympathetic nucleus. Anterograde transport of HRP revealed that visceral afferents from the intestine and bladder projected into the parasympathetic nucleus. Most of the projections were collaterals from afferent axons in Lissauer's tract that passed in lamina I laterally and medially around the dorsal horn. These afferent collaterals were located in close proximity to preganglionic perikarya and dendrites in laminae I, V and VI. The proximity of visceral afferents and efferents in the sacral cord probably reflects the existence of polysynaptic rather than monosynaptic connections since electrophysiological studies revealed that both the defecation and micturition reflexes occurred with very long central delays (45–70 msec). The reflex pathways mediating defecation and micturition in cats with an intact neuraxis were markedly different. Defecation was dependent upon a spinal reflex with unmyelinated (C-fiber) peripheral afferent and efferent limbs. On the other hand, micturition was mediated by a spinobulbospinal pathway with myelinated peripheral afferent (A-fiber) and efferent axons (B-fiber). Transection of the spinal cord at T12—L2 blocked the micturition reflex but only transiently depressed the defecation reflex. In chronic spinal cats the micturition reflex recovered 1–2 weeks after spinalization; however, in these animals bladder-to-bladder micturition reflexes were elicited by C-fiber rather than A-fiber afferents. The C-fiber afferent-evoked reflex was weak or undetectable in animals with an intact neuraxis. Transection of the spinal cord also changed the micturition reflex in neonatal kittens (age 5–28 days). In neonates with an intact neuraxis bladder-to-bladder reflexes occurred via a long latency spinobulbospinal pathway (325–430 msec). The long latency is attributable to the slow conduction velocity in immature unmyelinated peripheral and central axons. In chronic spinal kittens (3–7 days after spinalization) the long latency reflex was abolished and a shorter latency (90–150 msec) bladder reflex was unmasked. The emergence of this spinal pathway may reflect axonal sprouting and the formation of new reflex connections within the sacral parasympathetic nucleus.

References (57)

  • M.F. Nolan et al.

    A quantitative ultrastructural analysis of the synaptic population in the sacral visceral gray

    Exp. Neurol.

    (1978)
  • J.M. Petras et al.

    Sympathetic and parasympathetic innervation of the urinary bladder and urethra

    Brain Res.

    (1978)
  • M. Sato et al.

    Localization of motoneurons innervating perineal muscles: a HRP study in cat

    Brain Res.

    (1978)
  • A. Sato et al.

    Reflex changes in the urinary bladder after mechanical and thermal stimulation of the skin at various segmental levels in cats

    Neuroscience

    (1977)
  • M. Selzer et al.

    Convergence of visceral and cutaneous afferent pathways in the lumbar spinal cord

    Brain Res.

    (1969)
  • M. Selzer et al.

    Interactions between visceral and cutaneous afferents in the spinal cord: reciprocal primary afferent fiber depolarization

    Brain Res.

    (1969)
  • T. Yamamoto et al.

    Sacral spinal innervations of the rectal and vesical smooth muscles and the sphincteric striated muscles as demonstrated by the horseradish peroxidase method

    Neurosci. Lett.

    (1978)
  • F.J.F. Barrington

    The relationship of the hindbrain to micturition

    Brain

    (1921)
  • F.J.F. Barrington

    The effect of lesion of the hind- and midbrain on micturition in the cat

    Quart. J. exp. Physiol.

    (1925)
  • F.J.F. Barrington

    The component reflexes of micturition in the cat

    Brain

    (1931)
  • H.K. Brown et al.

    Ultrastructure and quantitative synaptology of the sacral parasympathetic nucleus

    J. Neurocytol.

    (1979)
  • R.E. Coggeshall

    Law of separation of function of the spinal roots

    Physiol. Rev.

    (1980)
  • W.C. De Groat

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

    J. Physiol. (Lond.)

    (1976)
  • W.C. De Groat

    Inhibitory mechanisms in the sacral reflex pathways to the urinary bladder

  • W.C. De Groat et al.

    Physiology of the urinary bladder and urethra

    Ann. intern. Med.

    (1980)
  • W.C. De Groat et al.

    Neural control of the urinary bladder and large intestine

  • W.C. De Groat et al.

    Properties of interneurons in the sacral autonomic nucleus of the cat

  • W.C. De Groat et al.

    Preganglionic C-fibers: a major component of the sacral autonomic outflow to the colon of the cat

    Pflügers Arch. ges. Physiol.

    (1975)
  • Cited by (423)

    • Voluntary versus reflex micturition control

      2023, Neuro-Urology Research: A Comprehensive Overview
    View all citing articles on Scopus
    View full text