Skip to main content

Extrinsic Sensory Innervation of the Gut: Structure and Function

  • Chapter
  • First Online:
The Enteric Nervous System

Part of the book series: Advances in Experimental Medicine and Biology ((ANS,volume 891))

Abstract

Extrinsic sensory neurons play a key role in the function of the gastrointestinal tract. They are responsible for the sensations that arise in the gut and can initiate automatic reflexes. In some cases, disordered sensation is clinically problematic—pain, bloating, excessive urgency and nausea are well-known examples. Major advances have been made in understanding the function of somatic sensory neurons in the last 50 years. However, the sensory neurons that mediate sensations from the viscera remain less well understood. This is partly because viscera receive a dense autonomic innervation that can be difficult to separate from extrinsic sensory neurons. A key requirement to understand the genesis of sensation is to distinguish the different classes of sensory neurons and the types of stimuli which they encode. The aim of this short paper is to summarise what was known about these matters 30 years ago and highlight some of the major advances in the understanding of the types of extrinsic sensory neurons to the gut. Necessarily, the choice of papers is somewhat idiosyncratic, but they illustrate the range of advances that have been made in distinguishing the different classes of gastrointestinal afferent nerves.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, Collins SM, Corinaldesi R (2004) Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126:693–702

    Article  PubMed  Google Scholar 

  • Bayliss WM (1901) On the origin from the spinal cord of the vaso-dilator fibres of the hind-limb, and on the nature of these fibres. J Physiol 26:173–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berthoud HR, Kressel M, Raybould HE, Neuhuber WL (1995) Vagal sensors in the rat duodenal mucosa – distribution and structure as revealed by in vivo Dii-tracing. Anat Embryol (Berl) 191:203–212

    Article  CAS  Google Scholar 

  • Berthoud HR, Patterson LM, Neumann F, Neuhuber WL (1997) Distribution and structure of vagal afferent intraganglionic laminar endings (IGLEs) in the rat gastrointestinal tract. Anat Embryol (Berl) 195:183–191

    Article  CAS  Google Scholar 

  • Berthoud HR, Lynn PA, Blackshaw LA (2001) Vagal and spinal mechanosensors in the rat stomach and colon have multiple receptive fields. Am J Physiol Regul Integr Comp Physiol 280:R1371–R1381

    CAS  PubMed  Google Scholar 

  • Berthoud HR, Blackshaw LA, Brookes SJ, Grundy D (2004) Neuroanatomy of extrinsic afferents supplying the gastrointestinal tract. Neurogastroenterol Motil 16(Suppl 1):28–33

    Article  PubMed  Google Scholar 

  • Bessou P, Perl ER (1966) A movement receptor of the small intestine. J Physiol 182:404–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beyak MJ, Bulmer DCE, Jiang W, Keating C, Rong W, Grundy D (2006) Extrinsic afferent nerves innervating the gastrointestinal tract. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 4th edn. Academic, San Diego

    Google Scholar 

  • Blackshaw LA, Gebhart GF (2002) The pharmacology of gastrointestinal nociceptive pathways. Curr Opin Pharmacol 2:642–649

    Article  CAS  PubMed  Google Scholar 

  • Blackshaw LA, Grundy D (1990) Effects of cholecystokinin (CCK-8) on two classes of gastroduodenal vagal afferent fibre. J Auton Nerv Syst 31:191–201

    Article  CAS  PubMed  Google Scholar 

  • Brierley SM, Jones RC 3rd, Gebhart GF, Blackshaw LA (2004) Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127:166–178

    Article  PubMed  Google Scholar 

  • Brierley SM, Carter R, Jones W 3rd, Xu L, Robinson DR, Hicks GA, Gebhart GF, Blackshaw LA (2005) Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 567:267–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brierley SM, Hughes PA, Harrington A, Blackshaw LA (2012) Innervation of the gastrointestinal tract by spinal and vagal afferent nerves. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 5th edn. Elsevier, Amsterdam, pp 703–731

    Chapter  Google Scholar 

  • Cervero F, Sharkey KA (1988) An electrophysiological and anatomical study of intestinal afferent fibres in the rat. J Physiol 401:381–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke GD, Davison JS (1978) Mucosal receptors in the gastric antrum and small intestine of the rat with afferent fibres in the cervical vagus. J Physiol 284:55–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clifton GL, Coggeshall RE, Vance WH, Willis WD (1976) Receptive fields of unmyelinated ventral root afferent fibres in the cat. J Physiol 256:573–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coggeshall RE, Ito H (1977) Sensory fibres in ventral roots L7 and Si in the cat. J Physiol 267:215–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doerffler-Melly J, Neuhuber WL (1988) Rectospinal neurons: evidence for a direct projection from the enteric to the central nervous system in the rat. Neurosci Lett 92:121–125

    Article  CAS  PubMed  Google Scholar 

  • Eastwood C, Maubach K, Kirkup AJ, Grundy D (1998) The role of endogenous cholecystokinin in the sensory transduction of luminal nutrient signals in the rat jejunum. Neurosci Lett 254:145–148

    Article  CAS  PubMed  Google Scholar 

  • Feng B, Gebhart GF (2011) Characterization of silent afferents in the pelvic and splanchnic innervations of the mouse colorectum. Am J Physiol 300:G170–G180

    CAS  Google Scholar 

  • Feng B, La JH, Schwartz ES, Tanaka T, McMurray TP, Gebhart GF (2012) Long-term sensitization of mechanosensitive and -insensitive afferents in mice with persistent colorectal hypersensitivity. Am J Physiol 302:G676–G683

    Article  CAS  Google Scholar 

  • Floyd K, Morrison JF (1974) Splanchnic mechanoreceptors in the dog. Q J Exp Physiol Cogn Med Sci 59:361–366

    CAS  PubMed  Google Scholar 

  • Fox EA, Phillips RJ, Martinson FA, Baronowsky EA, Powley TL (2000) Vagal afferent innervation of smooth muscle in the stomach and duodenum of the mouse: morphology and topography. J Comp Neurol 428:558–576

    Article  CAS  PubMed  Google Scholar 

  • Gibbins IL, Furness JB, Costa M, MacIntyre I, Hillyard CJ, Girgis S (1985) Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 57:125–130

    Article  CAS  PubMed  Google Scholar 

  • Grundy D, Al-Chaer ED, Aziz Q, Collins SM, Ke M, Tache Y, Wood JD (2006) Fundamentals of neurogastroenterology: basic science. Gastroenterology 130:1391–1411

    Article  CAS  PubMed  Google Scholar 

  • Hibberd TJ, Zagorodnyuk VP, Spencer NJ, Brookes SJH (2012a) Identification and mechanosensitivity of viscerofugal neurons. Neuroscience 225:118–129

    Google Scholar 

  • Hibberd TJ, Zagorodnyuk VP, Spencer NJ, Brookes SJH (2012b) Viscerofugal neurons recorded from guinea-pig colonic nerves after organ culture. Neurogastroenterol Motil 24:1041-e1548

    Google Scholar 

  • Hibberd TJ, Spencer NJ, Zagorodnyuk VP, Chen BN, Brookes SJ (2014) Targeted electrophysiological analysis of viscerofugal neurons in the myenteric plexus of guinea-pig colon. Neuroscience 275:272–284

    Article  CAS  PubMed  Google Scholar 

  • Hughes PA, Brierley SM, Blackshaw LA (2009) Post-inflammatory modification of colonic afferent mechanosensitivity. Clin Exp Pharmacol Physiol 36:1034–1040

    Article  CAS  PubMed  Google Scholar 

  • Humenick A, Chen BN, Wiklendt L, Spencer NJ, Zagorodnyuk VP, Dinning PG, Costa M, Brookes SJ (2015) Activation of intestinal spinal afferent endings by changes in intra-mesenteric arterial pressure. J Physiol 593:3693–3709

    Article  CAS  PubMed  Google Scholar 

  • Iggo A (1955) Tension receptors in the stomach and the urinary bladder. J Physiol 128:593–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawasaki H, Takasaki K, Saito A, Goto K (1988) Calcitonin gene-related peptide acts as a novel vasodilator neurotransmitter in mesenteric resistance vessels of the rat. Nature 335:164–167

    Article  CAS  PubMed  Google Scholar 

  • Kuramoto H, Furness JB (1989) Distribution of enteric nerve cells that project from the small intestine to the coeliac ganglion in the guinea-pig. J Auton Nerv Syst 27:241–248

    Article  CAS  PubMed  Google Scholar 

  • Longhurst JC, Dittman LE (1987) Hypoxia, bradykinin, and prostaglandins stimulate ischemically sensitive visceral afferents. Am J Physiol 253:H556–H567

    CAS  PubMed  Google Scholar 

  • Lynn PA, Blackshaw LA (1999) In vitro recordings of afferent fibres with receptive fields in the serosa, muscle and mucosa of rat colon. J Physiol 518:271–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynn PA, Brookes SJH (2011) Function and morphology correlates of rectal nerve mechanoreceptors innervating the guinea pig internal anal sphincter. Neurogastroenterol Motil 23:88–95

    Article  CAS  PubMed  Google Scholar 

  • Lynn PA, Olsson C, Zagorodnyuk V, Costa M, Brookes SJ (2003) Rectal intraganglionic laminar endings are transduction sites of extrinsic mechanoreceptors in the guinea pig rectum. Gastroenterology 125:786–794

    Article  PubMed  Google Scholar 

  • Lynn PA, Chen BN, Zagorodnyuk VP, Costa M, Brookes SJH (2008) TNBS-induced inflammation modulates the function of one class of low-threshold rectal mechanoreceptors in the guinea pig. Am J Physiol 295:G862–G871

    CAS  Google Scholar 

  • Meehan AG, Kreulen DL (1992) A capsaicin-sensitive inhibitory reflex from the colon to mesenteric arteries in the guinea-pig. J Physiol 448:153–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messenger JP, Furness JB (1993) Distribution of enteric nerve cells projecting to the superior and inferior mesenteric ganglia of the guinea-pig. Cell Tissue Res 271:333–339

    Article  CAS  PubMed  Google Scholar 

  • Morrison JF (1973) Splanchnic slowly adapting mechanoreceptors with punctate receptive fields in the mesentery and gastrointestinal tract of the cat. J Physiol 233:349–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paintal A (1954) A study of gastric stretch receptors; their role in the peripheral mechanism of satiation of hunger and thirst. J Physiol 126:255–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryall RW, Piercey MF (1970) Visceral afferent and efferent fibers in sacral ventral roots in cats. Brain Res 23:57–65

    Article  CAS  PubMed  Google Scholar 

  • Sengupta JN (2000) An overview of esophageal sensory receptors. Am J Med 108(Suppl 4a):87S–89S

    Article  PubMed  Google Scholar 

  • Sengupta JN, Saha JK, Goyal RK (1992) Differential sensitivity to bradykinin of esophageal distension-sensitive mechanoreceptors in vagal and sympathetic afferents of the opossum. J Neurophysiol 68:1053–1067

    CAS  PubMed  Google Scholar 

  • Song X, Chen BN, Zagorodnyuk VP, Lynn PA, Blackshaw LA, Grundy D, Brunsden AM, Costa M, Brookes SJH (2009) Identification of medium/high-threshold extrinsic mechanosensitive afferent nerves to the gastrointestinal tract. Gastroenterology 137:274–284

    Article  PubMed  PubMed Central  Google Scholar 

  • Su X, Gebhart GF (1998) Mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat are polymodal in character. J Neurophysiol 80:2632–2644

    CAS  PubMed  Google Scholar 

  • Tassicker BC, Hennig GW, Costa M, Brookes SJH (1999) Rapid anterograde and retrograde tracing from mesenteric nerve trunks to the guinea-pig small intestine in vitro. Cell Tissue Res 295:437–452

    Article  CAS  PubMed  Google Scholar 

  • Tornblom H, Lindberg G, Nyberg B, Veress B (2002) Full-thickness biopsy of the jejunum reveals inflammation and enteric neuropathy in irritable bowel syndrome [see comment]. Gastroenterology 123:1972–1979

    Article  PubMed  Google Scholar 

  • Wahnschaffe U, Ullrich R, Riecken EO, Schulzke JD (2001) Celiac disease-like abnormalities in a subgroup of patients with irritable bowel syndrome. Gastroenterology 121:1329–1338

    Article  CAS  PubMed  Google Scholar 

  • Yu S, Undem BJ, Kollarik M (2005) Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus. J Physiol 563:831–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zagorodnyuk VP, Brookes SJ (2000) Transduction sites of vagal mechanoreceptors in the guinea pig esophagus. J Neurosci 20:6249–6255

    CAS  PubMed  Google Scholar 

  • Zagorodnyuk VP, Chen BN, Brookes SJ (2001) Intraganglionic laminar endings are mechano-transduction sites of vagal tension receptors in the guinea-pig stomach. J Physiol 534:255–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Simon Brookes .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Brookes, S., Chen, N., Humenick, A., Spencer, N.J., Costa, M. (2016). Extrinsic Sensory Innervation of the Gut: Structure and Function. In: Brierley, S., Costa, M. (eds) The Enteric Nervous System. Advances in Experimental Medicine and Biology(), vol 891. Springer, Cham. https://doi.org/10.1007/978-3-319-27592-5_7

Download citation

Publish with us

Policies and ethics