Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1997 Dec 1;505(Pt 2):473–491. doi: 10.1111/j.1469-7793.1997.473bb.x

Orally projecting interneurones in the guinea-pig small intestine.

S J Brookes 1, A C Meedeniya 1, P Jobling 1, M Costa 1
PMCID: PMC1160078  PMID: 9423187

Abstract

1. Orally projecting, cholinergic interneurones are important in mediating ascending excitatory reflexes in the small intestine. We have shown that there is just one major class of orally projecting interneurone, which we have characterized using retrograde labelling in organ culture, combined with immunohistochemistry, intracellular recording and dye filling. 2. Orally projecting interneurones, previously shown to be immunoreactive for choline acetyltransferase, tachykinins, enkephalin, calretinin and neurofilament protein triplet, have axons up to 14 mm long and are the only class of cells with orally directed axons more than 8.5 mm long. 3. They are all small Dogiel type I neurones with short dendrites, usually lamellar in form, and a single axon which sometimes bifurcates. Their axons give rise to short varicose collaterals in myenteric ganglia more than 3 mm oral to their cell bodies. 4. Orally projecting interneurones receive prominent fast excitatory post synaptic potentials (fast EPSPs). A major source of fast EPSPs is other ascending interneurones located further aborally. They also receive fast EPSPs from circumferential pathways. 5. In the stretched preparations used in this study, orally projecting interneurones were highly excitable, firing repeatedly to depolarizing current pulses and had negligible long after-hyperpolarizations following their action potentials. They did not receive measurable non-cholinergic slow excitatory synaptic inputs. 6. Ascending interneurones had a characteristic inflection in their membrane responses to depolarizing current pulses and their first action potential was typically delayed by approximately 30 ms. Under single electrode voltage clamp, ascending interneurones had a transient outward current when depolarized above -70 mV from more hyperpolarized holding potentials. Ascending interneurones also consistently showed marked inward rectification under both current clamp and voltage clamp conditions. 7. This class of cells has consistent morphological, neurochemical and electrophysiological characteristics and are important in mediating orally directed enteric reflexes.

Full text

PDF
473

Images in this article

Selected References

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

  1. Bayliss W. M., Starling E. H. The movements and innervation of the small intestine. J Physiol. 1899 May 11;24(2):99–143. doi: 10.1113/jphysiol.1899.sp000752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bornstein J. C., Hendriks R., Furness J. B., Trussell D. C. Ramifications of the axons of AH-neurons injected with the intracellular marker biocytin in the myenteric plexus of the guinea pig small intestine. J Comp Neurol. 1991 Dec 15;314(3):437–451. doi: 10.1002/cne.903140303. [DOI] [PubMed] [Google Scholar]
  3. Brookes S. J., Song Z. M., Ramsay G. A., Costa M. Long aboral projections of Dogiel type II, AH neurons within the myenteric plexus of the guinea pig small intestine. J Neurosci. 1995 May;15(5 Pt 2):4013–4022. doi: 10.1523/JNEUROSCI.15-05-04013.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brookes S. J., Song Z. M., Steele P. A., Costa M. Identification of motor neurons to the longitudinal muscle of the guinea pig ileum. Gastroenterology. 1992 Sep;103(3):961–973. doi: 10.1016/0016-5085(92)90030-3. [DOI] [PubMed] [Google Scholar]
  5. Brookes S. J., Steele P. A., Costa M. Calretinin immunoreactivity in cholinergic motor neurones, interneurones and vasomotor neurones in the guinea-pig small intestine. Cell Tissue Res. 1991 Mar;263(3):471–481. doi: 10.1007/BF00327280. [DOI] [PubMed] [Google Scholar]
  6. Brookes S. J., Steele P. A., Costa M. Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine. Neuroscience. 1991;42(3):863–878. doi: 10.1016/0306-4522(91)90050-x. [DOI] [PubMed] [Google Scholar]
  7. Cassell J. F., Clark A. L., McLachlan E. M. Characteristics of phasic and tonic sympathetic ganglion cells of the guinea-pig. J Physiol. 1986 Mar;372:457–483. doi: 10.1113/jphysiol.1986.sp016020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cassell J. F., McLachlan E. M. The effect of a transient outward current (IA) on synaptic potentials in sympathetic ganglion cells of the guinea-pig. J Physiol. 1986 May;374:273–288. doi: 10.1113/jphysiol.1986.sp016079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Costa M., Brookes S. J., Steele P. A., Gibbins I., Burcher E., Kandiah C. J. Neurochemical classification of myenteric neurons in the guinea-pig ileum. Neuroscience. 1996 Dec;75(3):949–967. doi: 10.1016/0306-4522(96)00275-8. [DOI] [PubMed] [Google Scholar]
  11. Costa M., Furness J. B. The peristaltic reflex: an analysis of the nerve pathways and their pharmacology. Naunyn Schmiedebergs Arch Pharmacol. 1976 Jul;294(1):47–60. doi: 10.1007/BF00692784. [DOI] [PubMed] [Google Scholar]
  12. Finkel A. S., Redman S. Theory and operation of a single microelectrode voltage clamp. J Neurosci Methods. 1984 Jun;11(2):101–127. doi: 10.1016/0165-0270(84)90029-3. [DOI] [PubMed] [Google Scholar]
  13. Furness J. B., Costa M., Miller R. J. Distribution and projections of nerves with enkephalin-like immunoreactivity in the guinea-pig small intestine. Neuroscience. 1983 Apr;8(4):653–664. doi: 10.1016/0306-4522(83)90001-5. [DOI] [PubMed] [Google Scholar]
  14. Furness J. B., Johnson P. J., Pompolo S., Bornstein J. C. Evidence that enteric motility reflexes can be initiated through entirely intrinsic mechanisms in the guinea-pig small intestine. Neurogastroenterol Motil. 1995 Jun;7(2):89–96. doi: 10.1111/j.1365-2982.1995.tb00213.x. [DOI] [PubMed] [Google Scholar]
  15. Galligan J. J., North R. A., Tokimasa T. Muscarinic agonists and potassium currents in guinea-pig myenteric neurones. Br J Pharmacol. 1989 Jan;96(1):193–203. doi: 10.1111/j.1476-5381.1989.tb11800.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Galligan J. J., Tatsumi H., Shen K. Z., Surprenant A., North R. A. Cation current activated by hyperpolarization (IH) in guinea pig enteric neurons. Am J Physiol. 1990 Dec;259(6 Pt 1):G966–G972. doi: 10.1152/ajpgi.1990.259.6.G966. [DOI] [PubMed] [Google Scholar]
  17. Grider J. R., Jin J. G. Distinct populations of sensory neurons mediate the peristaltic reflex elicited by muscle stretch and mucosal stimulation. J Neurosci. 1994 May;14(5 Pt 1):2854–2860. doi: 10.1523/JNEUROSCI.14-05-02854.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. HUKUHARA T., YAMAGAMI M., NAKAYAMA S. On the intestinal intrinsic reflexes. Jpn J Physiol. 1958 Mar 30;8(1):9–20. doi: 10.2170/jjphysiol.8.9. [DOI] [PubMed] [Google Scholar]
  19. Harris-Warrick R. M. Pattern generation. Curr Opin Neurobiol. 1993 Dec;3(6):982–988. doi: 10.1016/0959-4388(93)90171-t. [DOI] [PubMed] [Google Scholar]
  20. Hirst G. D., Holman M. E., Spence I. Two types of neurones in the myenteric plexus of duodenum in the guinea-pig. J Physiol. 1974 Jan;236(2):303–326. doi: 10.1113/jphysiol.1974.sp010436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hirst G. D., Johnson S. M., van Helden D. F. The calcium current in a myenteric neurone of the guinea-pig ileum. J Physiol. 1985 Apr;361:297–314. doi: 10.1113/jphysiol.1985.sp015647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hirst G. D. Mechanisms of peristalsis. Br Med Bull. 1979 Sep;35(3):263–268. doi: 10.1093/oxfordjournals.bmb.a071587. [DOI] [PubMed] [Google Scholar]
  23. Johnson P. J., Bornstein J. C., Yuan S. Y., Furness J. B. Analysis of contributions of acetylcholine and tachykinins to neuro-neuronal transmission in motility reflexes in the guinea-pig ileum. Br J Pharmacol. 1996 Jun;118(4):973–983. doi: 10.1111/j.1476-5381.1996.tb15495.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Johnson S. M., Katayama Y., North R. A. Slow synaptic potentials in neurones of the myenteric plexus. J Physiol. 1980 Apr;301:505–516. doi: 10.1113/jphysiol.1980.sp013220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kirchgessner A. L., Gershon M. D. Projections of submucosal neurons to the myenteric plexus of the guinea pig intestine: in vitro tracing of microcircuits by retrograde and anterograde transport. J Comp Neurol. 1988 Nov 22;277(4):487–498. doi: 10.1002/cne.902770403. [DOI] [PubMed] [Google Scholar]
  26. Kirchgessner A. L., Tamir H., Gershon M. D. Identification and stimulation by serotonin of intrinsic sensory neurons of the submucosal plexus of the guinea pig gut: activity-induced expression of Fos immunoreactivity. J Neurosci. 1992 Jan;12(1):235–248. doi: 10.1523/JNEUROSCI.12-01-00235.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kunze W. A., Bornstein J. C., Furness J. B. Identification of sensory nerve cells in a peripheral organ (the intestine) of a mammal. Neuroscience. 1995 May;66(1):1–4. doi: 10.1016/0306-4522(95)00067-s. [DOI] [PubMed] [Google Scholar]
  28. Morita K., North R. A., Katayama Y. Evidence that substance P is a neurotransmitter in the myenteric plexus. Nature. 1980 Sep 11;287(5778):151–152. doi: 10.1038/287151a0. [DOI] [PubMed] [Google Scholar]
  29. North R. A., Slack B. E., Surprenant A. Muscarinic M1 and M2 receptors mediate depolarization and presynaptic inhibition in guinea-pig enteric nervous system. J Physiol. 1985 Nov;368:435–452. doi: 10.1113/jphysiol.1985.sp015867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. North R. A., Tokimasa T. Muscarinic synaptic potentials in guinea-pig myenteric plexus neurones. J Physiol. 1982 Dec;333:151–156. doi: 10.1113/jphysiol.1982.sp014445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pompolo S., Furness J. B. Origins of synaptic inputs to calretinin immunoreactive neurons in the guinea-pig small intestine. J Neurocytol. 1993 Jul;22(7):531–546. doi: 10.1007/BF01189041. [DOI] [PubMed] [Google Scholar]
  32. Smith T. K., Bornstein J. C., Furness J. B. Distension-evoked ascending and descending reflexes in the circular muscle of guinea-pig ileum: an intracellular study. J Auton Nerv Syst. 1990 Mar;29(3):203–217. doi: 10.1016/0165-1838(90)90146-a. [DOI] [PubMed] [Google Scholar]
  33. Smith T. K., Furness J. B. Reflex changes in circular muscle activity elicited by stroking the mucosa: an electrophysiological analysis in the isolated guinea-pig ileum. J Auton Nerv Syst. 1988 Dec;25(2-3):205–218. doi: 10.1016/0165-1838(88)90025-2. [DOI] [PubMed] [Google Scholar]
  34. Song Z. M., Brookes S. J., Costa M. All calbindin-immunoreactive myenteric neurons project to the mucosa of the guinea-pig small intestine. Neurosci Lett. 1994 Oct 24;180(2):219–222. doi: 10.1016/0304-3940(94)90524-x. [DOI] [PubMed] [Google Scholar]
  35. Song Z. M., Brookes S. J., Costa M. Identification of myenteric neurons which project to the mucosa of the guinea-pig small intestine. Neurosci Lett. 1991 Aug 19;129(2):294–298. doi: 10.1016/0304-3940(91)90484-b. [DOI] [PubMed] [Google Scholar]
  36. Song Z. M., Brookes S. J., Costa M. Projections of specific morphological types of neurons within the myenteric plexus of the small intestine of the guinea-pig. Cell Tissue Res. 1996 Jul;285(1):149–156. doi: 10.1007/s004410050630. [DOI] [PubMed] [Google Scholar]
  37. Song Z. M., Brookes S. J., Ramsay G. A., Costa M. Characterization of myenteric interneurons with somatostatin immunoreactivity in the guinea-pig small intestine. Neuroscience. 1997 Oct;80(3):907–923. doi: 10.1016/s0306-4522(96)00605-7. [DOI] [PubMed] [Google Scholar]
  38. Song Z. M., Brookes S. J., Steele P. A., Costa M. Projections and pathways of submucous neurons to the mucosa of the guinea-pig small intestine. Cell Tissue Res. 1992 Jul;269(1):87–98. doi: 10.1007/BF00384729. [DOI] [PubMed] [Google Scholar]
  39. Stebbing M. J., Bornstein J. C. Electrophysiological mapping of fast excitatory synaptic inputs to morphologically and chemically characterized myenteric neurons of guinea-pig small intestine. Neuroscience. 1996 Aug;73(4):1017–1028. doi: 10.1016/0306-4522(96)00121-2. [DOI] [PubMed] [Google Scholar]
  40. Surprenant A. Control of the gastrointestinal tract by enteric neurons. Annu Rev Physiol. 1994;56:117–140. doi: 10.1146/annurev.ph.56.030194.001001. [DOI] [PubMed] [Google Scholar]
  41. Tonini M., Costa M. A pharmacological analysis of the neuronal circuitry involved in distension-evoked enteric excitatory reflex. Neuroscience. 1990;38(3):787–795. doi: 10.1016/0306-4522(90)90071-b. [DOI] [PubMed] [Google Scholar]
  42. Waterman S. A., Tonini M., Costa M. The role of ascending excitatory and descending inhibitory pathways in peristalsis in the isolated guinea-pig small intestine. J Physiol. 1994 Nov 15;481(Pt 1):223–232. doi: 10.1113/jphysiol.1994.sp020433. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES