Neuroanatomy of extrinsic afferents supplying the gastrointestinal tract
Abstract
Here we discuss the neuroanatomy of extrinsic gastrointestinal (GI) afferent neurones, the relationship between structure and function and the role of afferents in disease. Three pathways connect the gut to the central nervous system: vagal afferents signal mainly from upper GI regions, pelvic afferents mainly from the colorectal region and splanchnic afferents from throughout. Vagal afferents mediate reflex regulation of gut function and behaviour, operating mainly at physiological levels. There are two major functional classes − tension receptors, responding to muscular contraction and distension, and mucosal receptors. The function of vagal endings correlates well with their anatomy: tracing studies show intramuscular arrays (IMAs) and intraganglionic laminar endings (IGLEs); IGLEs are now known to respond to tension. Functional mucosal receptors correlate with endings traced to the lamina propria. Pelvic afferents serve similar functions to vagal afferents, and additionally mediate both innocuous and noxious sensations. Splanchnic afferents comprise mucosal and stretch‐sensitive afferents with low thresholds in addition to high‐threshold serosal/mesenteric afferents suggesting diverse roles. IGLEs, probably of pelvic origin, have been identified recently in the rectum and respond similarly to gastric vagal IGLEs. Gastrointestinal afferents may be sensitized or inhibited by chemical mediators released from several cell types. Whether functional changes have anatomical correlates is not known, but it is likely that they underlie diseases involving visceral hypersensitivity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Vagal afferents are thought to be polymodal, responding to mechanical, chemical or hormonal signals.
“Due to the vast variety of receptors expressed on vagal afferents, they are thought to be polymodal, in that they respond to a variety of signals which are mechanical, chemical or hormonal in nature (Berthoud et al., 2004).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Berthoud et al., 2004
The ANS conveys physiological conditions in the gut, such as acidity, levels of nutrients, osmolarity and pain, to the brain.
“The ANS conveys physiological conditions in the gut, such as acidity, levels of nutrients, osmolarity and pain, to the brain49.”
From The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease (2018) · cites this paper as [49]
Cites
Functional and chemical anatomy of the afferent vagal system
Berthoud, H.-R., & Neuhuber, W. L. (2000) · Autonomic Neuroscience · doi:10.1016/s1566-0702(00)00215-0 · Cited by 1,280 · see citing works
Self-citationvan der Kooy, D., Koda, L. Y., McGinty, J. F., Gerfen, C. R., & Bloom, F. E. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902240102 · Cited by 733 · see citing works
Sensory innervation of the viscera: peripheral basis of visceral pain
Cerveró, F. (1994) · Physiological Reviews · doi:10.1152/physrev.1994.74.1.95 · Cited by 526 · see citing works
Tension receptors in the stomach and the urinary bladder
Iggo, A. (1955) · The Journal of Physiology · doi:10.1113/jphysiol.1955.sp005327 · Cited by 515 · see citing works
Berthoud, H., & Powley, T. L. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903190206 · Cited by 287 · see citing works
Self-citationZagorodnyuk, V. P., Chen, B. N., & Brookes, S. J. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00255.x · Cited by 267 · see citing works
Self-citationNeuroanatomy of visceral nociception: vagal and splanchnic afferent
Grundy, D. (2002) · Gut · doi:10.1136/gut.51.suppl_1.i2 · Cited by 251 · see citing works
Self-citationDistribution of the vanilloid receptor (VR1) in the gastrointestinal tract
Ward, S. M., Bayguinov, J. R., Won, K., Grundy, D., & Berthoud, H. R. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10801 · Cited by 243 · see citing works
Self-citationAl–Chaer, E. D., Lawand, N., Westlund, K. N., & Willis, W. D. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.4.2661 · Cited by 241 · see citing works
Berthoud, H., Kressel, M., Raybould, H., & Neuhuber, W. (1995) · Anatomy and Embryology · doi:10.1007/bf00187819 · Cited by 216 · see citing works
Self-citationBerthoud, H., Patterson, L. M., Neumann, F., & Neuhuber, W. (1997) · Anatomy and Embryology · doi:10.1007/s004290050037 · Cited by 198 · see citing works
Self-citationTransduction Sites of Vagal Mechanoreceptors in the Guinea Pig Esophagus
Zagorodnyuk, V. P., & Brookes, S. J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06249.2000 · Cited by 196 · see citing works
Self-citationNeuhuber, W. (1987) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(87)90153-6 · Cited by 180 · see citing works
I. Receptors on visceral afferents
Kirkup, A. J., Brunsden, A. M., & Grundy, D. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.5.g787 · Cited by 174 · see citing works
Self-citationGASTRIC MUCOSAL CHEMORECEPTORS WITH VAGAL AFFERENT FIBRES IN THE CAT
Iggo, A. (1957) · Quarterly Journal of Experimental Physiology and Cognate Medical Sciences · doi:10.1113/expphysiol.1957.sp001284 · Cited by 167 · see citing works
Lynn, P. A., Olsson, C., Zagorodnyuk, V. P., Costa, M., & Brookes, S. J. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)01050-3 · Cited by 153 · see citing works
Self-citationBlackshaw, L. A., & Grundy, D. (1993) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(93)90360-7 · Cited by 145 · see citing works
Self-citationVegetative innervation of the esophagus. II. Intraganglionic laminar endings
Rodrigo, J., Hernández, C. J., Vidal, M. A., & Pedrosa, J. Á. (1975) · Cells Tissues Organs · doi:10.1159/000144431 · Cited by 134 · see citing works
Blumberg, H., Haupt, P., J�nig, W., & Köhler, W. (1983) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00584710 · Cited by 133 · see citing works
Vagal Afferent Nerve Fibres Contact Mast Cells in Rat Small Intestinal Mucosa
Williams, R. M., Berthoud, H., & Stead, R. H. (2010) · NeuroImmunoModulation · doi:10.1159/000097346 · Cited by 128 · see citing works
Self-citationBerthoud, H. R., & Patterson, L. M. (1996) · Cells Tissues Organs · doi:10.1159/000147837 · Cited by 125 · see citing works
Self-citationLynn, P. A., & Blackshaw, L. A. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0271r.x · Cited by 115 · see citing works
Self-citationExcitation of rat colonic afferent fibres by 5‐HT 3 receptors
Hicks, G. A., Coldwell, J. R., Schindler, M., Ward, P. A. B., Jenkins, D., Lynn, P. A., Humphrey, P. P. A., & Blackshaw, L. A. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.025452 · Cited by 114 · see citing works
Self-citationOn the function of spinal primary afferent fibres supplying colon and urinary bladder
Jänig, W., & Koltzenburg, M. (1990) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(90)90108-u · Cited by 108 · see citing works
The pharmacology of gastrointestinal nociceptive pathways
Blackshaw, L. A. (2002) · Current Opinion in Pharmacology · doi:10.1016/s1471-4892(02)00211-4 · Cited by 106 · see citing works
Self-citationVagal and spinal mechanosensors in the rat stomach and colon have multiple receptive fields
Berthoud, H., Lynn, P. A., & Blackshaw, L. A. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.5.r1371 · Cited by 104 · see citing works
Self-citationBlackshaw, L. A., Grundy, D., & Scratcherd, T. (1987) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(87)90130-5 · Cited by 103 · see citing works
Self-citationI. Morphology and topography of vagal afferents innervating the GI tract
Powley, T. L., & Phillips, R. J. (2002) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00249.2002 · Cited by 99 · see citing works
Davison, J. S. (1972) · Quarterly Journal of Experimental Physiology and Cognate Medical Sciences · doi:10.1113/expphysiol.1972.sp002176 · Cited by 98 · see citing works
Kressel, M., Berthoud, H., & Neuhuber, W. (1994) · Cell and Tissue Research · doi:10.1007/bf00305379 · Cited by 92 · see citing works
Self-citationTassicker, B. C., Hennig, G. W., Costa, M., & Brookes, S. J. (1999) · Cell and Tissue Research · doi:10.1007/s004410051250 · Cited by 85 · see citing works
Self-citationCottrell, D. F., & Iggo, A. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015388 · Cited by 78 · see citing works
Mucosal enteroceptors with vagal afferent fibres in the proximal duodenum of sheep.
Cottrell, D. F., & Iggo, A. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015390 · Cited by 78 · see citing works
Booth, C. E., Kirkup, A. J., Hicks, G. A., Humphrey, P. P. A., & Grundy, D. (2001) · Gastroenterology · doi:10.1053/gast.2001.26335 · Cited by 76 · see citing works
Self-citationFox, E. A., Phillips, R., Byerly, M. S., Baronowsky, E. A., Chi, M., & Powley, T. L. (2002) · Anatomy and Embryology · doi:10.1007/s00429-002-0261-x · Cited by 73 · see citing works
C-Kit mutant mice have a selective loss of vagal intramuscular mechanoreceptors in the forestomach
Fox, E. A., Phillips, R. J., Martinson, F. A., Baronowsky, E. A., & Powley, T. L. (2001) · Anatomy and Embryology · doi:10.1007/s004290100184 · Cited by 70 · see citing works
Socioeconomic Status and the Rorschach
Frank, G. (1994) · Psychological Reports · doi:10.2466/pr0.1994.74.1.95 · Cited by 56 · see citing works
Khan, A. M., Stanley, B., Bozzetti, L., Chin, C., Stivers, C., & Currás-Collazo, M. C. (2000) · The Journal of comparative neurology · doi:10.1002/1096-9861(20001218)428:3 · Cited by 44 · see citing works
Phillips (2000) · doi:10.1002/(sici)1096-9861(20000605)421:3
Flagged first, then by citations
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Gershon, M. D., & Tack, J. (2007) · Gastroenterology · doi:10.1053/j.gastro.2006.11.002 · Cited by 1,563 · see citing works
The enteric nervous system and gastrointestinal innervation: integrated local and central control
Furness, J. B., Callaghan, B. P., Rivera, L. R., & Cho, H.-J. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_3 · Cited by 827 · see citing works
The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease
Yang, T., Richards, E. M., Pepine, C. J., & Raizada, M. K. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0018-2 · Cited by 753 · see citing works
Sensory neurons that detect stretch and nutrients in the digestive system
Williams, E. K., Chang, R. B., Strochlic, D. E., Umans, B. D., Lowell, B. B., & Liberles, S. D. (2016) · Cell · doi:10.1016/j.cell.2016.05.011 · Cited by 645 · see citing works
The Brain, Appetite, and Obesity
Berthoud, H., & Morrison, C. D. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093551 · Cited by 699 · see citing works
Self-citationGenetic identification of vagal sensory neurons that control feeding
Bai, L., Mesgarzadeh, S., Ramesh, K. S., Huey, E. L., Liu, Y., Gray, L. A., Aitken, T. J., Chen, Y., Beutler, L. R., Ahn, J. S., et al. (2019) · Cell · doi:10.1016/j.cell.2019.10.031 · Cited by 494 · see citing works
Hindbrain Neurons as an Essential Hub in the Neuroanatomically Distributed Control of Energy Balance
Grill, H. J., & Hayes, M. R. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.06.015 · Cited by 501 · see citing works
Brainstem circuits regulating gastric function
Travagli, R. A., Hermann, G. E., Browning, K. N., & Rogers, R. C. (2006) · Annual Review of Physiology · doi:10.1146/annurev.physiol.68.040504.094635 · Cited by 498 · see citing works
The Parabrachial Nucleus: CGRP Neurons Function as a General Alarm
Palmiter, R. D. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.03.007 · Cited by 442 · see citing works
Gut Microbiota in Hypertension and Atherosclerosis: A Review
Verhaar, B. J. H., Prodan, A., Nieuwdorp, M., & Muller, M. (2020) · Nutrients · doi:10.3390/nu12102982 · Cited by 411 · see citing works
The Lipid Messenger OEA Links Dietary Fat Intake to Satiety
Schwartz, G. J., Fu, J., Astarita, G., Li, X., Gaetani, S., Campolongo, P., Cuomo, V., & Piomelli, D. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.08.005 · Cited by 370 · see citing works
Vagal neurocircuitry and its influence on gastric motility
Travagli, R. A., & Anselmi, L. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.76 · Cited by 323 · see citing works
The vagus nerve, food intake and obesity
Berthoud, H.-R. (2008) · Regulatory Peptides · doi:10.1016/j.regpep.2007.08.024 · Cited by 316 · see citing works
Self-citationBile acid signaling pathways from the enterohepatic circulation to the central nervous system
Mertens, K. L., Kalsbeek, A., Soeters, M. R., & Eggink, H. M. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00617 · Cited by 287 · see citing works
Toll-like Receptors 3, 4, and 7 Are Expressed in the Enteric Nervous System and Dorsal Root Ganglia
Barajon, I., Serrao, G., Arnaboldi, F., Opizzi, E., Ripamonti, G., Balsari, A., & Rumio, C. (2009) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.2009.953539 · Cited by 287 · see citing works
Keita, Å. V., & Söderholm, J. D. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01498.x · Cited by 286 · see citing works
Sensory transmission in the gastrointestinal tract
Blackshaw, L. A., Brookes, S. J., Grundy, D., & Schemann, M. (2007) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2006.00871.x · Cited by 285 · see citing works
Self-citationRüttimann, E. B., Arnold, M., Hillebrand, J. J., Geary, N., & Langhans, W. (2008) · Endocrinology · doi:10.1210/en.2008-1221 · Cited by 256 · see citing works
Imaging and modelling of digestion in the stomach and the duodenum
Schulze, K. S. (2006) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2006.00759.x · Cited by 256 · see citing works
A multidimensional coding architecture of the vagal interoceptive system
Zhao, Q., Yu, C. D., Wang, R., Xu, Q. J., Pra, R. D., Zhang, L., & Chang, R. B. (2022) · Nature · doi:10.1038/s41586-022-04515-5 · Cited by 243 · see citing works
Perez-Burgos, A., Wang, B., Mao, Y.-K., Mistry, B., Neufeld, K.-A. M., Bienenstock, J., & Kunze, W. (2013) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00128.2012 · Cited by 235 · see citing works
Integrative neurocircuits that control metabolism and food intake
Brüning, J. C., & Fenselau, H. (2023) · Science · doi:10.1126/science.abl7398 · Cited by 214 · see citing works
Borgmann, D., Ciglieri, E., Biglari, N., Brandt, C., Cremer, A. L., Backes, H., Tittgemeyer, M., Wunderlich, F. T., Brüning, J. C., & Fenselau, H. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.05.002 · Cited by 207 · see citing works
Necrotizing enterocolitis: It’s not all in the gut
Meister, A. L., Doheny, K. K., & Travagli, R. A. (2019) · Experimental Biology and Medicine · doi:10.1177/1535370219891971 · Cited by 217 · see citing works
The gut, its microbiome, and the brain: connections and communications
Gershon, M. D., & Margolis, K. G. (2021) · Journal of Clinical Investigation · doi:10.1172/jci143768 · Cited by 209 · see citing works
An inter-organ neural circuit for appetite suppression
Zhang, T., Perkins, M. H., Chang, H., Han, W., & de Araujo, I. E. (2022) · Cell · doi:10.1016/j.cell.2022.05.007 · Cited by 192 · see citing works
Harnessing Gut Microbes for Mental Health: Getting From Here to There
Bruce‐Keller, A. J., Salbaum, J. M., & Berthoud, H. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.014 · Cited by 192 · see citing works
Self-citationGebhart, G. F., & Bielefeldt, K. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150049 · Cited by 224 · see citing works
Signalling from the periphery to the brain that regulates energy homeostasis
Kim, K., Seeley, R. J., & Sandoval, D. A. (2018) · Nature reviews. Neuroscience · doi:10.1038/nrn.2018.8 · Cited by 181 · see citing works
Hypothalamic detection of macronutrients via multiple gut-brain pathways
Goldstein, N., McKnight, A. D., Carty, J. R. E., Arnold, M., Betley, J. N., & Alhadeff, A. L. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2020.12.018 · Cited by 176 · see citing works
Basic and clinical aspects of gastrointestinal pain
Knowles, C. H., & Aziz, Q. (2009) · Pain · doi:10.1016/j.pain.2008.12.011 · Cited by 170 · see citing works
Tavakoli, P., Vollmer-Conna, U. S., Hadzi-Pavlovic, D., & Grimm, M. (2021) · Public health reviews · doi:10.3389/phrs.2021.1603990 · Cited by 173 · see citing works
Checa-Ros, A., Jeréz-Calero, A., Molina-Carballo, A., Campoy, C., & Muñoz-Hoyos, A. (2021) · Nutrients · doi:10.3390/nu13010249 · Cited by 164 · see citing works
The Paraventricular Nucleus of the Hypothalamus: Development, Function, and Human Diseases
Qin, C., Li, J., & Tang, K. (2018) · Endocrinology · doi:10.1210/en.2018-00453 · Cited by 164 · see citing works
Review article: endocannabinoids and their receptors in the enteric nervous system
Duncan, M., Davison, J. S., & Sharkey, K. A. (2005) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2005.02648.x · Cited by 155 · see citing works
Mechanisms of CCK signaling from gut to brain
Raybould, H. E. (2007) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.09.006 · Cited by 151 · see citing works
Vagal afferent nerves with nociceptive properties in guinea‐pig oesophagus
Yu, S., Undem, B. J., & Kollárik, M. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.079574 · Cited by 147 · see citing works
Fundamentals of Neurogastroenterology: Physiology/Motility – Sensation
Boeckxstaens, G., Camilleri, M., Sifrim, D., Houghton, L. A., Elsenbruch, S., Lindberg, G., Azpiroz, F., & Parkman, H. P. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.02.030 · Cited by 142 · see citing works
The gut-to-brain axis for toxin-induced defensive responses
Xie, Z., Zhang, X., Zhao, M., Huo, L., Huang, M., Li, D., Zhang, S., Cheng, X., Gu, H., Zhang, C., et al. (2022) · Cell · doi:10.1016/j.cell.2022.10.001 · Cited by 137 · see citing works
Perez‐Burgos, A., Wang, L., McVey Neufeld, K., Mao, Y., Ahmadzai, M., Janssen, L. J., Stanisz, A. M., Bienenstock, J., & Kunze, W. A. (2015) · The Journal of Physiology · doi:10.1113/jp270229 · Cited by 123 · see citing works
The Role of PVH Circuits in Leptin Action and Energy Balance
Sutton, A. K., Myers, M. G., & Olson, D. P. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105347 · Cited by 121 · see citing works
Beyak, M. J., & Vanner, S. (2005) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2004.00596.x · Cited by 121 · see citing works
Feng, B., & Gebhart, G. F. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00406.2010 · Cited by 118 · see citing works
Regulation of enteric functions by adenosine: Pathophysiological and pharmacological implications
Antonioli, L., Fornai, M., Colucci, R., Ghisu, N., Tuccori, M., Tacca, M. D., & Blandizzi, C. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.08.010 · Cited by 114 · see citing works
KUWAHARA, A., MATSUDA, K., KUWAHARA, Y., ASANO, S., INUI, T., & MARUNAKA, Y. (2020) · Biomedical Research · doi:10.2220/biomedres.41.199 · Cited by 112 · see citing works
Vittal, H., Farrugia, G., Gomez, G., & Pasricha, P. J. (2007) · Nature Clinical Practice Gastroenterology & Hepatology · doi:10.1038/ncpgasthep0838 · Cited by 109 · see citing works
Acid-sensitive vagal sensory pathways and cough
Kollárik, M., Ru, F., & Undem, B. J. (2006) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2006.11.010 · Cited by 106 · see citing works
Wolpert, N., Rebollo, I., & Tallon‐Baudry, C. (2020) · Psychophysiology · doi:10.1111/psyp.13599 · Cited by 96 · see citing works
Recognizing the role of the vagus nerve in depression from microbiota-gut brain axis
Tan, C., Yan, Q., Ma, Y., Fang, J., & Yang, Y. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.1015175 · Cited by 111 · see citing works
A Western Diet Increases Serotonin Availability in Rat Small Intestine
Bertrand, R. L., Senadheera, S. N., Markus, I., Liu, L., Howitt, L., Chen, H., Murphy, T. V., Sandow, S. L., & Bertrand, P. P. (2010) · Endocrinology · doi:10.1210/en.2010-0377 · Cited by 100 · see citing works
Koopmans, S. J., & Schuurman, T. (2015) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2015.03.044 · Cited by 102 · see citing works
The critical role of CCK in the regulation of food intake and diet-induced obesity
Cawthon, C. R., & Serre, C. B. D. L. (2021) · Peptides · doi:10.1016/j.peptides.2020.170492 · Cited by 99 · see citing works
Helicobacter pylori Infection and Extragastric Diseases—A Focus on the Central Nervous System
Baj, J., Forma, A., Flieger, W., Morawska, I., Michalski, A., Buszewicz, G., Sitarz, E., Portincasa, P., Garruti, G., Flieger, M., et al. (2021) · Cells · doi:10.3390/cells10092191 · Cited by 80 · see citing works
Enteric nervous system: reflexes, pattern generators and motility
Wood, J. D. (2008) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3282f56125 · Cited by 108 · see citing works
The gut-brain axis rewired: adding a functional vagal nicotinic “sensory synapse”
Perez‐Burgos, A., Mao, Y., Bienenstock, J., & Kunze, W. A. (2014) · The FASEB Journal · doi:10.1096/fj.13-245282 · Cited by 91 · see citing works
Bansal, V., Costantini, T. W., Ryu, S. Y., Peterson, C. Y., Loomis, W. H., Putnam, J., Elicieri, B. P., Baird, A., & Coimbra, R. S. M. (2010) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/ta.0b013e3181d87373 · Cited by 91 · see citing works
Visceral versus somatic pain: an educational review of anatomy and clinical implications
Boezaart, A. P., Smith, C. R., Chembrovich, S., Zasimovich, Y., Server, A., Morgan, G., Theron, A., Booysen, K., & Reina, M. Á. (2021) · Regional Anesthesia & Pain Medicine · doi:10.1136/rapm-2020-102084 · Cited by 98 · see citing works
Mechanosensitive Piezo Channels in the Gastrointestinal Tract
Alcaino, C., Farrugia, G., & Beyder, A. (2017) · Current topics in membranes · doi:10.1016/bs.ctm.2016.11.003 · Cited by 89 · see citing works
Richards, P., Thornberry, N. A., & Pinto, S. (2021) · Molecular Metabolism · doi:10.1016/j.molmet.2021.101175 · Cited by 88 · see citing works
Obesity surgery and gut–brain communication
Berthoud, H., Shin, A. C., & Zheng, H. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.01.023 · Cited by 84 · see citing works
Self-citationIntraperitoneal Local Anesthetic Improves Recovery After Colon Resection
Kahokehr, A. A., Sammour, T., Zargar‐Shoshtari, K., Taylor, M., & Hill, A. G. (2011) · Annals of Surgery · doi:10.1097/sla.0b013e318221f0cf · Cited by 83 · see citing works
Antonioli, L., Colucci, R., Pellegrini, C., Giustarini, G., Tuccori, M., Blandizzi, C., & Fornai, M. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.04.002 · Cited by 81 · see citing works
Aktar, R., Parkar, N., Stentz, R., Baumard, L., Parker, A., Goldson, A. J., Brion, A., Carding, S. R., Blackshaw, L. A., & Peiris, M. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1766936 · Cited by 80 · see citing works
Self-citationThe Functional and Neurobiological Properties of Bad Taste
Schier, L. A., & Spector, A. C. (2018) · Physiological Reviews · doi:10.1152/physrev.00044.2017 · Cited by 75 · see citing works
Exploring relationships for visceral and somatic pain with autonomic control and personality
Paine, P., Kishor, J., Worthen, S. F., Gregory, L. J., & Aziz, Q. (2009) · Pain · doi:10.1016/j.pain.2009.02.022 · Cited by 79 · see citing works
Burgell, R., & Scott, S. (2012) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2012.18.4.373 · Cited by 172 · see citing works
Neural signalling of gut mechanosensation in ingestive and digestive processes
Kim, M., Heo, G., & Kim, S. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00544-7 · Cited by 79 · see citing works
Learning of food preferences: mechanisms and implications for obesity & metabolic diseases
Berthoud, H., Morrison, C. D., Ackroff, K., & Sclafani, A. J. (2021) · International Journal of Obesity · doi:10.1038/s41366-021-00894-3 · Cited by 74 · see citing works
Self-citationBasic and clinical aspects of visceral sensation: transmission in the CNS
Bielefeldt, K., Christianson, J. A., & Davis, B. M. (2005) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2005.00671.x · Cited by 72 · see citing works
Labouesse, M. A., Weber‐Stadlbauer, U., Weber, E., Arnold, M., Langhans, W., & Pacheco‐López, G. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02364.x · Cited by 70 · see citing works
Gastrointestinal Microbiome and Neurologic Injury
Panther, E. J., Dodd, W., Clark, A., & Lucke-Wold, B. P. (2022) · Biomedicines · doi:10.3390/biomedicines10020500 · Cited by 71 · see citing works
Dietary fat sensing via fatty acid oxidation in enterocytes: possible role in the control of eating
Langhans, W., Leitner, C., & Arnold, M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00610.2010 · Cited by 69 · see citing works
The CCK(-like) receptor in the animal kingdom: Functions, evolution and structures
Staljanssens, D., Azari, E. K., Christiaens, O., Beaufays, J., Lins, L., Camp, J. V., & Smagghe, G. J. (2010) · Peptides · doi:10.1016/j.peptides.2010.11.025 · Cited by 63 · see citing works
Qiao, L. Y., & Grider, J. R. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2006.12.024 · Cited by 63 · see citing works
The relationship between gastric motility and nausea: Gastric prokinetic agents as treatments
Sanger, G. J., Broad, J., & Andrews, P. L. R. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.06.031 · Cited by 62 · see citing works
Mouse colon sensory neurons detect extracellular acidosis via TRPV1
Sugiura, T., Bielefeldt, K., & Gebhart, G. F. (2007) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00440.2006 · Cited by 60 · see citing works
Washington, M. C., Raboin, S. J., Thompson, W., Larsen, C. J., & Sayegh, A. I. (2010) · Brain Research · doi:10.1016/j.brainres.2010.05.002 · Cited by 58 · see citing works
Role of the intestinal microbiota in contributing to weight disorders and associated comorbidities
Hul, M. V., Neyrinck, A. M., Everard, A., Abot, A., Bindels, L. B., Delzenne, N. M., Knauf, C., & Cani, P. D. (2024) · Clinical Microbiology Reviews · doi:10.1128/cmr.00045-23 · Cited by 60 · see citing works
Gut microbes and food reward: From the gut to the brain
d’Oplinter, A. D. W., Huwart, S. J. P., Cani, P. D., & Everard, A. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.947240 · Cited by 55 · see citing works
Optogenetic and chemogenetic techniques for neurogastroenterology
Boesmans, W., Hao, M. M., & Berghe, P. V. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.151 · Cited by 54 · see citing works
Vagal influences over mast cells
Stead, R. H., Colley, E. C., Wang, B., Partosoedarso, E. R., Lin, J., STANISZ, A. M., & Hillsley, K. (2006) · Autonomic Neuroscience · doi:10.1016/j.autneu.2006.01.002 · Cited by 54 · see citing works
Wang, G., Wang, X.-Y., Liu, S., Qu, M., Xia, Y. L., NEEDLEMAN, B. J., Mikami, D. J., & Wood, J. D. (2014) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00125.2014 · Cited by 52 · see citing works
Detection of macronutrients in the intestinal wall
Raybould, H. E., Glatzle, J., Freeman, S. L., Whited, K. L., Darcel, N., Liou, A. P., & Bohan, D. (2006) · Autonomic Neuroscience · doi:10.1016/j.autneu.2006.01.016 · Cited by 53 · see citing works
Peeters, P. J., Aerssens, J., Hoogt, R. D., STANISZ, A. M., Göhlmann, H. W. H., Hillsley, K., Meulemans, A., Grundy, D., Stead, R. H., & Coulie, B. J. (2005) · Physiological Genomics · doi:10.1152/physiolgenomics.00169.2005 · Cited by 50 · see citing works
Self-citationXia, C., Gulick, M. A., Yu, S. J., Grider, J. R., Murthy, K. S., Kuemmerle, J. F., Akbarali, H. I., & Qiao, L. Y. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-30 · Cited by 49 · see citing works
Sullivan, C. N., Raboin, S. J., Gulley, S., Sinzobahamvya, N. T., Green, G. M., Reeve, J. R., & Sayegh, A. I. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00490.2006 · Cited by 49 · see citing works
Udit, S., & Gautron, L. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00134 · Cited by 49 · see citing works
Gallaher, Z. R., Ryu, V., Herzog, T., Ritter, R. C., & Czaja, K. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.01.079 · Cited by 47 · see citing works
Azari, E. K., Ramachandran, D., Weibel, S., Arnold, M., Romano, A., Gaetani, S., Langhans, W., & Mansouri, A. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00067.2014 · Cited by 46 · see citing works
Hayes, M. R., & Covașă, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.018 · Cited by 46 · see citing works
Clerici, L., Bottari, D., & Bottari, B. (2025) · Current Nutrition Reports · doi:10.1007/s13668-025-00619-2 · Cited by 53 · see citing works
Neural regulation of intestinal nutrient absorption
Mourad, F. H., & Saadé, N. E. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.07.010 · Cited by 44 · see citing works
Brainstem Control of the Gastric Function
Rogers, R., & Hermann, G. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-382026-6.00031-2 · Cited by 28 · see citing works
Ye, Y., Haija, M. A. E., Morgan, D. A., Guo, D., Song, Y., Frank, A. P., Tian, L., Riedl, R. A., Burnett, C. M.-L., Gao, Z., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108270 · Cited by 42 · see citing works
Fatty acid oxidation in the energostatic control of eating—A new idea
Langhans, W. (2008) · Appetite · doi:10.1016/j.appet.2008.06.014 · Cited by 41 · see citing works
Peiris, M., Aktar, R., Reed, D. E., Cibert‐Goton, V., Zdanaviciene, A., Halder, W., Robinow, A. D., Corke, S., Dogra, H., Knowles, C. H., et al. (2021) · Gut · doi:10.1136/gutjnl-2020-323219 · Cited by 40 · see citing works
Self-citationExtrinsic Sensory Afferent Nerves Innervating the Gastrointestinal Tract
Beyak, M. J., Bulmer, D. C., Jiang, W. G., Keating, C., Rong, W., & Grundy, D. (2006) · Elsevier eBooks · doi:10.1016/b978-012088394-3/50028-3 · Cited by 41 · see citing works
Self-citationMacrophages regulate gastrointestinal motility through complement component 1q
Pendse, M., Selle, H. D., Võ, N. H., Quinn, G. M., Dende, C., Li, Y., Salinas, C. N., Srinivasan, T., Propheter, D. C., Crofts, A. A., et al. (2023) · eLife · doi:10.7554/elife.78558 · Cited by 36 · see citing works
Plasticity of vagal afferent signaling in the gut
Grabauskas, G., & Owyang, C. (2017) · Medicina · doi:10.1016/j.medici.2017.03.002 · Cited by 38 · see citing works
- Authors
- Berthoud, H. R., Blackshaw, L. A., Brookes, S. J. H., & Grundy, D.
- Affiliations
- Pennington Biomedical Research Center (US)
- Royal Adelaide Hospital (AU)
- Flinders University (AU)
- University of Sheffield (GB)
- Corresponding author
- Berthoud, H. R.
- Venue
- Neurogastroenterology & Motility
- Publisher
- Wiley
- Published
- 2004-04
- Volume
- 16
- Issue
- s1
- Pages
- 28-33
- ISSN
- 1350-1925 (ISSN-L)
- 1365-2982
- OpenAlex
- W1972094807
- Cited by
- 274
- References
- 39
- Citations by year
- 2026: 9 · 2025: 7 · 2024: 11 · 2023: 10 · 2022: 15 · 2021: 17 · 2020: 11 · 2019: 10 · 2018: 13 · 2017: 10 · 2016: 18 · 2015: 7 · 2014: 16 · 2013: 6 · 2012: 20
- FWCI
- 2.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurogastroenterology & Motility (publishedVersion)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Flinders Academic Commons (Flinders University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- neuroanatomy, vagal afferents, splanchnic afferents, tension receptors, visceral hypersensitivity, visceral sensation
- MeSH terms
- Animals, Digestive System, Humans, Nerve Endings, Neuronal Plasticity, Enteric Nervous System, Visceral Afferents
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review