Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1995 Sep 1;487(Pt 2):453–463. doi: 10.1113/jphysiol.1995.sp020892

Medullary-evoked EPSPs in neonatal rat sympathetic preganglionic neurones in vitro.

S A Deuchars 1, S F Morrison 1, M P Gilbey 1
PMCID: PMC1156585  PMID: 8558476

Abstract

1. Whole-cell patch clamp recordings were made from twenty-three sympathetic preganglionic neurones (SPNs) in the upper thoracic segments of a neonatal rat brainstem-spinal cord preparation to study their synaptic responses to stimulation of the rostral ventrolateral medulla (RVLM) and the receptors involved. 2. SPNs were identified by their antidromic activation following stimulation of a ventral root, their morphology and their location in the spinal cord. 3. Electrical stimulation within the RVLM elicited EPSPs in all SPNs tested (n = 23). These EPSPs consisted of one or more components that had different time courses, voltage relationships and pharmacological sensitivities. 4. All SPNs responded to RVLM stimulation with a constant-latency fast EPSP that increased in size as the membrane was hyperpolarized. This EPSP was reduced in amplitude by the non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (10-20 microM). 5. In thirteen SPNs the response to RVLM stimulation was a complex EPSP consisting of a fast EPSP and a slow EPSP that either followed or summed with the fast EPSP. The amplitude of the slow EPSP was (i) either reduced in size or not affected as the membrane was hyperpolarized, and (ii) reduced by the NMDA receptor antagonist, D, L-2-amino-5-phosphonovaleric acid (50 microM). 6. Selective activation of neuronal cell bodies in the RVLM by chemical stimulation elicited slow depolarizations and increases in synaptic activity in SPNs. 7. These results provide evidence that an excitatory amino acid is involved in transmitting sympathoexcitatory drive from the RVLM, partly via a monosynaptic pathway. Both non-NMDA and NMDA receptors play a role in mediating this drive.

Full text

PDF
453

Images in this article

Selected References

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

  1. Arata A., Onimaru H., Homma I. Respiration-related neurons in the ventral medulla of newborn rats in vitro. Brain Res Bull. 1990 Apr;24(4):599–604. doi: 10.1016/0361-9230(90)90165-v. [DOI] [PubMed] [Google Scholar]
  2. Birch P. J., Grossman C. J., Hayes A. G. 6,7-Dinitro-quinoxaline-2,3-dion and 6-nitro,7-cyano-quinoxaline-2,3-dion antagonise responses to NMDA in the rat spinal cord via an action at the strychnine-insensitive glycine receptor. Eur J Pharmacol. 1988 Oct 26;156(1):177–180. doi: 10.1016/0014-2999(88)90163-x. [DOI] [PubMed] [Google Scholar]
  3. Bittar P., Muller D. Time-dependent reversal of long-term potentiation by brief cooling shocks in rat hippocampal slices. Brain Res. 1993 Aug 27;620(2):181–188. doi: 10.1016/0006-8993(93)90154-f. [DOI] [PubMed] [Google Scholar]
  4. Burrows M. Effects of temperature on a central synapse between identified motor neurons in the locust. J Comp Physiol A. 1989 Sep;165(5):687–695. doi: 10.1007/BF00611000. [DOI] [PubMed] [Google Scholar]
  5. Cabot J. B., Alessi V., Carroll J., Ligorio M. Spinal cord lamina V and lamina VII interneuronal projections to sympathetic preganglionic neurons. J Comp Neurol. 1994 Sep 22;347(4):515–530. doi: 10.1002/cne.903470404. [DOI] [PubMed] [Google Scholar]
  6. Davison A. N., Dobbing J. Myelination as a vulnerable period in brain development. Br Med Bull. 1966 Jan;22(1):40–44. doi: 10.1093/oxfordjournals.bmb.a070434. [DOI] [PubMed] [Google Scholar]
  7. Deuchars S. A., Spyer K. M., Brooks P. A., Gilbey M. P. A study of sympathetic preganglionic neuronal activity in a neonatal rat brainstem-spinal cord preparation. J Auton Nerv Syst. 1995 Mar 18;52(1):51–63. doi: 10.1016/0165-1838(94)00144-9. [DOI] [PubMed] [Google Scholar]
  8. Dun N. J., Wu S. Y., Shen E., Miyazaki T., Dun S. L., Ren C. Synaptic mechanisms in sympathetic preganglionic neurons. Can J Physiol Pharmacol. 1992;70 (Suppl):S86–S91. doi: 10.1139/y92-248. [DOI] [PubMed] [Google Scholar]
  9. Errchidi S., Monteau R., Hilaire G. Noradrenergic modulation of the medullary respiratory rhythm generator in the newborn rat: an in vitro study. J Physiol. 1991 Nov;443:477–498. doi: 10.1113/jphysiol.1991.sp018846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fulton B. P., Walton K. Electrophysiological properties of neonatal rat motoneurones studied in vitro. J Physiol. 1986 Jan;370:651–678. doi: 10.1113/jphysiol.1986.sp015956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hanker J. S., Yates P. E., Metz C. B., Rustioni A. A new specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochem J. 1977 Nov;9(6):789–792. doi: 10.1007/BF01003075. [DOI] [PubMed] [Google Scholar]
  12. Inokuchi H., Yoshimura M., Yamada S., Polosa C., Nishi S. Fast excitatory postsynaptic potentials and the responses to excitant amino acids of sympathetic preganglionic neurons in the slice of the cat spinal cord. Neuroscience. 1992;46(3):657–667. doi: 10.1016/0306-4522(92)90152-r. [DOI] [PubMed] [Google Scholar]
  13. Llewellyn-Smith I. J., Phend K. D., Minson J. B., Pilowsky P. M., Chalmers J. P. Glutamate-immunoreactive synapses on retrogradely-labelled sympathetic preganglionic neurons in rat thoracic spinal cord. Brain Res. 1992 May 22;581(1):67–80. doi: 10.1016/0006-8993(92)90345-a. [DOI] [PubMed] [Google Scholar]
  14. Marks S. A., Gilbey M. P. Effect on cardiac sympathetic nerve activity of phenylephrine microinjected into the cat intermediolateral cell column. J Physiol. 1992;453:185–195. doi: 10.1113/jphysiol.1992.sp019223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mayer M. L., Westbrook G. L. Mixed-agonist action of excitatory amino acids on mouse spinal cord neurones under voltage clamp. J Physiol. 1984 Sep;354:29–53. doi: 10.1113/jphysiol.1984.sp015360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McAllen R. M., Häbler H. J., Michaelis M., Peters O., Jänig W. Monosynaptic excitation of preganglionic vasomotor neurons by subretrofacial neurons of the rostral ventrolateral medulla. Brain Res. 1994 Jan 21;634(2):227–234. doi: 10.1016/0006-8993(94)91925-9. [DOI] [PubMed] [Google Scholar]
  17. Mo N., Dun N. J. Excitatory postsynaptic potentials in neonatal rat sympathetic preganglionic neurons: possible mediation by NMDA receptors. Neurosci Lett. 1987 Jun 26;77(3):327–332. doi: 10.1016/0304-3940(87)90522-2. [DOI] [PubMed] [Google Scholar]
  18. Morrison S. F., Callaway J., Milner T. A., Reis D. J. Rostral ventrolateral medulla: a source of the glutamatergic innervation of the sympathetic intermediolateral nucleus. Brain Res. 1991 Oct 18;562(1):126–135. doi: 10.1016/0006-8993(91)91196-8. [DOI] [PubMed] [Google Scholar]
  19. Morrison S. F., Ernsberger P., Milner T. A., Callaway J., Gong A., Reis D. J. A glutamate mechanism in the intermediolateral nucleus mediates sympathoexcitatory responses to stimulation of the rostral ventrolateral medulla. Prog Brain Res. 1989;81:159–169. doi: 10.1016/s0079-6123(08)62006-3. [DOI] [PubMed] [Google Scholar]
  20. Murase K., Randić M. Electrophysiological properties of rat spinal dorsal horn neurones in vitro: calcium-dependent action potentials. J Physiol. 1983 Jan;334:141–153. doi: 10.1113/jphysiol.1983.sp014485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nowak L., Bregestovski P., Ascher P., Herbet A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 1984 Feb 2;307(5950):462–465. doi: 10.1038/307462a0. [DOI] [PubMed] [Google Scholar]
  22. Pickering A. E., Spanswick D., Logan S. D. Whole-cell recordings from sympathetic preganglionic neurons in rat spinal cord slices. Neurosci Lett. 1991 Sep 16;130(2):237–242. doi: 10.1016/0304-3940(91)90405-i. [DOI] [PubMed] [Google Scholar]
  23. Pyner S., Coote J. H. A comparison between the adult rat and neonate rat of the architecture of sympathetic preganglionic neurones projecting to the superior cervical ganglion, stellate ganglion and adrenal medulla. J Auton Nerv Syst. 1994 Jul;48(2):153–166. doi: 10.1016/0165-1838(94)90031-0. [DOI] [PubMed] [Google Scholar]
  24. Shen E., Mo N., Dun N. J. APV-sensitive dorsal root afferent transmission to neonate rat sympathetic preganglionic neurons in vitro. J Neurophysiol. 1990 Sep;64(3):991–999. doi: 10.1152/jn.1990.64.3.991. [DOI] [PubMed] [Google Scholar]
  25. Thomson A. M. Augmentation by glycine and blockade by 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) of responses to excitatory amino acids in slices of rat neocortex. Neuroscience. 1990;39(1):69–79. doi: 10.1016/0306-4522(90)90222-p. [DOI] [PubMed] [Google Scholar]
  26. Zagon A., Smith A. D. Monosynaptic projections from the rostral ventrolateral medulla oblongata to identified sympathetic preganglionic neurons. Neuroscience. 1993 Jun;54(3):729–743. doi: 10.1016/0306-4522(93)90243-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES