Loss of neurotrophin-3 from smooth muscle disrupts vagal gastrointestinal afferent signaling and satiation

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 11, 2013, Pages

  Fox, Edward A ^a   Biddinger, Jessica E ^a   Baquet, Zachary C ^b   Jones, Kevin R ^b   McAdams, Jennifer ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Conditional knockout; Food intake; Meal microstructure; Meal patterns; Vagus nerve

Indexed keywords

BETA GALACTOSIDASE; BRAIN DERIVED NEUROTROPHIC FACTOR; CRE RECOMBINASE; NEUROTROPHIN 3; PROTEIN C FOS; TRANSGELIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA POSTREMA; ARTICLE; BODY WEIGHT; BRAIN STEM; CONTROLLED STUDY; ENTORHINAL CORTEX; FEEDING; FEEDING BEHAVIOR; FOOD INTAKE; GASTROINTESTINAL TRACT FUNCTION; GENE INACTIVATION; HIPPOCAMPUS; LAMINA PROPRIA; LARGE INTESTINE; LOXP SITE; MOUSE; MUSCLE SPINDLE; NEGATIVE FEEDBACK; NONHUMAN; POLYADENYLATION; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REPORTER GENE; SATIETY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; SOLITARY TRACT NUCLEUS; STOMACH WALL; VAGUS NERVE;

CONDITIONAL KNOCKOUT; FOOD INTAKE; MEAL MICROSTRUCTURE; MEAL PATTERNS; VAGUS NERVE;

ANIMALS; BODY WEIGHT; EATING; FEEDING BEHAVIOR; FEMALE; GASTROINTESTINAL TRACT; MALE; MICE; MUSCLE, SMOOTH; NEUROTROPHIN 3; SATIATION; SIGNAL TRANSDUCTION; SOLITARY NUCLEUS; VAGUS NERVE;

EID: 84889576042     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00337.2013     Document Type: Article

References (98)

1. Airaksinen MS, Koltzenburg M, Lewin GR, Masu Y, Helbig C, Wolf E, Brem G, Toyka KV, Thoenen H, Meyer M. Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron 16: 287-295, 1996.
2. Albers KM, Perrone TN, Goodness TP, Jones ME, Green MA, Davis BM. Cutaneous overexpression of NT-3 increases sensory and sympathetic neuron number and enhances touch dome and hair follicle innervation. J Cell Biol 134: 487-497, 1996.
3. Arvanov VL, Seebach BS, Mendell LM. NT-3 evokes an LTP-like facilitation of AMPA/kainate receptor-mediated synaptic transmission in the neonatal rat spinal cord. J Neurophysiol 84: 752-758, 2000.
4. Bates B, Rios M, Trumpp A, Chen C, Fan G, Bishop JM, Jaenisch R. Neurotrophin-3 is required for proper cerebellar development. Nat Neurosci 2: 115-117, 1999.
5. Berthoud HR. The vagus nerve, food intake and obesity. Regul Pept 149: 15-25, 2008.
6. Biddinger JE, Fox EA. Increased vagal sensory neuron and intestinal axon bundle number in mice with smooth muscle-knockout (KO) of brain-derived neurotrophic factor (BDNF) may contribute to augmented intestinal mechanoreceptor innervation and satiation (Abstract). Program No. 47613. 2013 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2013.
7. Buchman VL, Davies AM. Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development 118: 989-1001, 1993.
8. Chalazonitis A, Pham TD, Rothman TP, DiStefano PS, Bothwell M, Blair-Flynn J, Tessarollo L, Gershon MD. Neurotrophin-3 is required for the survival-differentiation of subsets of developing enteric neurons. J Neurosci 21: 5620-5636, 2001.
9. Chavez M, Kelly L, York DA, Berthoud HR. Chemical lesion of visceral afferents causes transient overconsumption of unfamiliar high-fat diets in rats. Am J Physiol Regul Integr Comp Physiol 272: R1657-R1663, 1997.
10. Chen Y, Zeng J, Cen L, Wang X, Yao G, Wang W, Qi W, Kong K. Multiple roles of the p75 neurotrophin receptor in the nervous system. J Int Med Res 37: 281-288, 2009.
11. Chen Z, Wu J, Yang C, Fan P, Balazs L, Jiao Y, Lu M, Gu W, Li C, Pfeffer LM, Tigyi G, Yue J. DiGeorge syndrome critical region 8 (DGCR8) protein-mediated microRNA biogenesis is essential for vascular smooth muscle cell development in mice. J Biol Chem 287: 19018-19028, 2012.
12. Chi MM, Fan G, Fox EA. Increased short-term food satiation and sensitivity to cholecystokinin in neurotrophin-4 knock-in mice. Am J Physiol Regul Integr Comp Physiol 287: R1044-R1053, 2004.
13. Clifton PG, Vickers SP, Somerville EM. Little and often: ingestive behavior patterns following hippocampal lesions in rats. Behav Neurosci 112: 502-511, 1998.
14. Cordon-Cardo C, Tapley P, Jing SQ, Nanduri V, O'Rourke E, Lamballe F, Kovary K, Klein R, Jones KR, Reichardt LF, Barbacid M. The trk tyrosine protein kinase mediates the mitogenic properties of nerve growth factor and neurotrophin-3. Cell 66: 173-183, 1991.
15. Covasa M, Ritter RC. Rats maintained on high-fat diets exhibit reduced satiety in response to CCK and bombesin. Peptides 19: 1407-1415, 1998.
16. Daly DM, Park SJ, Valinsky WC, Beyak MJ. Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse. J Physiol 589: 2857-2870, 2011.
17. Davidson TL, Chan K, Jarrard LE, Kanoski SE, Clegg DJ, Benoit SC. Contributions of the hippocampus and medial prefrontal cortex to energy and body weight regulation. Hippocampus 19: 235-252, 2009.
18. Davis JD. A model for the control of ingestion-20 years later. In: Progress in Psychobiology and Physiological Psychology, edited by Morrison AR and Fluharty SJ. San Diego, CA: Academic, 1998, p. 127-173.
19. de Lartigue G, Barbier de la Serre C, Espero E, Lee J, Raybould HE. Leptin resistance in vagal afferent neurons inhibits cholecystokinin signaling and satiation in diet induced obese rats. PLoS One 7: e32967, 2012.
20. Delafoy L, Gelot A, Ardid D, Eschalier A, Bertrand C, Doherty AM, Diop L. Interactive involvement of brain derived neurotrophic factor, nerve growth factor, and calcitonin gene related peptide in colonic hypersensitivity in the rat. Gut 55: 940-945, 2006.
21. Dockray GJ, Burdyga G. Plasticity in vagal afferent neurones during feeding and fasting: mechanisms and significance. Acta Physiol (Oxf) 201: 313-321, 2011.
22. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87: 27-45, 1985.
23. Dymecki SM. Flp recombinase promotes site-specific DNA recombination in embryonic stem cells and transgenic mice. Proc Natl Acad Sci USA 93: 6191-6196, 1996.
24. ElShamy WM, Ernfors P. Brain-derived neurotrophic factor, neurotrophin- 3, and neurotrophin-4 complement and cooperate with each other sequentially during visceral neuron development. J Neurosci 17: 8667-8675, 1997.
25. Emond M, Schwartz GJ, Moran TH. Meal-related stimuli differentially induce c-Fos activation in the nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 280: R1315-R1321, 2001.
26. Ernfors P. Local and target-derived actions of neurotrophins during peripheral nervous system development. Cell Mol Life Sci 58: 1036-1044, 2001.
27. Ernfors P, Lee KF, Kucera J, Jaenisch R. Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77: 503-512, 1994.
28. Ernfors P, Merlio JP, Persson H. Cells expressing messenger-RNA for neurotrophins and their receptors during embryonic rat development. Eur J Neurosci 4: 1140-1158, 1992.
29. Farinas I, Jones KR, Backus C, Wang XY, Reichardt LF. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369: 658-661, 1994.
30. Farinas I, Wilkinson GA, Backus C, Reichardt LF, Patapoutian A. Characterization of neurotrophin and Trk receptor functions in developing sensory ganglia: direct NT-3 activation of TrkB neurons in vivo. Neuron 21: 325-334, 1998.
31. Farinas I, Yoshida CK, Backus C, Reichardt LF. Lack of neurotrophin- 3 results in death of spinal sensory neurons and premature differentiation of their precursors. Neuron 17: 1065-1078, 1996.
32. Forloni G, Fisone G, Guaitani A, Ladinsky H, Consolo S. Role of the hippocampus in the sex-dependent regulation of eating behavior: studies with kainic acid. Physiol Behav 38: 321-326, 1986.
33. Fox EA. A genetic approach for investigating vagal sensory roles in regulation of gastrointestinal function and food intake. Auton Neurosci 126-127: 9-29, 2006.
34. Fox EA, Biddinger JE, Jones KR, McAdams J, Worman A. Mechanism of hyperphagia contributing to obesity in brain-derived neurotrophic factor knockout mice. Neuroscience 229: 176-199, 2013.
35. Fox EA, Byerly MS. A mechanism underlying mature-onset obesity: evidence from the hyperphagic phenotype of brain-derived neurotrophic factor mutants. Am J Physiol Regul Integr Comp Physiol 286: R994-R1004, 2004.
36. Fox EA, McAdams J. Smooth-muscle-specific expression of neurotrophin- 3 in mouse embryonic and neonatal gastrointestinal tract. Cell Tissue Res 340: 267-286, 2010.
37. Fox EA, Phillips RJ, Baronowsky EA, Byerly MS, Jones S, Powley TL. Neurotrophin-4 deficient mice have a loss of vagal intraganglionic mechanoreceptors from the small intestine and a disruption of short-term satiety. J Neurosci 21: 8602-8615, 2001.
38. Francis N, Farinas I, Brennan C, Rivas-Plata K, Backus C, Reichardt L, Landis S. NT-3, like NGF, is required for survival of sympathetic neurons, but not their precursors. Dev Biol 210: 411-427, 1999.
39. Fritzsch B, Farinas I, Reichardt LF. Lack of neurotrophin 3 causes losses of both classes of spiral ganglion neurons in the cochlea in a region-specific fashion. J Neurosci 17: 6213-6225, 1997.
40. Frutkin AD, Shi H, Otsuka G, Leveen P, Karlsson S, Dichek DA. A critical developmental role for tgfbr2 in myogenic cell lineages is revealed in mice expressing SM22-Cre, not SMMHC-Cre. J Mol Cell Cardiol 41: 724-731, 2006.
41. Genc B, Ozdinler PH, Mendoza AE, Erzurumlu RS. A chemoattractant role for NT-3 in proprioceptive axon guidance. PLoS Biol 2: e403, 2004.
42. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22: 6309-6314, 2002.
43. Gorski JA, Zeiler SR, Tamowski S, Jones KR. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J Neurosci 23: 6856-6865, 2003.
44. Hassane S, Claij N, Jodar M, Dedman A, Lauritzen I, Duprat F, Koenderman JS, van der Wal A, Breuning MH, de Heer E, Honore E, DeRuiter MC, Peters DJ. Pkd1-inactivation in vascular smooth muscle cells and adaptation to hypertension. Lab Invest 91: 24-32, 2011.
45. Hoehner JC, Wester T, Pahlman S, Olsen L. Localization of neurotrophins and their high-affinity receptors during human enteric nervous system development. Gastroenterology 110: 756-767, 1996.
46. Holtwick R, Gotthardt M, Skryabin B, Steinmetz M, Potthast R, Zetsche B, Hammer RE, Herz J, Kuhn M. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci USA 99: 7142-7147, 2002.
47. Huang EJ, Reichardt LF. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642, 2003.
48. Huang EJ, Wilkinson GA, Farinas I, Backus C, Zang K, Wong SL, Reichardt LF. Expression of Trk receptors in the developing mouse trigeminal ganglion: in vivo evidence for NT-3 activation of TrkA and TrkB in addition to TrkC. Development 126: 2191-2203, 1999.
49. Huber K, Kuehnel F, Wyatt S, Davies AM. TrkB expression and early sensory neuron survival are independent of endogenous BDNF. J Neurosci Res 59: 372-378, 2000.
50. Katoh-Semba R, Kaisho Y, Shintani A, Nagahama M, Kato K. Tissue distribution and immunocytochemical localization of neurotrophin-3 in the brain and peripheral tissues of rats. J Neurochem 66: 330-337, 1996.
51. Kelly LA, Chavez M, Berthoud HR. Transient overconsumption of novel foods by deafferentated rats: effects of novel diet composition. Physiol Behav 65: 793-800, 1999.
52. Klein R, Jing SQ, Nanduri V, O'Rourke E, Barbacid M. The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65: 189-197, 1991.
53. Kucera J, Fan G, Jaenisch R, Linnarsson S, Ernfors P. Dependence of developing group Ia afferents on neurotrophin-3. J Comp Neurol 363: 307-320, 1995.
54. Kuruvilla R, Zweifel LS, Glebova NO, Lonze BE, Valdez G, Ye H, Ginty DD. A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118: 243-255, 2004.
55. Langlois D, Hneino M, Bouazza L, Parlakian A, Sasaki T, Bricca G, Li JY. Conditional inactivation of TGF-beta type II receptor in smooth muscle cells and epicardium causes lethal aortic and cardiac defects. Transgenic Res 19: 1069-1082, 2010.
56. Lentz SI, Knudson CM, Korsmeyer SJ, Snider WD. Neurotrophins support the development of diverse sensory axon morphologies. J Neurosci 19: 1038-1048, 1999.
57. Lepore JJ, Cheng L, Min Lu M, Mericko PA, Morrisey EE, Parmacek MS. High-efficiency somatic mutagenesis in smooth muscle cells and cardiac myocytes in SM22alpha-Cre transgenic mice. Genesis 41: 179- 184, 2005.
58. Liebl DJ, Tessarollo L, Palko ME, Parada LF. Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. J Neurosci 17: 9113-9121, 1997.
59. Lommatzsch M, Braun A, Mannsfeldt A, Botchkarev VA, Botchkareva NV, Paus R, Fischer A, Lewin GR, Renz H. Abundant production of brain-derived neurotrophic factor by adult visceral epithelia. Implications for paracrine and target-derived neurotrophic functions. Am J Pathol 155: 1183-1193, 1999.
60. Maisonpierre PC, Belluscio L, Friedman B, Alderson RF, Wiegand SJ, Furth ME, Lindsay RM, Yancopoulos GD. NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5: 501-509, 1990.
61. Maisonpierre PC, Belluscio L, Squinto S, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247: 1446-1451, 1990.
62. Malhowski AJ, Hira H, Bashiruddin S, Warburton R, Goto J, Robert B, Kwiatkowski DJ, Finlay GA. Smooth muscle protein-22-mediated deletion of Tsc1 results in cardiac hypertrophy that is mTORC1-mediated and reversed by rapamycin. Hum Mol Genet 20: 1290-1305, 2011.
63. Maxwell IH, Harrison GS, Wood WM, Maxwell F. A DNA cassette containing a trimerized SV40 polyadenylation signal which efficiently blocks spurious plasmid-initiated transcription. Biotechniques 7: 276-280, 1989.
64. Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 112: 803-814, 2002.
65. Murphy MC, Fox EA. Anterograde tracing method using DiI to label vagal innervation of the embryonic and early postnatal mouse gastrointestinal tract. J Neurosci Methods 163: 213-225, 2007.
66. Oakley RA, Garner AS, Large TH, Frank E. Muscle sensory neurons require neurotrophin-3 from peripheral tissues during the period of normal cell death. Development 121: 1341-1350, 1995.
67. Ochodnicky P, Cruz CD, Yoshimura N, Cruz F. Neurotrophins as regulators of urinary bladder function. Nat Rev Urol 9: 628-637, 2012.
68. Oestreicher E, Knipper M, Arnold A, Zenner HP, Felix D. Neurotrophin 3 potentiates glutamatergic responses of IHC afferents in the cochlea in vivo. Eur J Neurosci 12: 1584-1590, 2000.
69. Pan Y, Balazs L, Tigyi G, Yue J. Conditional deletion of Dicer in vascular smooth muscle cells leads to the developmental delay and embryonic mortality. Biochem Biophys Res Commun 408: 369-374, 2011.
70. Patapoutian A, Backus C, Kispert A, Reichardt LF. Regulation of neurotrophin-3 expression by epithelial-mesenchymal interactions: the role of Wnt factors. Science 283: 1180-1183, 1999.
71. Raab M, Worl J, Brehmer A, Neuhuber WL. Reduction of NT-3 or TrkC results in fewer putative vagal mechanoreceptors in the mouse esophagus. Auton Neurosci 108: 22-31, 2003.
72. Rateri DL, Moorleghen JJ, Balakrishnan A, Owens AP 3rd, Howatt DA, Subramanian V, Poduri A, Charnigo R, Cassis LA, Daugherty A. Endothelial cell-specific deficiency of Ang II type 1a receptors attenuates Ang II-induced ascending aortic aneurysms in LDL receptor-/- mice. Circ Res 108: 574-581, 2011.
73. Rinaman L, Baker EA, Hoffman GE, Stricker EM, Verbalis JG. Medullary c-Fos activation in rats after ingestion of a satiating meal. Am J Physiol Regul Integr Comp Physiol 275: R262-R268, 1998.
74. Rinaman L, Levitt P. Establishment of vagal sensorimotor circuits during fetal development in rats. J Neurobiol 24: 641-659, 1993.
75. Scarisbrick IA, Jones EG, Isackson PJ. Coexpression of mRNAs for NGF, BDNF, and NT-3 in the cardiovascular system of the pre- and postnatal rat. J Neurosci 13: 875-893, 1993.
76. Schmidt EE, Taylor DS, Prigge JR, Barnett S, Capecchi MR. Illegitimate Cre-dependent chromosome rearrangements in transgenic mouse spermatids. Proc Natl Acad Sci USA 97: 13702-13707, 2000.
77. Schwartz GJ, Moran TH. Duodenal nutrient exposure elicits nutrientspecific gut motility and vagal afferent signals in rat. Am J Physiol Regul Integr Comp Physiol 274: R1236-R1242, 1998.
78. Schwartz GJ, Salorio CF, Skoglund C, Moran TH. Gut vagal afferent lesions increase meal size but do not block gastric preload-induced feeding suppression. Am J Physiol Regul Integr Comp Physiol 276: R1623-R1629, 1999.
79. Sobocki J, Krolczyk G, Herman RM, Matyja A, Thor PJ. Influence of vagal nerve stimulation on food intake and body weight-results of experimental studies. J Physiol Pharmacol 56, Suppl 6: 27-33, 2005.
80. Speer MY, Yang HY, Brabb T, Leaf E, Look A, Lin WL, Frutkin A, Dichek D, Giachelli CM. Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ Res 104: 733-741, 2009.
81. Stearns AT, Balakrishnan A, Radmanesh A, Ashley SW, Rhoads DB, Tavakkolizadeh A. Relative contributions of afferent vagal fibers to resistance to diet-induced obesity. Dig Dis Sci 57: 1281-1290, 2012.
82. Sternini C, Su D, Arakawa J, de Giorgio R, Rickman DW, Davis BM, Albers KM, Brecha NC. Cellular localization of Pan-trk immunoreactivity and trkC mRNA in the enteric nervous system. J Comp Neurol 368: 597-607, 1996.
83. Subramanian V, Golledge J, Ijaz T, Bruemmer D, Daugherty A. Pioglitazone-induced reductions in atherosclerosis occur via smooth muscle cell-specific interaction with PPAR_. Circ Res 107: 953-958, 2010.
84. Tessarollo L, Tsoulfas P, Donovan MJ, Palko ME, Blair-Flynn J, Hempstead BL, Parada LF. Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis. Proc Natl Acad Sci USA 94: 14776-14781, 1997.
85. Tessarollo L, Vogel KS, Palko ME, Reid SW, Parada LF. Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proc Natl Acad Sci USA 91: 11844-11848, 1994.
86. Tucker KL, Meyer M, Barde YA. Neurotrophins are required for nerve growth during development. Nat Neurosci 4: 29-37, 2001.
87. Ulupinar E, Jacquin MF, Erzurumlu RS. Differential effects of NGF and NT-3 on embryonic trigeminal axon growth patterns. J Comp Neurol 425: 202-218, 2000.
88. Umans L, Cox L, Tjwa M, Bito V, Vermeire L, Laperre K, Sipido K, Moons L, Huylebroeck D, Zwijsen A. Inactivation of Smad5 in endothelial cells and smooth muscle cells demonstrates that Smad5 is required for cardiac homeostasis. Am J Pathol 170: 1460-1472, 2007.
89. Vermehren-Schmaedick A, Jenkins VK, Hsieh HY, Brown AL, Page MP, Brooks VL, Balkowiec A. Upregulation of brain-derived neurotrophic factor expression in nodose ganglia and the lower brainstem of hypertensive rats. J Neurosci Res 91: 220-229, 2013.
90. Walls EK, Phillips RJ, Wang FB, Holst MC, Powley TL. Suppression of meal size by intestinal nutrients is eliminated by celiac vagal deafferentation. Am J Physiol Regul Integr Comp Physiol 269: R1410-R1419, 1995.
91. White FA, Silos-Santiago I, Molliver DC, Nishimura M, Phillips H, Barbacid M, Snider WD. Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J Neurosci 16: 4662-4672, 1996.
92. Wilson-Gerwing TD, Dmyterko MV, Zochodne DW, Johnston JM, Verge VM. Neurotrophin-3 suppresses thermal hyperalgesia associated with neuropathic pain and attenuates transient receptor potential vanilloid receptor-1 expression in adult sensory neurons. J Neurosci 25: 758-767, 2005.
93. Winter J. Brain derived neurotrophic factor, but not nerve growth factor, regulates capsaicin sensitivity of rat vagal ganglion neurones. Neurosci Lett 241: 21-24, 1998.
94. Xiang Z, Burnstock G. Development of nerves expressing P2X3 receptors in the myenteric plexus of rat stomach. Histochem Cell Biol 122: 111-119, 2004.
95. Yoganarasimha D, Rao G, Knierim JJ. Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 21: 1363-1374, 2011.
96. Yox DP, Stokesberry H, Ritter RC. Vagotomy attenuates suppression of sham feeding induced by intestinal nutrients. Am J Physiol Regul Integr Comp Physiol 260: R503-R508, 1991.
97. Zeeni N, Chaumontet C, Moyse E, Fromentin G, Tardivel C, Tome D, Jean A, Darcel N. A positive change in energy balance modulates TrkB expression in the hypothalamus and nodose ganglia of rats. Brain Res 1289: 49-55, 2009.
98. Zhou XF, Rush RA. Functional roles of neurotrophin 3 in the developing and mature sympathetic nervous system. Mol Neurobiol 13: 185-197, 1996.