Skip to main content
Log in

Projections and chemistry of Dogiel type II neurons in the mouse colon

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The physiological properties, shapes, projections and neurochemistries of Dogiel type II neurons have been thoroughly investigated in the guinea-pig intestine in which these neurons have been identified as intrinsic primary afferent neurons. Dogiel type II neurons in the myenteric ganglia of mice have similar physiological properties to those in guinea-pigs but whether other features of the neurons are similar is unknown. We have used intracellular dye-filling, retrograde tracing, immunohistochemistry and nerve lesions to determine salient features of Dogiel type II neurons of the mouse colon. Dye-filling showed that the neurons provide profuse terminal networks in the myenteric ganglia and also have axons that project towards the mucosa. Retrograde tracing and lesion studies showed that these axons provide direct innervation to the mucosa. High proportions of the neurons had immunoreactivity for calretinin, calbindin, choline acetyltransferase, the purine P2X2 receptor and calcitonin gene-related peptide (CGRP). CGRP was the most selective marker of the neurons. Following surgery to remove an area of myenteric plexus, the CGRP-immunoreactive nerve fibres in the mucosa degenerated. Thus, Dogiel type II neurons in mice have similar shapes and projections but some differences in chemistry from those in guinea-pigs. The close similarities between the two species in the shapes, projections and electrophysiology of these neurons suggest that they serve the same functions in both species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–J
Fig. 2
Fig. 3A–C
Fig. 4A–D
Fig. 5A–E
Fig. 6A, B
Fig. 7A–G

Similar content being viewed by others

References

  • Bertrand PP, Kunze WAA, Bornstein JC, Furness JB (1998) Electrical mapping of the projections of intrinsic primary afferent neurons to the mucosa of the guinea-pig small intestine. Neurogastroenterol Motil 10:533–541

    Article  PubMed  Google Scholar 

  • Bian X, Ren J, DeVries M, Schnegelsberg B, Cockayne DA, Ford APDW, Galligan JJ (2003) Peristalsis is impaired in the small intestine of mice lacking the P2X3 subunit. J Physiol (Lond) 551:309–322

    Article  CAS  Google Scholar 

  • Boettger MK, Till S, Chen MX, Anand U, Otto WR, Plumpton C, Trezise DJ, Tate SN, Bountra C, Coward K, Birch R, Anand P (2002) Calcium-activated potassium channel SK1- and IK1-like immunoreactivity in injured human sensory neurones and its regulation by neurotrophic factors. Brain 125:252–263

    Article  CAS  PubMed  Google Scholar 

  • Bornstein JC, Hendriks R, Furness JB, Trussell DC (1991) 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 314:437–451

    CAS  PubMed  Google Scholar 

  • Brehmer A, Schrodl F, Neuhuber W (1999a) Morphological classifications of enteric neurons-100 years after Dogiel. Anat Embryol 200:125–135

    Article  PubMed  Google Scholar 

  • Brehmer A, Schrödl F, Neuhuber W, Hens J, Timmermans J-P (1999b) Comparison of enteric neuronal morphology as demonstrated by Dil-tracing under different tissue-handling conditions. Anat Embryol 199:57–62

    Article  CAS  PubMed  Google Scholar 

  • Brehmer A, Blaser B, Seitz G, Schrodl F, Neuhuber W (2004) Pattern of lipofuscin pigmentation in nitrergic and non-nitrergic neurofilament immunoreactive myenteric neuron types in human small intestine. Histochem Cell Biol 121:13–20

    Article  CAS  PubMed  Google Scholar 

  • Brookes SJH, Ewart WR, Wingate DL (1987) Intracellular recordings from myenteric neurones in the human colon. J Physiol (Lond) 390:305–318

    CAS  Google Scholar 

  • Brookes SJH, Steele PA, Costa M (1991) Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine. Neuroscience 42:863–878

    CAS  PubMed  Google Scholar 

  • Browning KN, Lees GM (1996) Myenteric neurons of the rat descending colon; electrophysiological and correlated morphological properties. Neuroscience 73:1029–1047

    Article  CAS  PubMed  Google Scholar 

  • Castelucci P, Robbins HL, Poole DP, Furness JB (2002) The distribution of purine P2X2 receptors in the guinea pig enteric nervous system. Histochem Cell Biol 117:415–422

    CAS  PubMed  Google Scholar 

  • Chiocchetti R, Poole DP, Kimura H, Aimi Y, Robbins HL, Castelucci P, Furness JB (2003) Evidence that two forms of choline acetyltransferase are differentially expressed in subclasses of enteric neurons. Cell Tissue Res 311:11–22

    Article  CAS  PubMed  Google Scholar 

  • Clerc N, Furness JB, Bornstein JC, Kunze WAA (1998) Correlation of electrophysiological and morphological characteristics of myenteric neurons of the duodenum in the guinea-pig. Neuroscience 82:899–914

    Article  CAS  PubMed  Google Scholar 

  • Cornelissen W, Laet A de, Kroese ABA, Van Bogaert P-P, Scheuermann DW, Timmermans J-P (2000) Electrophysiological features of morphological Dogiel type II neurons in the myenteric plexus of pig small intestine. J Neurophysiol 84:102–111

    CAS  PubMed  Google Scholar 

  • Costa M, Brookes SJH, Steele PA, Gibbins I, Burcher E, Kandiah CJ (1996) Neurochemical classification of myenteric neurons in the guinea-pig ileum. Neuroscience 75:949–967

    Article  CAS  PubMed  Google Scholar 

  • Dogiel AS (1899) Über den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugetiere. Arch Anat Physiol Leipzig Anat Abt Jg 1899:130–158

    Google Scholar 

  • Erde SM, Sherman D, Gershon MD (1985) Morphology and serotonergic innervation of physiologically identified cells of the guinea pig’s myenteric plexus. J Neurosci 5:617–633

    CAS  PubMed  Google Scholar 

  • Fairman CL, Clagett-Dame M, Lennon VA, Epstein ML (1995) Appearance of neurons in the developing chick gut. Dev Dyn 204:192–201

    CAS  PubMed  Google Scholar 

  • Furness JB, Bornstein JC, Trussell DC (1988) Shapes of nerve cells in the myenteric plexus of the guinea-pig small intestine revealed by the intracellular injection of dye. Cell Tissue Res 254:561–571

    CAS  PubMed  Google Scholar 

  • Furness JB, Trussell DC, Pompolo S, Bornstein JC, Smith TK (1990) Calbindin neurons of the guinea-pig small intestine: quantitative analysis of their numbers and projections. Cell Tissue Res 260:261–272

    CAS  PubMed  Google Scholar 

  • Furness JB, Kunze WAA, Bertrand PP, Clerc N, Bornstein JC (1998) Intrinsic primary afferent neurons of the intestine. Prog Neurobiol 54:1–18

    CAS  PubMed  Google Scholar 

  • Furness JB, Robbins HL, Selmer I-S, Hunne B, Chen MX, Hicks GA, Moore S, Neylon CB (2003) Expression of intermediate conductance potassium channel immunoreactivity in neurons and epithelial cells of the rat gastrointestinal tract. Cell Tissue Res 314:179–189

    Google Scholar 

  • Furness JB, Jones C, Nurgali K, Clerc N (2004) Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol 72:143–164

    Article  CAS  PubMed  Google Scholar 

  • Gershon MD (1999) Lessons from genetically engineered animal models. II. Disorders of enteric neuronal development: insights from transgenic mice. Am J Physiol 277:G262–G267

    CAS  PubMed  Google Scholar 

  • Grider JR (1994) CGRP as a transmitter in the sensory pathway mediating peristaltic reflex. Am J Physiol 266:G1139–G1145

    CAS  PubMed  Google Scholar 

  • Hens J, Schrödl F, Brehmer A, Adriaensen D, Neuhuber W, Scheuermann DW, Schemann M, Timmermans J-P (2000) Mucosal projections of enteric neurons in the porcine small intestine. J Comp Neurol 421:426–436

    Article  Google Scholar 

  • Hens J, Vanderwinden J-M, De Laet MH, Scheuermann DW, Timmermans J-P (2001) Morphological and neurochemical identification of enteric neurones with mucosal projections in the human small intestine. J Neurochem 76:464–471

    Article  CAS  PubMed  Google Scholar 

  • Kirchgessner AL, Gershon MD (1988) 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 277:487–498

    CAS  PubMed  Google Scholar 

  • Kunze WAA, Furness JB, Bornstein JC (1993) Simultaneous intracellular recordings from enteric neurons reveal that myenteric AH neurons transmit via slow excitatory postsynaptic potentials. Neuroscience 55:685–694

    Article  CAS  PubMed  Google Scholar 

  • Li ZS, Furness JB (1998) Immunohistochemical localization of cholinergic markers in putative intrinsic primary afferent neurons of the guinea-pig small intestine. Cell Tissue Res 294:35–43

    CAS  PubMed  Google Scholar 

  • Lomax AEG, Furness JB (2000) Neurochemical classification of enteric neurons in the guinea-pig distal colon. Cell Tissue Res 302:59–73

    CAS  PubMed  Google Scholar 

  • Lomax AEG, Sharkey KA, Bertrand PP, Low AM, Bornstein JC, Furness JB (1999) Correlation of morphology, electrophysiology and chemistry of neurons in the myenteric plexus of the guinea-pig distal colon. J Auton Nerv Syst 76:45–61

    Article  CAS  PubMed  Google Scholar 

  • Mann PT, Southwell BR, Ding YQ, Shigemoto R, Mizuno N, Furness JB (1997) Localisation of neurokinin 3 (NK3) receptor immunoreactivity in the rat gastrointestinal tract. Cell Tissue Res 289:1–9

    Article  CAS  PubMed  Google Scholar 

  • Mann PT, Furness JB, Southwell BR (1999) Choline acetyltransferase immunoreactivity of putative intrinsic primary afferent neurons in the rat ileum. Cell Tissue Res 297:241–248

    CAS  PubMed  Google Scholar 

  • Messenger JP, Furness JB (1990) Projections of chemically-specified neurons in the guinea-pig colon. Arch Histol Cytol 53:467–495

    CAS  PubMed  Google Scholar 

  • Neunlist M, Schemann M (1997) Projections and neurochemical coding of myenteric neurons innervating the mucosa of the guinea pig proximal colon. Cell Tissue Res 287:119–125

    CAS  PubMed  Google Scholar 

  • Nurgali K, Furness JB, Stebbing MJ (2003) Correlation of electrophysiology, shape and synaptic properties of myenteric AH neurons of the guinea-pig distal colon. Auton Neurosci 103:50–64

    Article  PubMed  Google Scholar 

  • Nurgali K, Stebbing MJ, Furness JB (2004) Correlation of electrophysiological and morphological characteristics of enteric neurons in the mouse colon. J Comp Neurol 468:112–124

    Article  PubMed  Google Scholar 

  • Pompolo S, Furness JB (1988) Ultrastructure and synaptic relationships of calbindin-reactive, Dogiel type II neurons, in myenteric ganglia of guinea-pig small intestine. J Neurocytol 17:771–782

    CAS  PubMed  Google Scholar 

  • Sang Q, Young HM (1996) Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 284:39–53

    Article  CAS  PubMed  Google Scholar 

  • Sang Q, Williamson S, Young HM (1997) Projections of chemically identified myenteric neurons of the small and large intestine of the mouse. J Anat 190:209–222

    Article  CAS  PubMed  Google Scholar 

  • Scheuermann DW, Stach W, Timmermans JP, Adriaensen D, De Groodt Lasseel MHA (1991) Calbindin D-28k in the enteric nervous system of the pig and its coexistence with 5-hydroxytryptamine. Verh Anat Ges 84:369–370

    Google Scholar 

  • Song ZM, Brookes SJH, Costa M (1991) Identification of myenteric neurons which project to the mucosa of the guinea-pig small intestine. Neurosci Lett 129:294–298

    CAS  Google Scholar 

  • Song ZM, Brookes SJH, Costa M (1994) All calbindin-immunoreactive myenteric neurons project to the mucosa of the guinea-pig small intestine. Neurosci Lett 180:219–222

    CAS  Google Scholar 

  • Song ZM, Brookes SJH, Costa M (1996) Projections of specific morphological types of neurons within the myenteric plexus of the small intestine of the guinea-pig. Cell Tissue Res 285:149–156

    Google Scholar 

  • Stach W (1981) Zur neuronalen Organisation des Plexus myentericus Auerbach im Schweinedünndarm II Typ II-neurone. Z Mikrosk Anat Forsch 95:161–192

    CAS  PubMed  Google Scholar 

  • Stach W (1989) A revised morphological classification of neurons in the enteric nervous system. In: Singer MV, Goebell H (eds) Nerves and the gastrointestinal tract. MTP, Lancaster, pp 29–45

  • Stewart AL, Anderson RB, Young HM (2003) Characterization of lacZ-expressing cells in the gut of embryonic and adult DβH-nlacZ mice. J Comp Neurol 464:208–219

    Article  PubMed  Google Scholar 

  • Tamura K, Ito H, Wade PR (2001) Morphology, electrophysiology, and calbindin immunoreactivity of myenteric neurons in the guinea pig distal colon. J Comp Neurol 437:423–437

    Google Scholar 

  • Tooyama I, Kimura H (2000) A protein encoded by an alternative splice variant of choline acetyltransferase mRNA is localized preferentially in peripheral nerve cells and fibers. J Chem Neuroanat 17:217–226

    CAS  PubMed  Google Scholar 

  • Van Nassauw L, Hens J, Bogers J, VanMarck E, Timmermans J-P (2000) Retrograde DiI tracing of enteric neurons projecting to the mucosa in the murine small intestine. In: Krammer H-J, Singer MV (eds) Neurogastroenterology, from the basics to the clinics. Kluwer, Dordrecht, pp 92–95

  • Vogalis F, Hillsley K, Smith T (2000) Recording ionic events from cultured, DiI-labelled myenteric neurons in the guinea-pig proximal colon. J Neurosci Methods 96:25–34

    Article  CAS  PubMed  Google Scholar 

  • Walters JRF, Bishop AE, Facer P, Lawson DEM, Rogers JH, Polak JM (1993) Calretinin and calbindin-D28k immunoreactivity in the human gastrointestinal tract. Gastroenterology 104:1381–1389

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

These studies were funded by the National Health and Medical Research Council (Australia). We thank Michelle Thacker and Marine Corniou for their assistance with experiments. We are also grateful to Dr. Mao X. Chen for supplying the anti-IK antibody (M20) and Prof. Hiroshi Kimura for the anti-pChAT antiserum. Preliminary experiments to locate pChAT in mouse enteric neurons were conducted by Dr. Roberto Chiocchetti.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John B. Furness.

Additional information

These studies were funded by the National Health and Medical Research Council (Australia)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Furness, J.B., Robbins, H.L., Xiao, J. et al. Projections and chemistry of Dogiel type II neurons in the mouse colon. Cell Tissue Res 317, 1–12 (2004). https://doi.org/10.1007/s00441-004-0895-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-004-0895-5

Keywords

Navigation