1932

Abstract

Guided by sight, scent, texture, and taste, animals ingest food. Once ingested, it is up to the gut to make sense of the food's nutritional value. Classic sensory systems rely on neuroepithelial circuits to convert stimuli into signals that guide behavior. However, sensation of the gut milieu was thought to be mediated only by the passive release of hormones until the discovery of synapses in enteroendocrine cells. These are gut sensory epithelial cells, and those that form synapses are referred to as neuropod cells. Neuropod cells provide the foundation for the gut to transduce sensory signals from the intestinal milieu to the brain through fast neurotransmission onto neurons, including those of the vagus nerve. These findings have sparked a new field of exploration in sensory neurobiology—that of gut-brain sensory transduction.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-091619-022657
2020-07-08
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/neuro/43/1/annurev-neuro-091619-022657.html?itemId=/content/journals/10.1146/annurev-neuro-091619-022657&mimeType=html&fmt=ahah

Literature Cited

  1. Alcaino C, Knutson KR, Treichel AJ, Yildiz G, Strege PR et al. 2018. A population of gut epithelial enterochromaffin cells is mechanosensitive and requires Piezo2 to convert force into serotonin release. PNAS 115:E7632–41
    [Google Scholar]
  2. Altschuler SM, Ferenci DA, Lynn RB, Miselis RR 1991. Representation of the cecum in the lateral dorsal motor nucleus of the vagus nerve and commissural subnucleus of the nucleus tractus solitarii in rat. J. Comp. Neurol. 304:261–74
    [Google Scholar]
  3. Bai L, Mesgarzadeh S, Ramesh KS, Huey EL, Liu Y, Gray LA 2019. Genetic identification of vagal sensory neurons that control feeding. Cell 179:51129–43.e23
    [Google Scholar]
  4. Ball GG. 1974. Vagotomy: effect on electrically elicited eating and self-stimulation in the lateral hypothalamus. Science 184:484–85
    [Google Scholar]
  5. Bayliss WM, Starling EH. 1902. The mechanism of pancreatic secretion. J. Physiol. 28:325–53
    [Google Scholar]
  6. Bellono NW, Bayrer JR, Leitch DB, Castro J, Zhang C et al. 2017. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 170:185–98.e16
    [Google Scholar]
  7. Berthoud HR, Neuhuber WL. 2000. Functional and chemical anatomy of the afferent vagal system. Auton. Neurosci. 85:1–17
    [Google Scholar]
  8. Beutler LR, Chen Y, Ahn JS, Lin YC, Essner RA, Knight ZA 2017. Dynamics of gut-brain communication underlying hunger. Neuron 96:461–75.e5
    [Google Scholar]
  9. Bogunovic M, Dave SH, Tilstra JS, Chang DT, Harpaz N et al. 2007. Enteroendocrine cells express functional Toll-like receptors. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1770–83
    [Google Scholar]
  10. Bohórquez DV, Shahid RA, Erdmann A, Kreger AM, Wang Y et al. 2015. Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J. Clin. Investig. 125:782–86
    [Google Scholar]
  11. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM et al. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. PNAS 108:16050–55
    [Google Scholar]
  12. Brookes SJ, Spencer NJ, Costa M, Zagorodnyuk VP 2013. Extrinsic primary afferent signalling in the gut. Nat. Rev. Gastroenterol. Hepatol. 10:286–96
    [Google Scholar]
  13. Bulbring E, Crema A. 1959. The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa. J. Physiol. 146:18–28
    [Google Scholar]
  14. Chaudhri OB, Salem V, Murphy KG, Bloom SR 2008. Gastrointestinal satiety signals. Annu. Rev. Physiol. 70:239–55
    [Google Scholar]
  15. Chimerel C, Emery E, Summers DK, Keyser U, Gribble FM, Reimann F 2014. Bacterial metabolite indole modulates incretin secretion from intestinal enteroendocrine L cells. Cell Rep 9:1202–8
    [Google Scholar]
  16. Chin A, Svejda B, Gustafsson BI, Granlund AB, Sandvik AK et al. 2012. The role of mechanical forces and adenosine in the regulation of intestinal enterochromaffin cell serotonin secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 302:G397–405
    [Google Scholar]
  17. Cho HJ, Robinson ES, Rivera LR, McMillan PJ, Testro A et al. 2014. Glucagon-like peptide 1 and peptide YY are in separate storage organelles in enteroendocrine cells. Cell Tissue Res 357:63–69
    [Google Scholar]
  18. Clark KB, Krahl SE, Smith DC, Jensen RA 1995. Post-training unilateral vagal stimulation enhances retention performance in the rat. Neurobiol. Learn. Mem. 63:213–16
    [Google Scholar]
  19. Clark KB, Smith DC, Hassert DL, Browning RA, Naritoku DK, Jensen RA 1998. Posttraining electrical stimulation of vagal afferents with concomitant vagal efferent inactivation enhances memory storage processes in the rat. Neurobiol. Learn. Mem. 70:364–73
    [Google Scholar]
  20. Cohen LJ, Esterhazy D, Kim SH, Lemetre C, Aguilar RR et al. 2017. Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature 549:48–53
    [Google Scholar]
  21. Craig AD. 2005. Forebrain emotional asymmetry: a neuroanatomical basis. ? Trends Cogn. Sci. 9:566–71
    [Google Scholar]
  22. Crick FHC 1979. Thinking about the brain. Sci. Am. 241:3219–33
    [Google Scholar]
  23. Cunningham JT, Mifflin SW, Gould GG, Frazer A 2008. Induction of c-Fos and ΔFosB immunoreactivity in rat brain by vagal nerve stimulation. Neuropsychopharmacology 33:1884–95
    [Google Scholar]
  24. Daly K, Al-Rammahi M, Moran A, Marcello M, Ninomiya Y, Shirazi-Beechey SP 2013. Sensing of amino acids by the gut-expressed taste receptor T1R1-T1R3 stimulates CCK secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 304:G271–82
    [Google Scholar]
  25. Davidson TL, Kanoski SE, Chan K, Clegg DJ, Benoit SC, Jarrard LE 2010. Hippocampal lesions impair retention of discriminative responding based on energy state cues. Behav. Neurosci. 124:97–105
    [Google Scholar]
  26. Davison JS, Clarke GD. 1988. Mechanical properties and sensitivity to CCK of vagal gastric slowly adapting mechanoreceptors. Am. J. Physiol. 255:G55–61
    [Google Scholar]
  27. de Araujo IE, Oliveira-Maia AJ, Sotnikova TD, Gainetdinov RR, Caron MG et al. 2008. Food reward in the absence of taste receptor signaling. Neuron 57:930–41
    [Google Scholar]
  28. Depoortere I. 2014. Taste receptors of the gut: emerging roles in health and disease. Gut 63:179–90
    [Google Scholar]
  29. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B et al. 2011. Normal gut microbiota modulates brain development and behavior. PNAS 108:3047–52
    [Google Scholar]
  30. Dinan TG, Cryan JF. 2017. Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J. Physiol. 595:489–503
    [Google Scholar]
  31. Dlugosz A, Muschiol S, Zakikhany K, Assadi G, D'Amato M, Lindberg G 2014. Human enteroendocrine cell responses to infection with Chlamydia trachomatis: a microarray study. Gut Pathog 6:24
    [Google Scholar]
  32. Dlugosz A, Zakikhany K, Muschiol S, Hultenby K, Lindberg G 2011. Infection of human enteroendocrine cells with Chlamydia trachomatis: a possible model for pathogenesis in irritable bowel syndrome. Neurogastroenterol. Motil. 23:928–34
    [Google Scholar]
  33. Drucker DJ, Yusta B. 2014. Physiology and pharmacology of the enteroendocrine hormone glucagon-like peptide-2. Annu. Rev. Physiol. 76:561–83
    [Google Scholar]
  34. Duca FA, Swartz TD, Sakar Y, Covasa M 2012. Increased oral detection, but decreased intestinal signaling for fats in mice lacking gut microbiota. PLOS ONE 7:e39748
    [Google Scholar]
  35. Engelstoft MS, Park WM, Sakata I, Kristensen LV, Husted AS et al. 2013. Seven transmembrane G protein–coupled receptor repertoire of gastric ghrelin cells. Mol. Metab. 2:376–92
    [Google Scholar]
  36. Feyrter F. 1938. Uber diffuse endokrine epitheliale Organe Leipzig, Ger: J.A. Barth
    [Google Scholar]
  37. Follesa P, Biggio F, Gorini G, Caria S, Talani G et al. 2007. Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain. Brain Res 1179:28–34
    [Google Scholar]
  38. Fothergill LJ, Callaghan B, Hunne B, Bravo DM, Furness JB 2017. Costorage of enteroendocrine hormones evaluated at the cell and subcellular levels in male mice. Endocrinology 158:2113–23
    [Google Scholar]
  39. Fraser KA, Davison JS. 1992. Cholecystokinin-induced c-fos expression in the rat brain stem is influenced by vagal nerve integrity. Exp. Physiol. 77:225–28
    [Google Scholar]
  40. Fukumoto S, Tatewaki M, Yamada T, Fujimiya M, Mantyh C et al. 2003. Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284:R1269–76
    [Google Scholar]
  41. Glass LL, Calero-Nieto FJ, Jawaid W, Larraufie P, Kay RG et al. 2017. Single-cell RNA-sequencing reveals a distinct population of proglucagon-expressing cells specific to the mouse upper small intestine. Mol. Metab. 6:1296–303
    [Google Scholar]
  42. Greenberg D, Smith GP, Gibbs J 1990. Intraduodenal infusions of fats elicit satiety in sham-feeding rats. Am. J. Physiol. 259:R110–18
    [Google Scholar]
  43. Gribble FM, Reimann F. 2016. Enteroendocrine cells: chemosensors in the intestinal epithelium. Annu. Rev. Physiol. 78:277–99
    [Google Scholar]
  44. Haber AL, Biton M, Rogel N, Herbst RH, Shekhar K et al. 2017. A single-cell survey of the small intestinal epithelium. Nature 551:333–39
    [Google Scholar]
  45. Han W, Tellez LA, Perkins MH, Perez IO, Qu T et al. 2018. A neural circuit for gut-induced reward. Cell 175:665–78 2018. Cell 175:887–88
    [Google Scholar]
  46. Heidenhain R. 1870. Untersuchungen über den Bau der Labdrüsen. Arch. Mikrosk. Anat. 6:368–406
    [Google Scholar]
  47. Heredia DJ, Dickson EJ, Bayguinov PO, Hennig GW, Smith TK 2009. Localized release of serotonin (5-hydroxytryptamine) by a fecal pellet regulates migrating motor complexes in murine colon. Gastroenterology 136:1328–38
    [Google Scholar]
  48. Hofer D, Puschel B, Drenckhahn D 1996. Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. PNAS 93:6631–34
    [Google Scholar]
  49. Ichikawa H, De Repentigny Y, Kothary R, Sugimoto T 2006. The survival of vagal and glossopharyngeal sensory neurons is dependent upon dystonin. Neuroscience 137:531–36
    [Google Scholar]
  50. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ et al. 2007. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. PNAS 104:15069–74
    [Google Scholar]
  51. Jeanningros R. 1982. Vagal unitary responses to intestinal amino acid infusions in the anesthetized cat: a putative signal for protein induced satiety. Physiol. Behav. 28:9–21
    [Google Scholar]
  52. Kaelberer MM, Buchanan KL, Klein ME, Barth BB, Montoya MM et al. 2018. A gut-brain neural circuit for nutrient sensory transduction. Science 361:eaat5236
    [Google Scholar]
  53. Kaji I, Karaki S, Tanaka R, Kuwahara A 2011. Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide. J. Mol. Histol. 42:27–38
    [Google Scholar]
  54. Kandel ER, Schwartz JH, Jessell TM 2000. Principles of Neural Science New York: McGraw-Hill
    [Google Scholar]
  55. Klarer M, Arnold M, Gunther L, Winter C, Langhans W, Meyer U 2014. Gut vagal afferents differentially modulate innate anxiety and learned fear. J. Neurosci. 34:7067–76
    [Google Scholar]
  56. Kokrashvili Z, Rodriguez D, Yevshayeva V, Zhou H, Margolskee RF, Mosinger B 2009. Release of endogenous opioids from duodenal enteroendocrine cells requires Trpm5. Gastroenterology 137:598–606.e2
    [Google Scholar]
  57. Kupari J, Haring M, Agirre E, Castelo-Branco G, Ernfors P 2019. An atlas of vagal sensory neurons and their molecular specialization. Cell Rep 27:2508–23.e4
    [Google Scholar]
  58. Lal S, Kirkup AJ, Brunsden AM, Thompson DG, Grundy D 2001. Vagal afferent responses to fatty acids of different chain length in the rat. Am. J. Physiol. Gastrointest. Liver Physiol. 281:G907–15
    [Google Scholar]
  59. Lange CG, James W 1922. A Series of Reprints and Translations, Vol. 1: The Emotions Baltimore, MD: Williams & Wilkins Co.
    [Google Scholar]
  60. Larraufie P, Dore J, Lapaque N, Blottiere HM 2017. TLR ligands and butyrate increase Pyy expression through two distinct but inter-regulated pathways. Cell Microbiol 19:e12648
    [Google Scholar]
  61. Lebrun LJ, Lenaerts K, Kiers D, Pais de Barros JP, Le Guern N et al. 2017. Enteroendocrine L cells sense LPS after gut barrier injury to enhance GLP-1 secretion. Cell Rep 21:1160–68
    [Google Scholar]
  62. Liou AP, Chavez DI, Espero E, Hao S, Wank SA, Raybould HE 2011a. Protein hydrolysate-induced cholecystokinin secretion from enteroendocrine cells is indirectly mediated by the intestinal oligopeptide transporter PepT1. Am. J. Physiol. Gastrointest. Liver Physiol. 300:G895–902
    [Google Scholar]
  63. Liou AP, Lu X, Sei Y, Zhao X, Pechhold S et al. 2011b. The G-protein–coupled receptor GPR40 directly mediates long-chain fatty acid–induced secretion of cholecystokinin. Gastroenterology 140:903–12
    [Google Scholar]
  64. Lovén C. 1868. Beiträge zur Kenntniss vom Bau der Geschmackswärzchen der Zunge. Arch. Mikrosk. Anat. 4:96–110
    [Google Scholar]
  65. Lu VB, Rievaj J, O'Flaherty EA, Smith CA, Pais R et al. 2019. Adenosine triphosphate is co-secreted with glucagon-like peptide-1 to modulate intestinal enterocytes and afferent neurons. Nat. Commun. 10:1029
    [Google Scholar]
  66. Lund ML, Egerod KL, Engelstoft MS, Dmytriyeva O, Theodorsson E et al. 2018. Enterochromaffin 5-HT cells—a major target for GLP-1 and gut microbial metabolites. Mol. Metab. 11:70–83
    [Google Scholar]
  67. Lundberg JM, Dahlstrom A, Bylock A, Ahlman H, Pettersson G et al. 1978. Ultrastructural evidence for an innervation of epithelial enterochromaffine cells in the guinea pig duodenum. Acta Physiol. Scand. 104:3–12
    [Google Scholar]
  68. Margolskee RF. 2002. Molecular mechanisms of bitter and sweet taste transduction. J. Biol. Chem. 277:1–4
    [Google Scholar]
  69. Mei N. 1978. Vagal glucoreceptors in the small intestine of the cat. J. Physiol. 282:485–506
    [Google Scholar]
  70. Monnikes H, Lauer G, Bauer C, Tebbe J, Zittel TT, Arnold R 1997. Pathways of Fos expression in locus ceruleus, dorsal vagal complex, and PVN in response to intestinal lipid. Am. J. Physiol. 273:R2059–71
    [Google Scholar]
  71. Mordes JP, Herrera MG, Silen W 1977. Decreased weight gain and food intake in vagotomized rats. Proc. Soc. Exp. Biol. Med. 156:257–60
    [Google Scholar]
  72. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G et al. 2002. An amino-acid taste receptor. Nature 416:199–202
    [Google Scholar]
  73. Newson B, Ahlman H, Dahlstrom A, Das Gupta TK, Nyhus LM 1979. On the innervation of the ileal mucosa in the rat—a synapse. Acta Physiol. Scand. 105:387–89
    [Google Scholar]
  74. Norgren R, Smith GP. 1988. Central distribution of subdiaphragmatic vagal branches in the rat. J. Comp. Neurol. 273:207–23
    [Google Scholar]
  75. Paintal AS. 1953. Impulses in vagal afferent fibres from stretch receptors in the stomach and their role in the peripheral mechanism of hunger. Nature 172:1194–95
    [Google Scholar]
  76. Palazzo M, Balsari A, Rossini A, Selleri S, Calcaterra C et al. 2007. Activation of enteroendocrine cells via TLRs induces hormone, chemokine, and defensin secretion. J. Immunol. 178:4296–303
    [Google Scholar]
  77. Pavlov IP. 1910. The Work of the Digestive Glands London: Griffin
    [Google Scholar]
  78. Phifer CB, Berthoud HR. 1998. Duodenal nutrient infusions differentially affect sham feeding and Fos expression in rat brain stem. Am. J. Physiol. 274:R1725–33
    [Google Scholar]
  79. Phillips AG, Nikaido RS. 1975. Disruption of brain stimulation–induced feeding by dopamine receptor blockade. Nature 258:750–51
    [Google Scholar]
  80. Phillips RJ, Powley TL. 1998. Gastric volume detection after selective vagotomies in rats. Am. J. Physiol. 274:R1626–38
    [Google Scholar]
  81. Prechtl JC, Powley TL. 1990. The fiber composition of the abdominal vagus of the rat. Anat. Embryol. 181:101–15
    [Google Scholar]
  82. Psichas A, Sleeth ML, Murphy KG, Brooks L, Bewick GA et al. 2015. The short chain fatty acid propionate stimulates GLP-1 and PYY secretion via free fatty acid receptor 2 in rodents. Int. J. Obes. 39:424–29
    [Google Scholar]
  83. Randich A, Tyler WJ, Cox JE, Meller ST, Kelm GR, Bharaj SS 2000. Responses of celiac and cervical vagal afferents to infusions of lipids in the jejunum or ileum of the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 278:R34–43
    [Google Scholar]
  84. Reimann F, Habib AM, Tolhurst G, Parker HE, Rogers GJ, Gribble FM 2008. Glucose sensing in L cells: a primary cell study. Cell Metab 8:532–39
    [Google Scholar]
  85. Rezek M, Vanderweele DA, Novin D 1975. Stages in the recovery of feeding following vagotomy in rabbits. Behav. Biol. 14:75–84
    [Google Scholar]
  86. Richards P, Parker HE, Adriaenssens AE, Hodgson JM, Cork SC et al. 2014. Identification and characterization of GLP-1 receptor-expressing cells using a new transgenic mouse model. Diabetes 63:1224–33
    [Google Scholar]
  87. Rinaman L, Baker EA, Hoffman GE, Stricker EM, Verbalis JG 1998. Medullary c-Fos activation in rats after ingestion of a satiating meal. Am. J. Physiol. 275:R262–68
    [Google Scholar]
  88. Sakura H, Ashcroft SJ, Terauchi Y, Kadowaki T, Ashcroft FM 1998. Glucose modulation of ATP-sensitive K-currents in wild-type, homozygous and heterozygous glucokinase knock-out mice. Diabetologia 41:654–59
    [Google Scholar]
  89. Sanchez M, Darimont C, Panahi S, Drapeau V, Marette A et al. 2017. Effects of a diet-based weight-reducing program with probiotic supplementation on satiety efficiency, eating behaviour traits, and psychosocial behaviours in obese individuals. Nutrients 9:284
    [Google Scholar]
  90. Santos-Hernandez M, Miralles B, Amigo L, Recio I 2018. Intestinal signaling of proteins and digestion-derived products relevant to satiety. J. Agric. Food Chem. 66:10123–31
    [Google Scholar]
  91. Schwalbe G. 1867. Das Epithel der Papillae vallatae. Arch. Mikrosk. Anat. 3:504–8
    [Google Scholar]
  92. Schwartz GJ, McHugh PR, Moran TH 1991a. Integration of vagal afferent responses to gastric loads and cholecystokinin in rats. Am. J. Physiol. 261:R64–69
    [Google Scholar]
  93. Schwartz GJ, Netterville LA, McHugh PR, Moran TH 1991b. Gastric loads potentiate inhibition of food intake produced by a cholecystokinin analogue. Am. J. Physiol. 261:R1141–46
    [Google Scholar]
  94. Schwartz GJ, Tougas G, Moran TH 1995. Integration of vagal afferent responses to duodenal loads and exogenous CCK in rats. Peptides 16:707–11
    [Google Scholar]
  95. Sclafani A, Ackroff K, Schwartz GJ 2003. Selective effects of vagal deafferentation and celiac-superior mesenteric ganglionectomy on the reinforcing and satiating action of intestinal nutrients. Physiol. Behav. 78:285–94
    [Google Scholar]
  96. Sgritta M, Dooling SW, Buffington SA, Momin EN, Francis MB et al. 2019. Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron 101:246–59.e6
    [Google Scholar]
  97. Sidhu M, Cooke HJ. 1995. Role for 5-HT and ACh in submucosal reflexes mediating colonic secretion. Am. J. Physiol. 269:G346–51
    [Google Scholar]
  98. Suarez AN, Hsu TM, Liu CM, Noble EE, Cortella AM et al. 2018. Gut vagal sensory signaling regulates hippocampus function through multi-order pathways. Nat. Commun. 9:2181
    [Google Scholar]
  99. Sun L, Perakyla J, Holm K, Haapasalo J, Lehtimaki K et al. 2017. Vagus nerve stimulation improves working memory performance. J. Clin. Exp. Neuropsychol. 39:954–64
    [Google Scholar]
  100. Sundaresan S, Abumrad NA. 2015. Dietary lipids inform the gut and brain about meal arrival via CD36-mediated signal transduction. J. Nutr. 145:2195–200
    [Google Scholar]
  101. Sundaresan S, Shahid R, Riehl TE, Chandra R, Nassir F et al. 2013. CD36-dependent signaling mediates fatty acid-induced gut release of secretin and cholecystokinin. FASEB J 27:1191–202
    [Google Scholar]
  102. Swartz TD, Duca FA, de Wouters T, Sakar Y, Covasa M 2012. Up-regulation of intestinal type 1 taste receptor 3 and sodium glucose luminal transporter-1 expression and increased sucrose intake in mice lacking gut microbiota. Br. J. Nutr. 107:621–30
    [Google Scholar]
  103. Symonds EL, Peiris M, Page AJ, Chia B, Dogra H et al. 2015. Mechanisms of activation of mouse and human enteroendocrine cells by nutrients. Gut 64:618–26
    [Google Scholar]
  104. Thomas C, Gioiello A, Noriega L, Strehle A, Oury J et al. 2009. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab 10:167–77
    [Google Scholar]
  105. Walls EK, Phillips RJ, Wang FB, Holst MC, Powley TL 1995. Suppression of meal size by intestinal nutrients is eliminated by celiac vagal deafferentation. Am. J. Physiol. 269:R1410–19
    [Google Scholar]
  106. Wang F, Knutson K, Alcaino C, Linden DR, Gibbons SJ et al. 2017. Mechanosensitive ion channel Piezo2 is important for enterochromaffin cell response to mechanical forces. J. Physiol. 595:79–91
    [Google Scholar]
  107. Williams EK, Chang RB, Strochlic DE, Umans BD, Lowell BB, Liberles SD 2016. Sensory neurons that detect stretch and nutrients in the digestive system. Cell 166:209–21
    [Google Scholar]
  108. Worthington JJ, Klementowicz JE, Rahman S, Czajkowska BI, Smedley C et al. 2013. Loss of the TGFβ-activating integrin αvβ8 on dendritic cells protects mice from chronic intestinal parasitic infection via control of type 2 immunity. PLOS Pathog 9:e1003675
    [Google Scholar]
  109. Young SH, Rey O, Sternini C, Rozengurt E 2010. Amino acid sensing by enteroendocrine STC-1 cells: role of the Na+-coupled neutral amino acid transporter 2. Am. J. Physiol. Cell Physiol. 298:C1401–13
    [Google Scholar]
  110. Yox DP, Stokesberry H, Ritter RC 1991. Vagotomy attenuates suppression of sham feeding induced by intestinal nutrients. Am. J. Physiol. 260:R503–8
    [Google Scholar]
  111. Zhang X, Fogel R, Renehan WE 1992. Physiology and morphology of neurons in the dorsal motor nucleus of the vagus and the nucleus of the solitary tract that are sensitive to distension of the small intestine. J. Comp. Neurol. 323:432–48
    [Google Scholar]
  112. Zittel TT, De Giorgio R, Sternini C, Raybould HE 1994. Fos protein expression in the nucleus of the solitary tract in response to intestinal nutrients in awake rats. Brain Res 663:266–70
    [Google Scholar]
  113. Zuo Y, Smith DC, Jensen RA 2007. Vagus nerve stimulation potentiates hippocampal LTP in freely-moving rats. Physiol. Behav. 90:583–89
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-091619-022657
Loading
/content/journals/10.1146/annurev-neuro-091619-022657
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error