Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1991 Mar;434:295–306. doi: 10.1113/jphysiol.1991.sp018470

Evidence for descending tonic inhibition specifically affecting sympathetic pathways to the kidney in rats.

K Hayes 1, C P Yardley 1, L C Weaver 1
PMCID: PMC1181418  PMID: 2023121

Abstract

1. The present study investigated the possibility that pre- and postganglionic neurones innervating the kidney and spleen in rats are affected by descending inhibitory as well as descending excitatory influences. This hypothesis was tested by comparing the effects of cervical spinal cord transection to the effects of blockade of tonic activity of excitatory neurones in the rostral ventrolateral medulla (RVLM). 2. Electrical discharge of multifibre postganglionic renal and splenic and preganglionic greater splanchnic nerves and 13th thoracic (T13) white rami was recorded in artificially respired, urethane-anaesthetized rats. In one group of rats, descending supraspinal pathways were interrupted by cervical spinal cord transection. In another group, tonic activity of rostral ventrolateral medulla (RVLM) neurones was blocked by bilateral microinjections of the inhibitory amino acid glycine. The effects of spinal cord transection were compared to effects of this bilateral RVLM blockade and to effects of unilateral RVLM blockade described in a previous study. 3. Spinal cord transection caused decreases in preganglionic greater splanchnic and postganglionic splenic nerves which were of the same magnitude as those caused by bilateral blockade of the RVLM. 4. In contrast, discharge of renal nerves was decreased more by bilateral RVLM blockade than by cervical spinal cord transection. Similarly, even unilateral RVLM blockade caused greater decreases in discharge of T13 white rami than were caused by spinal cord transection. 5. These findings suggest that renal nerves and their preganglionic inputs (T13 white rami) are controlled in part by tonic sympathoinhibitory influences which can be unmasked by blockade of the RVLM. These sympathoinhibitory influences do not appear to affect the activity of splanchnic and splenic nerves.

Full text

PDF
295

Images in this article

301Fig. 4
on p.301

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agarwal S. K., Gelsema A. J., Calaresu F. R. Neurons in rostral VLM are inhibited by chemical stimulation of caudal VLM in rats. Am J Physiol. 1989 Aug;257(2 Pt 2):R265–R270. doi: 10.1152/ajpregu.1989.257.2.R265. [DOI] [PubMed] [Google Scholar]
  2. Calaresu F. R., Yardley C. P. Medullary basal sympathetic tone. Annu Rev Physiol. 1988;50:511–524. doi: 10.1146/annurev.ph.50.030188.002455. [DOI] [PubMed] [Google Scholar]
  3. Coote J. H., Macleod V. H. The influence of bulbospinal monoaminergic pathways on sympathetic nerve activity. J Physiol. 1974 Sep;241(2):453–475. doi: 10.1113/jphysiol.1974.sp010666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dembowsky K., Czachurski J., Amendt K., Seller H. Tonic descending inhibition of the spinal somato-sympathetic reflex from the lower brain stem. J Auton Nerv Syst. 1980 Jul;2(2):157–182. doi: 10.1016/0165-1838(80)90043-0. [DOI] [PubMed] [Google Scholar]
  5. Ferguson M., Ryan G. B., Bell C. Localization of sympathetic and sensory neurons innervating the rat kidney. J Auton Nerv Syst. 1986 Aug;16(4):279–288. doi: 10.1016/0165-1838(86)90034-2. [DOI] [PubMed] [Google Scholar]
  6. Fleetwood-Walker S. M., Coote J. H., Gilbey M. P. Identification of spinally projecting neurones in the A1 catecholamine cell group of the ventrolateral medulla. Brain Res. 1983 Aug 22;273(1):25–33. doi: 10.1016/0006-8993(83)91090-9. [DOI] [PubMed] [Google Scholar]
  7. Granata A. R., Numao Y., Kumada M., Reis D. J. A1 noradrenergic neurons tonically inhibit sympathoexcitatory neurons of C1 area in rat brainstem. Brain Res. 1986 Jul 2;377(1):127–146. doi: 10.1016/0006-8993(86)91198-4. [DOI] [PubMed] [Google Scholar]
  8. Granata A. R., Ruggiero D. A., Park D. H., Joh T. H., Reis D. J. Brain stem area with C1 epinephrine neurons mediates baroreflex vasodepressor responses. Am J Physiol. 1985 Apr;248(4 Pt 2):H547–H567. doi: 10.1152/ajpheart.1985.248.4.H547. [DOI] [PubMed] [Google Scholar]
  9. Hayes K., Chevendra V., Weaver L. C. Pre- and postganglionic sympathetic activity in white rami of rats. Neurosci Lett. 1990 Jul 17;115(1):55–61. doi: 10.1016/0304-3940(90)90517-d. [DOI] [PubMed] [Google Scholar]
  10. Hayes K., Weaver L. C. Selective control of sympathetic pathways to the kidney, spleen and intestine by the ventrolateral medulla in rats. J Physiol. 1990 Sep;428:371–385. doi: 10.1113/jphysiol.1990.sp018217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Loewy A. D., McKellar S. Serotonergic projections from the ventral medulla to the intermediolateral cell column in the rat. Brain Res. 1981 Apr 27;211(1):146–152. doi: 10.1016/0006-8993(81)90074-3. [DOI] [PubMed] [Google Scholar]
  12. Loewy A. D. Raphe pallidus and raphe obscurus projections to the intermediolateral cell column in the rat. Brain Res. 1981 Oct 5;222(1):129–133. doi: 10.1016/0006-8993(81)90946-x. [DOI] [PubMed] [Google Scholar]
  13. McCall R. B. GABA-mediated inhibition of sympathoexcitatory neurons by midline medullary stimulation. Am J Physiol. 1988 Oct;255(4 Pt 2):R605–R615. doi: 10.1152/ajpregu.1988.255.4.R605. [DOI] [PubMed] [Google Scholar]
  14. McCall R. B., Harris L. T. Sympathetic alterations after midline medullary raphe lesions. Am J Physiol. 1987 Jul;253(1 Pt 2):R91–100. doi: 10.1152/ajpregu.1987.253.1.R91. [DOI] [PubMed] [Google Scholar]
  15. Meckler R. L., Weaver L. C. Characteristics of ongoing and reflex discharge of single splenic and renal sympathetic postganglionic fibres in cats. J Physiol. 1988 Feb;396:139–153. doi: 10.1113/jphysiol.1988.sp016955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Meckler R. L., Weaver L. C. Splenic, renal, and cardiac nerves have unequal dependence upon tonic supraspinal inputs. Brain Res. 1985 Jul 8;338(1):123–135. doi: 10.1016/0006-8993(85)90254-9. [DOI] [PubMed] [Google Scholar]
  17. Müller U. W., Dembowsky K., Czachurski J., Seller H. Tonic descending inhibition of the spinal cardio-sympathetic reflex in the cat. J Auton Nerv Syst. 1988 Aug;23(2):111–123. doi: 10.1016/0165-1838(88)90075-6. [DOI] [PubMed] [Google Scholar]
  18. Pilowsky P., West M., Chalmers J. Renal sympathetic nerve responses to stimulation, inhibition and destruction of the ventrolateral medulla in the rabbit. Neurosci Lett. 1985 Sep 16;60(1):51–55. doi: 10.1016/0304-3940(85)90380-5. [DOI] [PubMed] [Google Scholar]
  19. Schramm L. P., Chornoboy E. S. Sympathetic activity in spontaneously hypertensive rats after spinal transection. Am J Physiol. 1982 Nov;243(5):R506–R511. doi: 10.1152/ajpregu.1982.243.5.R506. [DOI] [PubMed] [Google Scholar]
  20. Schramm L. P., Livingstone R. H. Inhibition of renal nerve sympathetic activity by spinal stimulation in rat. Am J Physiol. 1987 Mar;252(3 Pt 2):R514–R525. doi: 10.1152/ajpregu.1987.252.3.R514. [DOI] [PubMed] [Google Scholar]
  21. Sripairojthikoon W., Wyss J. M. Cells of origin of the sympathetic renal innervation in rat. Am J Physiol. 1987 Jun;252(6 Pt 2):F957–F963. doi: 10.1152/ajprenal.1987.252.6.F957. [DOI] [PubMed] [Google Scholar]
  22. Stein R. D., Weaver L. C. Multi- and single-fibre mesenteric and renal sympathetic responses to chemical stimulation of intestinal receptors in cats. J Physiol. 1988 Feb;396:155–172. doi: 10.1113/jphysiol.1988.sp016956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Stein R. D., Weaver L. C., Yardley C. P. Ventrolateral medullary neurones: effects on magnitude and rhythm of discharge of mesenteric and renal nerves in cats. J Physiol. 1989 Jan;408:571–586. doi: 10.1113/jphysiol.1989.sp017477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Taylor R. F., Schramm L. P. Differential effects of spinal transection on sympathetic nerve activities in rats. Am J Physiol. 1987 Oct;253(4 Pt 2):R611–R618. doi: 10.1152/ajpregu.1987.253.4.R611. [DOI] [PubMed] [Google Scholar]
  25. Taylor R. F., Schramm L. P. Spinally mediated inhibition of abdominal and lumbar sympathetic activities. Am J Physiol. 1988 Apr;254(4 Pt 2):R655–R658. doi: 10.1152/ajpregu.1988.254.4.R655. [DOI] [PubMed] [Google Scholar]
  26. Willette R. N., Punnen S., Krieger A. J., Sapru H. N. Interdependence of rostral and caudal ventrolateral medullary areas in the control of blood pressure. Brain Res. 1984 Oct 29;321(1):169–174. doi: 10.1016/0006-8993(84)90696-6. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES