FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Histochem Cell Biol / Excitatory and inhibitory enteric innervation of horse lower...
Histochemistry and cell biology2015; 143(6); 625-635; doi: 10.1007/s00418-014-1306-y

Excitatory and inhibitory enteric innervation of horse lower esophageal sphincter.

Abstract: The lower esophageal sphincter (LES) is a specialized, thickened muscle region with a high resting tone mediated by myogenic and neurogenic mechanisms. During swallowing or belching, the LES undergoes strong inhibitory innervation. In the horse, the LES seems to be organized as a "one-way" structure, enabling only the oral-anal progression of food. We characterized the esophageal and gastric pericardial inhibitory and excitatory intramural neurons immunoreactive (IR) for the enzymes neuronal nitric oxide synthase (nNOS) and choline acetyltransferase. Large percentages of myenteric plexus (MP) and submucosal (SMP) plexus nNOS-IR neurons were observed in the esophagus (72 ± 9 and 69 ± 8 %, respectively) and stomach (57 ± 17 and 45 ± 3 %, respectively). In the esophagus, cholinergic MP and SMP neurons were 29 ± 14 and 65 ± 24 vs. 36 ± 8 and 38 ± 20 % in the stomach, respectively. The high percentage of nitrergic inhibitory motor neurons observed in the caudal esophagus reinforces the role of the enteric nervous system in the horse LES relaxation. These findings might allow an evaluation of whether selective groups of enteric neurons are involved in horse neurological disorders such as megaesophagus, equine dysautonomia, and white lethal foal syndrome.
Get Full Text
Publication Date: 2015-01-13 PubMed ID: 25578519DOI: 10.1007/s00418-014-1306-yGoogle Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article is mainly about the investigation of how neural innervation and certain enzymes control the relaxation mechanism of the lower esophagus in horses—information that might aid understanding of certain horse neurological diseases.

Introduction

  • The lower esophageal sphincter (LES) is a portion of the esophagus responsible for allowing food to go one way—from the mouth to the stomach. It has unique muscle structures that allow it to maintain high resting tone, which means it’s usually tightened or closed and only relaxes during swallowing or belching.
  • The study sought to investigate how this relaxation is triggered, specifically in horses, and provide insights that might help understand some neurological disorders in horses.

Investigation on Enzymes

  • The researchers focused on two enzymes produced by the neurons in the LES: neuronal nitric oxide synthase (nNOS) and choline acetyltransferase.
  • nNOS is believed to have inhibitory motor function, meaning it causes the muscles to relax. Choline acetyltransferase, on the other hand, is thought to trigger excitation of the neurons, which might be involved in the very process of triggering muscle contraction.

Study Findings

  • The study used immunoreactive techniques and found a significant presence of nNOS in the neurons of the LES in the esophagus and stomach—72 ± 9 % and 69 ± 8 % respectively for myenteric plexus (MP) and submucosal (SMP) plexus; 57 ± 17 and 45 ± 3 % respectively in the stomach.
  • Choline acetyltransferase was found in lower percentages: 29 ± 14 % and 65 ± 24 % in the esophagus, 36 ± 8 and 38 ± 20 % in the stomach for the same plexuses.
  • The high prevalence of nNOS-IR neurons, which are linked to inhibitory motor function, implies that nNOS has a significant role in the relaxation of the LES in horses.

Remifications and Future Work

  • The study provides insights into which enteric neurons could be implicated in horse neurological conditions such as megaesophagus (a condition where the esophagus becomes enlarged), equine dysautonomia (abnormal functioning of the autonomic nervous system), and white lethal foal syndrome (a genetic disorder in horses).

Cite This Article

APA
Chiocchetti R, Giancola F, Mazzoni M, Sorteni C, Romagnoli N, Pietra M. (2015). Excitatory and inhibitory enteric innervation of horse lower esophageal sphincter. Histochem Cell Biol, 143(6), 625-635. https://doi.org/10.1007/s00418-014-1306-y

Publication

Histochemistry and cell biology
ISSN: 1432-119X
NlmUniqueID: 9506663
Country: Germany
Language: English
Volume: 143
Issue: 6
Pages: 625-635

Researcher Affiliations

Chiocchetti, R
  • Department of Veterinary Medical Sciences (UNI EN ISO 9001:2008), University of Bologna, Via Tolara di Sopra 50, 40064, Ozzano dell'Emilia, Bologna, Italy, roberto.chiocchetti@unibo.it.
Giancola, F
    Mazzoni, M
      Sorteni, C
        Romagnoli, N
          Pietra, M

            MeSH Terms

            • Animals
            • Choline O-Acetyltransferase / metabolism
            • Enteric Nervous System / metabolism
            • Esophageal Diseases / metabolism
            • Esophageal Sphincter, Lower / metabolism
            • Esophagus / metabolism
            • Gastric Mucosa / metabolism
            • Horses
            • Myenteric Plexus / metabolism
            • Neurons / metabolism
            • Nitric Oxide Synthase Type I / metabolism
            • Submucous Plexus / metabolism

            References

            This article includes 64 references
            1. Clark ES, Morris DD, Whitlock RH. Esophageal manometry in horses, cows, and sheep during deglutition.. Am J Vet Res 1987 Apr;48(4):547-51.
              pubmed: 3592352
            2. Furness JB, Lloyd KC, Sternini C, Walsh JH. Projections of substance P, vasoactive intestinal peptide and tyrosine hydroxylase immunoreactive nerve fibres in the canine intestine, with special reference to the innervation of the circular muscle.. Arch Histol Cytol 1990 May;53(2):129-40.
              pubmed: 1695512doi: 10.1679/aohc.53.129google scholar: lookup
            3. Goyal RK, Rattan S. Nature of the vagal inhibitory innervation to the lower esophageal sphincter.. J Clin Invest 1975 May;55(5):1119-26.
              pubmed: 164484doi: 10.1172/JCI108013google scholar: lookup
            4. Noorian AR, Taylor GM, Annerino DM, Greene JG. Neurochemical phenotypes of myenteric neurons in the rhesus monkey.. J Comp Neurol 2011 Dec 1;519(17):3387-401.
              pubmed: 21618236doi: 10.1002/cne.22679google scholar: lookup
            5. Collman PI, Tremblay L, Diamant NE. The distribution of spinal and vagal sensory neurons that innervate the esophagus of the cat.. Gastroenterology 1992 Sep;103(3):817-22.
              pubmed: 1499932doi: 10.1016/0016-5085(92)90012-ngoogle scholar: lookup
            6. Freytag C, Seeger J, Siegemund T, Grosche J, Grosche A, Freeman DE, Schusser GF, Härtig W. Immunohistochemical characterization and quantitative analysis of neurons in the myenteric plexus of the equine intestine.. Brain Res 2008 Dec 9;1244:53-64.
              pubmed: 18930715doi: 10.1016/j.brainres.2008.09.070google scholar: lookup
            7. Boeckxstaens GE. The lower oesophageal sphincter.. Neurogastroenterol Motil 2005 Jun;17 Suppl 1:13-21.
              pubmed: 15836451doi: 10.1111/j.1365-2982.2005.00661.xgoogle scholar: lookup
            8. Rodrigo J, Uttenthal LO, Peinado MA, Esteban FJ, Fernández AP, Serrano J, Martínez de Velasco J, Santacana M, Bentura ML, Martínez-Murillo R, Pedrosa JA. Distribution of nitric oxide synthase in the esophagus of the cat and monkey.. J Auton Nerv Syst 1998 Jun 10;70(3):164-79.
              pubmed: 9700059doi: 10.1016/s0165-1838(98)00053-8google scholar: lookup
            9. Seelig LL Jr, Doody P, Brainard L, Gidda JS, Goyal RK. Acetylcholinesterase and choline acetyltransferase staining of neurons in the opossum esophagus.. Anat Rec 1984 May;209(1):125-30.
              pubmed: 6203439doi: 10.1002/ar.1092090115google scholar: lookup
            10. Collman PI, Tremblay L, Diamant NE. The central vagal efferent supply to the esophagus and lower esophageal sphincter of the cat.. Gastroenterology 1993 May;104(5):1430-8.
              pubmed: 8387041doi: 10.1016/0016-5085(93)90352-dgoogle scholar: lookup
            11. Clerc N. Afferent innervation of the lower oesophageal sphincter of the cat. An HRP study.. J Auton Nerv Syst 1983 Dec;9(4):623-36.
              pubmed: 6672050doi: 10.1016/0165-1838(83)90118-2google scholar: lookup
            12. Chiocchetti R, Bombardi C, Mongardi Fantaguzzi C, Russo D, Venturelli E, Montoneri C, Spadari A, Romagnoli N, Grandis A. Intrinsic innervation of the ileocaecal junction in the horse: preliminary study.. Equine Vet J 2009 Nov;41(8):759-64.
              pubmed: 20095223doi: 10.2746/042516409x407594google scholar: lookup
            13. Lefebvre RA, Smits GJ, Timmermans JP. Study of NO and VIP as non-adrenergic non-cholinergic neurotransmitters in the pig gastric fundus.. Br J Pharmacol 1995 Oct;116(3):2017-26.
              pubmed: 8640340doi: 10.1111/j.1476-5381.1995.tb16406.xgoogle scholar: lookup
            14. Muniz E, Lobo Ladd AA, Lobo Ladd FV, da Silva AA, Kmit FV, Borges AS, Teixeira R, da Mota LS, Belli CB, de Zoppa AL, da Silva LC, de Melo MP, Coppi AA. 3-D technology used to accurately understand equine ileocolonic aganglionosis.. Cells Tissues Organs 2013;198(2):160-8.
              pubmed: 23886660doi: 10.1159/000353218google scholar: lookup
            15. Wörl J, Neuhuber WL. Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after.. Histochem Cell Biol 2005 Feb;123(2):117-30.
              pubmed: 15729553doi: 10.1007/s00418-005-0764-7google scholar: lookup
            16. Pearson GT. Structural organization and neuropeptide distributions in the equine enteric nervous system: an immunohistochemical study using whole-mount preparations from the small intestine.. Cell Tissue Res 1994 Jun;276(3):523-34.
              pubmed: 7520362doi: 10.1007/BF00343949google scholar: lookup
            17. Sang Q, Ciampoli D, Greferath U, Sommer L, Young HM. Innervation of the esophagus in mice that lack MASH1.. J Comp Neurol 1999 May 24;408(1):1-10.
              pubmed: 10331576doi: 10.1002/(sici)1096-9861(19990524)408:1<1::aid-cne1>3.0.co;2-4google scholar: lookup
            18. Brehmer A, Rupprecht H, Neuhuber W. Two submucosal nerve plexus in human intestines.. Histochem Cell Biol 2010 Feb;133(2):149-61.
              pubmed: 19911189doi: 10.1007/s00418-009-0657-2google scholar: lookup
            19. Mazzuoli G, Mazzoni M, Albanese V, Clavenzani P, Lalatta-Costerbosa G, Lucchi ML, Furness JB, Chiocchetti R. Morphology and neurochemistry of descending and ascending myenteric plexus neurons of sheep ileum.. Anat Rec (Hoboken) 2007 Dec;290(12):1480-91.
              pubmed: 17972278doi: 10.1002/ar.20615google scholar: lookup
            20. van Ginneken C, Weyns A, van Meir F, Ooms L, Verhofstad A. Intrinsic innervation of the stomach of the fetal pig: an immunohistochemical study of VIP-immunoreactive nerve fibres and cell bodies.. Anat Histol Embryol 1996 Dec;25(4):269-75.
              pubmed: 9011104doi: 10.1111/j.1439-0264.1996.tb00091.xgoogle scholar: lookup
            21. Timmermans JP, Scheuermann DW, Stach W, Adriaensen D, De Groodt-Lasseel MH. Functional morphology of the enteric nervous system with special reference to large mammals.. Eur J Morphol 1992;30(2):113-22.
              pubmed: 1457247
            22. Kwiatek MA, Kahrilas PJ. Physiology of the LES.. Dis Esophagus 2012 May;25(4):286-91.
              pubmed: 21385287doi: 10.1111/j.1442-2050.2011.01184.xgoogle scholar: lookup
            23. Stach W. [The neuronal organization of the plexus myentericus (Auerbach) in the small intestine of the pig. II. Typ II-neurone (author's transl)].. Z Mikrosk Anat Forsch 1981;95(2):161-82.
              pubmed: 6169216
            24. Smid SD, Blackshaw LA. Vagal ganglionic and nonadrenergic noncholinergic neurotransmission to the ferret lower oesophageal sphincter.. Auton Neurosci 2000 Dec 28;86(1-2):30-6.
              pubmed: 11269922doi: 10.1016/S1566-0702(00)00210-1google scholar: lookup
            25. Vanden Berghe P, Coulie B, Tack J, Mawe GM, Schemann M, Janssens J. Neurochemical coding of myenteric neurons in the guinea-pig antrum.. Cell Tissue Res 1999 Jul;297(1):81-90.
              pubmed: 10398885doi: 10.1007/s004410051335google scholar: lookup
            26. Singaram C, Sengupta A, Sweet MA, Sugarbaker DJ, Goyal RK. Nitrinergic and peptidergic innervation of the human oesophagus.. Gut 1994 Dec;35(12):1690-6.
              pubmed: 7530228doi: 10.1136/gut.35.12.1690google scholar: lookup
            27. Wu M, Van Nassauw L, Kroese AB, Adriaensen D, Timmermans JP. Myenteric nitrergic neurons along the rat esophagus: evidence for regional and strain differences in age-related changes.. Histochem Cell Biol 2003 May;119(5):395-403.
              pubmed: 12721679doi: 10.1007/s00418-003-0526-3google scholar: lookup
            28. Kuramoto H, Kadowaki M. Vagus nerve stimulation preferentially induces Fos expression in nitrergic neurons of rat esophagus.. Cell Tissue Res 2006 Jun;324(3):361-7.
              pubmed: 16450125doi: 10.1007/s00441-005-0124-xgoogle scholar: lookup
            29. Russo D, Bombardi C, Grandis A, Furness JB, Spadari A, Bernardini C, Chiocchetti R. Sympathetic innervation of the ileocecal junction in horses.. J Comp Neurol 2010 Oct 1;518(19):4046-66.
              pubmed: 20737599doi: 10.1002/cne.22443google scholar: lookup
            30. Hornby PJ, Abrahams TP. Central control of lower esophageal sphincter relaxation.. Am J Med 2000 Mar 6;108 Suppl 4a:90S-98S.
              pubmed: 10718459doi: 10.1016/s0002-9343(99)00345-9google scholar: lookup
            31. Brehmer A, Schrödl F, Neuhuber W, Tooyama I, Kimura H. Co-expression pattern of neuronal nitric oxide synthase and two variants of choline acetyltransferase in myenteric neurons of porcine ileum.. J Chem Neuroanat 2004 Mar;27(1):33-41.
              pubmed: 15036361doi: 10.1016/j.jchemneu.2003.09.002google scholar: lookup
            32. Nakajima K, Tooyama I, Yasuhara O, Aimi Y, Kimura H. Immunohistochemical demonstration of choline acetyltransferase of a peripheral type (pChAT) in the enteric nervous system of rats.. J Chem Neuroanat 2000 Feb;18(1-2):31-40.
              pubmed: 10708917doi: 10.1016/s0891-0618(99)00058-7google scholar: lookup
            33. Murphy EM, Defontgalland D, Costa M, Brookes SJ, Wattchow DA. Quantification of subclasses of human colonic myenteric neurons by immunoreactivity to Hu, choline acetyltransferase and nitric oxide synthase.. Neurogastroenterol Motil 2007 Feb;19(2):126-34.
              pubmed: 17244167doi: 10.1111/j.1365-2982.2006.00843.xgoogle scholar: lookup
            34. Conklin JL. Nitric oxide: a mediator of esophageal motor function.. J Lab Clin Med 1998 Jan;131(1):10-20.
              pubmed: 9452122doi: 10.1016/s0022-2143(98)90072-5google scholar: lookup
            35. Komine M, Langohr IM, Kiupel M. Megaesophagus in Friesian horses associated with muscular hypertrophy of the caudal esophagus.. Vet Pathol 2014 Sep;51(5):979-85.
              pubmed: 24227010doi: 10.1177/0300985813511126google scholar: lookup
            36. Sang Q, Young HM. The origin and development of the vagal and spinal innervation of the external muscle of the mouse esophagus.. Brain Res 1998 Nov 2;809(2):253-68.
              pubmed: 9853118doi: 10.1016/s0006-8993(98)00893-2google scholar: lookup
            37. Dong H, Jiang Y, Srinivasan S, Mittal RK. Morphological, immunocytochemical, and functional characterization of esophageal enteric neurons in primary culture.. Am J Physiol Gastrointest Liver Physiol 2013 Jul 15;305(2):G129-38.
              pubmed: 23660501doi: 10.1152/ajpgi.00040.2013google scholar: lookup
            38. Niel JP, Gonella J, Roman C. [Horseradish peroxidase localization of the cell bodies of the sympathetic and parasympathetic neurones controlling the lower oesophageal sphincter in the cat (author's transl)].. J Physiol (Paris) 1980 Nov;76(6):591-9.
              pubmed: 7441569
            39. Morikawa S, Komuro T. Distribution of myenteric NO neurons along the guinea-pig esophagus.. J Auton Nerv Syst 1998 Dec 11;74(2-3):91-9.
              pubmed: 9915623doi: 10.1016/s0165-1838(98)00131-3google scholar: lookup
            40. Long JD, Orlando RC. Esophageal submucosal glands: structure and function.. Am J Gastroenterol 1999 Oct;94(10):2818-24.
              pubmed: 10520827doi: 10.1111/j.1572-0241.1999.1422_b.xgoogle scholar: lookup
            41. Yuan S, Costa M, Brookes SJ. Neuronal pathways and transmission to the lower esophageal sphincter of the guinea Pig.. Gastroenterology 1998 Sep;115(3):661-71.
              pubmed: 9721163doi: 10.1016/s0016-5085(98)70145-3google scholar: lookup
            42. Chiocchetti R, Bombardi C, Mongardi-Fantaguzzi C, Venturelli E, Russo D, Spadari A, Montoneri C, Romagnoli N, Grandis A. Intrinsic innervation of the horse ileum.. Res Vet Sci 2009 Oct;87(2):177-85.
              pubmed: 19380154doi: 10.1016/j.rvsc.2009.03.011google scholar: lookup
            43. Brookes SJ, Chen BN, Hodgson WM, Costa M. Characterization of excitatory and inhibitory motor neurons to the guinea pig lower esophageal sphincter.. Gastroenterology 1996 Jul;111(1):108-17.
              pubmed: 8698189doi: 10.1053/gast.1996.v111.pm8698189google scholar: lookup
            44. Fang S, Christensen J. Distribution of NADPH diaphorase in intramural plexuses of cat and opossum esophagus.. J Auton Nerv Syst 1994 Jan-Feb;46(1-2):123-33.
              pubmed: 8120336doi: 10.1016/0165-1838(94)90149-xgoogle scholar: lookup
            45. Onori L, Friedmann CA, Frigo GM, Tonini M. Effects of catecholamines, nicotine, acetylcholine and potassium on the mechanical activity of the colonic muscularis mucosae in the cat.. Am J Dig Dis 1971 Aug;16(8):689-92.
              pubmed: 5315378doi: 10.1007/BF02239590google scholar: lookup
            46. Pirie RS, Jago RC, Hudson NP. Equine grass sickness.. Equine Vet J 2014 Sep;46(5):545-53.
              pubmed: 24580639doi: 10.1111/evj.12254google scholar: lookup
            47. Goyal RK, Chaudhury A. Physiology of normal esophageal motility.. J Clin Gastroenterol 2008 May-Jun;42(5):610-9.
              pubmed: 18364578doi: 10.1097/MCG.0b013e31816b444dgoogle scholar: lookup
            48. Farré R, Sifrim D. Regulation of basal tone, relaxation and contraction of the lower oesophageal sphincter. Relevance to drug discovery for oesophageal disorders.. Br J Pharmacol 2008 Mar;153(5):858-69.
              pubmed: 17994108doi: 10.1038/sj.bjp.0707572google scholar: lookup
            49. Branchek TA, Gershon MD. Time course of expression of neuropeptide Y, calcitonin gene-related peptide, and NADPH diaphorase activity in neurons of the developing murine bowel and the appearance of 5-hydroxytryptamine in mucosal enterochromaffin cells.. J Comp Neurol 1989 Jul 8;285(2):262-73.
              pubmed: 2788179doi: 10.1002/cne.902850208google scholar: lookup
            50. Cottrell DF, McGorum BC, Pearson GT. The neurology and enterology of equine grass sickness: a review of basic mechanisms.. Neurogastroenterol Motil 1999 Apr;11(2):79-92.
              pubmed: 10320588doi: 10.1046/j.1365-2982.1999.00140.xgoogle scholar: lookup
            51. Furness JB. The enteric nervous system and neurogastroenterology.. Nat Rev Gastroenterol Hepatol 2012 Mar 6;9(5):286-94.
              pubmed: 22392290doi: 10.1038/nrgastro.2012.32google scholar: lookup
            52. Wedel T, Roblick U, Gleiss J, Schiedeck T, Bruch HP, Kühnel W, Krammer HJ. Organization of the enteric nervous system in the human colon demonstrated by wholemount immunohistochemistry with special reference to the submucous plexus.. Ann Anat 1999 Jul;181(4):327-37.
              pubmed: 10427369doi: 10.1016/S0940-9602(99)80122-8google scholar: lookup
            53. Pimont S, Bruley Des Varannes S, Le Neel JC, Aubert P, Galmiche JP, Neunlist M. Neurochemical coding of myenteric neurones in the human gastric fundus.. Neurogastroenterol Motil 2003 Dec;15(6):655-62.
              pubmed: 14651601doi: 10.1046/j.1350-1925.2003.00442.xgoogle scholar: lookup
            54. Hultgren BD. Ileocolonic aganglionosis in white progeny of overo spotted horses.. J Am Vet Med Assoc 1982 Feb 1;180(3):289-92.
              pubmed: 7056678
            55. Hempfling C, Seibold R, Shiina T, Heimler W, Neuhuber WL, Wörl J. Enteric co-innervation of esophageal striated muscle fibers: a phylogenetic study.. Auton Neurosci 2009 Dec 3;151(2):135-41.
              pubmed: 19748835doi: 10.1016/j.autneu.2009.08.006google scholar: lookup
            56. Teixeira AF, Vives P, Krammer HJ, Kühnel W, Wedel T. Structural organization of the enteric nervous system in the cattle esophagus revealed by wholemount immunohistochemistry.. Ital J Anat Embryol 2001;106(2 Suppl 1):313-21.
              pubmed: 11729972
            57. Bueno L, Ruckebusch Y. Perinatal development of intestinal myoelectrical activity in dogs and sheep.. Am J Physiol 1979 Jul;237(1):E61-7.
              pubmed: 464054doi: 10.1152/ajpendo.1979.237.1.E61google scholar: lookup
            58. Beck M, Schlabrakowski A, Schrödl F, Neuhuber W, Brehmer A. ChAT and NOS in human myenteric neurons: co-existence and co-absence.. Cell Tissue Res 2009 Oct;338(1):37-51.
              pubmed: 19711100doi: 10.1007/s00441-009-0852-4google scholar: lookup
            59. Grozdanovic Z, Baumgarten HG, Brüning G. Histochemistry of NADPH-diaphorase, a marker for neuronal nitric oxide synthase, in the peripheral autonomic nervous system of the mouse.. Neuroscience 1992;48(1):225-35.
              pubmed: 1374863doi: 10.1016/0306-4522(92)90351-2google scholar: lookup
            60. Mittal RK, Bhalla V. Oesophageal motor functions and its disorders.. Gut 2004 Oct;53(10):1536-42.
              pubmed: 15361508doi: 10.1136/gut.2003.035618google scholar: lookup
            61. Stick JA, Derksen FJ, McNitt DL, Chou CC. Equine esophageal pressure profile.. Am J Vet Res 1983 Feb;44(2):272-5.
              pubmed: 6830016
            62. Furness JB, Li ZS, Young HM, Förstermann U. Nitric oxide synthase in the enteric nervous system of the guinea-pig: a quantitative description.. Cell Tissue Res 1994 Jul;277(1):139-49.
              pubmed: 7519970doi: 10.1007/BF00303090google scholar: lookup
            63. Christensen HM. Government and the future of dentistry.. Alumni Bull Univ Mich Sch Dent 1973;:77-83.
              pubmed: 4534332
            64. Sanders KM, Smith TK. Motoneurones of the submucous plexus regulate electrical activity of the circular muscle of canine proximal colon.. J Physiol 1986 Nov;380:293-310.
              pubmed: 2886654doi: 10.1113/jphysiol.1986.sp016286google scholar: lookup

            Citations

            This article has been cited 7 times.
            1. Diana A, Freccero F, Giancola F, Linta N, Pietra M, Luca V, Salamanca G, Cipone M, Chiocchetti R. Ex vivo ultrasonographic and histological morphometry of small intestinal wall layers in horses. Vet Radiol Ultrasound 2022 May;63(3):353-363.
              doi: 10.1111/vru.13059pubmed: 35171532google scholar: lookup
            2. Toschi A, Galiazzo G, Piva A, Tagliavia C, Mazzuoli-Weber G, Chiocchetti R, Grilli E. Cannabinoid and Cannabinoid-Related Receptors in the Myenteric Plexus of the Porcine Ileum. Animals (Basel) 2021 Jan 21;11(2).
              doi: 10.3390/ani11020263pubmed: 33494452google scholar: lookup
            3. Galiazzo G, Giancola F, Stanzani A, Fracassi F, Bernardini C, Forni M, Pietra M, Chiocchetti R. Localization of cannabinoid receptors CB1, CB2, GPR55, and PPARα in the canine gastrointestinal tract. Histochem Cell Biol 2018 Aug;150(2):187-205.
              doi: 10.1007/s00418-018-1684-7pubmed: 29882158google scholar: lookup
            4. Wojtkiewicz J, Makowska K, Bejer-Olenska E, Gonkowski S. Zinc Transporter 3 (Znt3) as an Active Substance in the Enteric Nervous System of the Porcine Esophagus. J Mol Neurosci 2017 Mar;61(3):315-324.
              doi: 10.1007/s12031-016-0854-0pubmed: 27796869google scholar: lookup
            5. Taatjes DJ, Roth J. The Histochemistry and Cell Biology omnium-gatherum: the year 2015 in review. Histochem Cell Biol 2016 Mar;145(3):239-74.
              doi: 10.1007/s00418-016-1417-8pubmed: 26878854google scholar: lookup
            6. Alcantara De Sousa G, Nemoto M, Rudd JA, Sanger GJ, Andrews PLR. Emesis in Rodents: Present or Absent? A Critical Review of the Evidence and Implications for the Use of Rodents in Biomedical Research. Biology (Basel) 2025 Dec 25;15(1).
              doi: 10.3390/biology15010035pubmed: 41514876google scholar: lookup
            7. Holley L, Creasey HN, Bedenice D, Reed S, Romualdo da Silva DR, Trautwein V, Mazan M, Widmer G. Nebulization of 2% lidocaine has no detectable impact on the healthy equine respiratory microbiota. PLoS One 2025;20(1):e0316079.
              doi: 10.1371/journal.pone.0316079pubmed: 39854381google scholar: lookup
            Subscribe to our newsletter
            Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.