Peptide and lipid modulation of glutamatergic afferent synaptic transmission in the solitary tract nucleus

Frontiers in Neuroscience

Volumn , Issue JAN, 2012, Pages

  Andresen, Michael C ^a   Fawley, Jessica A ^a   Hofmann, Mackenzie E ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Capsaicin; Neuropeptides; Solitary tract nucleus; TRPV1; Vagal afferents

Indexed keywords

ANGIOTENSIN; CANNABINOID RECEPTOR; CHOLECYSTOKININ; G PROTEIN COUPLED RECEPTOR; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GLUTAMATE DECARBOXYLASE 65; GLUTAMIC ACID; OPIATE; OXYTOCIN; SEROTONIN; VANILLOID RECEPTOR 1; VASOPRESSIN;

BRAIN NERVE CELL; BRAIN STEM; DEPOLARIZATION; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FOREBRAIN; GASTROINTESTINAL TRACT; HYPOTHALAMUS; INTERNEURON; LIPID ANALYSIS; MOTONEURON NUCLEUS; MYELINATION; NERVE FIBER; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PEPTIDE ANALYSIS; PHENOTYPE; PRESSORECEPTOR; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; REVIEW; SENSORY NERVE; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS; SYNAPTIC TRANSMISSION; VAGUS NERVE;

EID: 84878989638     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00191     Document Type: Review

References (224)

1. Aars, H., Myhre, L., and Haswell, B. (1978). The function of baroreceptor C fibres in the rabbit's aortic nerve. Acta Physiol. Scand. 102, 84-93.
2. Abbott, L. F., and Regehr, W. G. (2004). Synaptic computation. Nature 431, 796-803.
3. Affleck, V. S., Coote, J. H., and Pyner, S. (2012). The projection and synaptic organisation of NTS afferent connections with presympathetic neurons, GABA and nNOS neurons in the paraventricular nucleus of the hypothalamus. Neuroscience 219, 48-61.
4. Agostoni, E., Chinnock, J. E., De Burgh Daly, M., and Murray, J. G. (1957). Functional and histological studies of the vagus nerve and its branches to the heart, lungs and abdominal viscera in the cat. J. Physiol. (Lond.) 135, 182-205.
5. Ahluwalia, J., Urban, L., Capogna, M., Bevan, S., and Nagy, I. (2000). Cannabinoid 1 receptors are expressed in nociceptive primary sensory neurons. Neuroscience 100, 685-688.
6. Aicher, S. A., Sharma, S., and Pickel, V. M. (1999). N-methyl-D-aspartate receptors are present in vagal afferents and their dendritic targets in the nucleus tractus solitarius. Neuroscience 91, 119-132.
7. Alberti, K. G., Zimmet, P., and Shaw, J. (2005). The metabolic syndrome - a new worldwide definition. Lancet 366, 1059-1062.
8. Alberti, K. G., Zimmet, P., and Shaw, J. (2006). Metabolic syndrome - a new world-wide definition. A consensus statement from the International Diabetes Federation. Diabet. Med. 23, 469-480.
9. Alhadeff, A. L., Rupprecht, L. E., and Hayes, M. R. (2012). GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 153, 647-658.
10. Alheid, G. F., Jiao, W., and McCrimmon, D. R. (2011). Caudal nuclei of the rat nucleus of the solitary tract differentially innervate respiratory compartments within the ventrolateral medulla. Neuroscience 190, 207-227.
11. Altschuler, S. M., Ferenci, D. A., Lynn, R. B., and Miselis, R. R. (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, 261-274.
12. Amaya, F., Shimosato, G., Kawasaki, Y., Hashimoto, S., Tanaka, Y., Ji, R. R., et al. (2006). Induction of CB1 cannabinoid receptor by inflammation in primary afferent neurons facilitates antihyperalgesic effect of peripheral CB1 agonist. Pain 124, 175-183.
13. Anders, K., Ohndorf, W., Dermietzel, R., and Richter, D. W. (1993). Synapses between slowly adapting lung stretch receptor afferents and inspiratory beta-neurons in the nucleus of the solitary tract of cats: a light and electron microscopic analysis. J. Comp. Neurol. 335, 163-172.
14. Andresen, M. C., Bailey, T. W., Jin, Y.-H., McDougall, S. J., Peters, J. H., and Aicher, S. A. (2007a). Cellular heterogeneity within the solitary tract nucleus and visceral afferent processing - electrophysiological approaches to discerning pathway performance. Tzu Chi Med. J. 19, 181-185.
15. Andresen, M. C., Doyle, M. W., Bailey, T. W., and Jin, Y.-H. (2007b). "TRPV1 in central cardiovascular control: discerning the C-fiber afferent pathway," in Molecular Sensors for Cardiovascular Homeostasis, ed. D. H. Wang (New York: Springer), 93-109.
16. Andresen, M. C., Hofmann, M. E., and Fawley, J. A. (2012). Invited review: the un-silent majority - TRPV1 drives "spontaneous" transmission of unmyelinated primary afferents within cardiorespiratory NTS. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R1207-R1216.
17. Andresen, M. C., Krauhs, J. M., and Brown, A. M. (1978). Relationship of aortic wall baroreceptor properties during development in normotensive and spontaneously hypertensive rats. Circ. Res. 43, 728-738.
18. Andresen, M. C., and Kunze, D. L. (1994). Nucleus tractus solitarius: gateway to neural circulatory control. Annu. Rev. Physiol. 56, 93-116.
19. Andresen, M. C., and Mendelowitz, D. (1996). Sensory afferent neurotransmission in caudal nucleus tractus solitarius - common denominators. Chem. Senses 21, 387-395.
20. Andresen, M. C., and Paton, J. F. (2011). "The nucleus of the solitary tract: processing information from viscerosensory afferents," in Central Regulation of Autonomic Functions, eds I. J. Llewellyn-Smith and A. J. Verberne (London: Oxford), 23-46.
21. Andresen, M. C., and Peters, J. H. (2008). Comparison of baroreceptive to other afferent synaptic transmission to the solitary tract nucleus. Am. J. Physiol. Heart Circ. Physiol. 295, H2032-H2042.
22. Andresen, M. C., and Yang, M. (1990). Non-NMDA receptors mediate sensory afferent synaptic transmission in medial nucleus tractus solitarius. Am. J. Physiol. 259, H1307-H1311.
23. Andresen, M. C., and Yang, M. (1995). Dynamics of sensory afferent synaptic transmission in aortic baroreceptor regions of nucleus tractus solitarius. J. Neurophysiol. 74, 1518-1528.
24. Appleyard, S. M., Bailey, T. W., Doyle, M. W., Jin, Y.-H., Smart, J. L., Low, M. J., et al. (2005). Proopiomelanocortin neurons in nucleus tractus solitarius are activated by visceral afferents: regulation by cholecystokinin and opioids. J. Neurosci. 25, 3578-3585.
25. Appleyard, S. M., Marks, D., Kobayashi, K., Okano, H., Low, M. J., and Andresen, M. C. (2007). Visceral afferents directly activate catecholamine neurons in the solitary tract nucleus. J. Neurosci. 27, 13292-13302.
26. Austgen, J. R., Fong, A. Y., Foley, C. M., Mueller, P. J., Kline, D. D., Heesch, C. M., et al. (2009). Expression of Group I metabotropic glutamate receptors on phenotypically different cells within the nucleus of the solitary tract in the rat. Neuroscience 159, 701-716.
27. Aylwin, M. L., Horowitz, J. M., and Bonham, A. C. (1997). NMDA receptors contribute to primary visceral afferent transmission in the nucleus of the solitary tract. J. Neurophysiol. 77, 2539-2548.
28. Babic, T., Townsend, R. L., Patterson, L. M., Sutton, G. M., Zheng, H., and Berthoud, H. R. (2009). Phenotype of neurons in the nucleus of the solitary tract that express CCK-induced activation of the ERK signaling pathway. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R845-R854.
29. Bailey, T. W., Appleyard, S. M., Jin, Y. H., and Andresen, M. C. (2008). Organization and properties of GABAergic neurons in solitary tract nucleus (NTS). J. Neurophysiol. 99, 1712-1722.
30. Bailey, T. W., Hermes, S. M., Aicher, S. A., and Andresen, M. C. (2007). Target-specific, dynamic pathway tuning by A-type potassium channels in solitary tract nucleus: cranial visceral afferent pathways to caudal ventrolateral medulla or paraventricular hypothalamus. J. Physiol. 582, 613-628.
31. Bailey, T. W., Hermes, S. M., Andresen, M. C., and Aicher, S. A. (2006a). Cranial visceral afferent pathways through the nucleus of the solitary tract to caudal ventrolateral medulla or paraventricular hypothalamus: target-specific synaptic reliability and convergence patterns. J. Neurosci. 26, 11893-11902.
32. Bailey, T. W., Jin, Y.-H., Doyle, M. W., Smith, S. M., and Andresen, M. C. (2006b). Vasopressin inhibits glutamate release via two distinct modes in the brainstem. J. Neurosci. 26, 6131-6142.
33. Balkowiec, A., Kunze, D. L., and Katz, D. M. (2000). Brain-derived neurotrophic factor acutely inhibits AMPA-mediated currents in developing sensory relay neurons. J. Neurosci. 20, 1904-1911.
34. Baptista, V., Browning, K. N., and Travagli, R. A. (2007). Effects of cholecystokinin-8s in the nucleus tractus solitarius of vagally deafferented rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1092-R1100.
35. Baptista, V., Ogawa, W. N., Aguiar, J. F., and Varanda, W. A. (2005a). Electrophysiological evidence for the presence of NR2C subunits of N-methyl-D-aspartate receptors in rat neurons of the nucleus tractus solitarius. Braz. J. Med. Biol. Res. 38, 105-110.
36. Baptista, V., Zheng, Z. L., Coleman, F. H., Rogers, R. C., and Travagli, R. A. (2005b). Cholecystokinin octapeptide increases spontaneous glutamatergic synaptic transmission to neurons of the nucleus tractus solitarius centralis. J. Neurophysiol. 94, 2763-2771.
37. Barnes, K. L., DeWeese, D. M., and Andresen, M. C. (2003). Angiotensin potentiates excitatory synaptic transmission to medial solitary tract nucleus neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R1340-R1353.
38. Baude, A., Strube, C., Tell, F., and Kessler, J. P. (2009). Glutamatergic neurotransmission in the nucleus tractus solitarii: structural and functional characteristics. J. Chem. Neuroanat. 38, 145-153.
39. Benarroch, E. E. (2005). Paraventricular nucleus, stress response, and cardiovascular disease. Clin. Auton. Res. 15, 254-263.
40. Binzen, U., Greffrath, W., Hennessy, S., Bausen, M., Saaler-Reinhardt, S., and Treede, R. D. (2006). Co-expression of the voltage-gated potassium channel Kv1.4 with transient receptor potential channels (TRPV1 and TRPV2) and the cannabinoid receptor CB1 in rat dorsal root ganglion neurons. Neuroscience 142, 527-539.
41. Broadwell, R. D., and Sofroniew, M. V. (1993). Serum proteins bypass the blood-brain barriers for extracellular entry to the central nervous system. Exp. Neurol. 120, 245-263.
42. Browning, K. N., and Travagli, R. A. (2007). Functional organization of presynaptic metabotropic glutamate receptors in vagal brainstem circuits. J. Neurosci. 27, 8979-8988.
43. Browning, K. N., and Travagli, R. A. (2010). Plasticity of vagal brainstem circuits in the control of gastric function. Neurogastroenterol. Motil. 22, 1154-1163.
44. Browning, K. N., Zheng, Z., Gettys, T. W., and Travagli, R. A. (2006). Vagal afferent control of opioidergic effects in rat brainstem circuits. J. Physiol. 575, 761-776.
45. Brozoski, D. T., Dean, C., Hopp, F. A., Hillard, C. J., and Seagard, J. L. (2009). Differential endocannabinoid regulation of baroreflex-evoked sympathoinhibition in normotensive versus hypertensive rats. Auton. Neurosci. 150, 82-93.
46. Brozoski, D. T., Dean, C., Hopp, F. A., and Seagard, J. L. (2005). Uptake blockade of endocannabinoids in the NTS modulates baroreflex-evoked sympathoinhibition. Brain Res. 1059, 197-202.
47. Buczynski, M. W., and Parsons, L. H. (2010). Quantification of brain endocannabinoid levels: methods, interpretations and pitfalls. Br. J. Pharmacol. 160, 423-442.
48. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D. (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824.
49. Cavalleri, M. T., Burgi, K., Cruz, J. S., Jordao, M. T., Ceroni, A., and Michelini, L. C. (2011). Afferent signaling drives oxytocinergic preautonomic neurons and mediates training-induced plasticity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R958-R966.
50. Chae, C. U., Lee, R. T., Rifai, N., and Ridker, P. M. (2001). Blood pressure and inflammation in apparently healthy men. Hypertension 38, 399-403.
51. Chan, R. K., and Sawchenko, P. E. (1994). Spatially and temporally differentiated patterns of c-fos expression in brainstem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J. Comp. Neurol. 348, 433-460.
52. Chan, R. K. W., and Sawchenko, P. E. (1998). Organization and transmitter specificity of medullary neurons activated by sustained hypertension: implications for understanding baroreceptor reflex circuitry. J. Neurosci. 18, 371-387.
53. Chaudhri, O. B., Salem, V., Murphy, K. G., and Bloom, S. R. (2008). Gastrointestinal satiety signals. Annu. Rev. Physiol. 70, 239-255.
54. Chen, C. Y., and Bonham, A. C. (2005). Glutamate suppresses GABA release via presynaptic metabotropic glutamate receptors at baroreceptor neurones in rats. J. Physiol. 562, 535-551.
55. Chen, C. Y., Bonham, A. C., Dean, C., Hopp, F. A., Hillard, C. J., and Seagard, J. L. (2010). Retrograde release of endocannabinoids inhibits presynaptic GABA release to second-order baroreceptive neurons in NTS. Auton. Neurosci. 158, 44-50.
56. Chen, C. Y., Ling, Eh, E. H., Horowitz, J. M., and Bonham, A. C. (2002). Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats. J. Physiol. 538, 773-786.
57. Chen, J., Paudel, K. S., Derbenev, A. V., Smith, B. N., and Stinchcomb, A. L. (2009). Simultaneous quantification of anandamide and other endocannabinoids in dorsal vagal complex of rat brainstem by LC-MS. Chromatographia 69, 1-7.
58. Chung, C., and Kavalali, E. T. (2006). Seeking a function for spontaneous neurotransmission. Nat. Neurosci. 9, 989-990.
59. Ciriello, J., and Calaresu, F. R. (1981). Projections from buffer nerves to the nucleus of the solitary tract: an anatomical and electrophysiological study in the cat. J. Auton. Nerv. Syst. 3, 299-310.
60. Clement, K., Vega, N., Laville, M., Pelloux, V., Guy-Grand, B., Basdevant, A., et al. (2002). Adipose tissue gene expression in patients with a loss of function mutation in the leptin receptor. Int. J. Obes. Relat. Metab. Disord. 26, 1533-1538.
61. Cone, R. D. (2005). Anatomy and regulation of the central melanocortin system. Nat. Neurosci. 8, 571-578.
62. Conn, P. J. (2003). Physiological roles and therapeutic potential of metabotropic glutamate receptors. Ann. N. Y. Acad. Sci. 1003, 12-21.
63. Corbett, E. K., Sinfield, J. K., McWilliam, P. N., Deuchars, J., and Batten, T. F. (2005). Differential expression of vesicular glutamate transporters by vagal afferent terminals in rat nucleus of the solitary tract: projections from the heart preferentially express vesicular glutamate transporter 1. Neuroscience 135, 133-145.
64. Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655-666.
65. Cui, R. J., Li, X., and Appleyard, S. M. (2011). Ghrelin inhibits visceral afferent activation of catecholamine neurons in the solitary tract nucleus. J. Neurosci. 31, 3484-3492.
66. Cui, R. J., Roberts, B. L., Zhao, H., Andresen, M. C., and Appleyard, S. M. (2012a). Opioids inhibit visceral afferent activation of catecholamine neurons in the solitary tract nucleus. Neuroscience 222, 181-190.
67. Cui, R. J., Roberts, B. L., Zhao, H., Zhu, M., and Appleyard, S. M. (2012b). Serotonin activates catecholamine neurons in the solitary tract nucleus by increasing spontaneous glutamate inputs. J. Neurosci. 32, 16530-16538.
68. Curran, A. K., Xia, L., Leiter, J. C., and Bartlett, D. Jr. (2005). Elevated body temperature enhances the laryngeal chemoreflex in decerebrate piglets. J. Appl. Physiol. 98, 780-786.
69. Dahlstrom, A., and Fuxe, K. (1964). Evidence for the existence of monoamine-containing neurons in the central nervous system I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand. 62, 1-79.
70. Dallman, M. F. (2010). Stress-induced obesity and the emotional nervous system. Trends Endocrinol. Metab. 21, 159-165.
71. Dashwood, M. R., Muddle, J. R., and Spyer, K. M. (1988). Opiate receptor subtypes in the nucleus tractus solitarii of the cat: the effect of vagal section. Eur. J. Pharmacol. 155, 85-92.
72. Davies, R. O., Kubin, L., and Pack, A. I. (1987). Pulmonary stretch receptor relay neurones of the cat: location and contralateral medullary projections. J. Physiol. 383, 571-585.
73. Derbenev, A. V., Stuart, T. C., and Smith, B. N. (2004). Cannabinoids suppress synaptic input to neurones of the rat dorsal motor nucleus of the vagus nerve. J. Physiol. 559, 923-938.
74. Deuchars, J., Li, Y. W., Kasparov, S., and Paton, J. F. R. (2000). Morphological and electrophysiological properties of neurones in the dorsal vagal complex of the rat activated by arterial baroreceptors. J. Comp. Neurol. 417, 233-249.
75. DiPatrizio, N. V., and Piomelli, D. (2012). The thrifty lipids: endocannabinoids and the neural control of energy conservation. Trends Neurosci. 35, 403-411.
76. Donoghue, S., Felder, R. B., Gilbey, M. P., Jordan, D., and Spyer, K. M. (1985). Post-synaptic activity evoked in the nucleus tractus solitarius by carotid sinus and aortic nerve afferents in the cat. J. Physiol. 360, 261-273.
77. Donoghue, S., Fox, R. E., Kidd, C., and Koley, B. N. (1981a). The distribution in the cat brain stem of neurones activated by vagal non-myelinated fibres from the heart and lungs. Q. J. Exp. Physiol. Cogn. Med. Sci. 66, 391-404.
78. Donoghue, S., Fox, R. E., Kidd, C., and McWilliam, P. N. (1981b). The terminations and secondary projections of myelinated and non-myelinated fibres of the aortic nerve in the cat. Q. J. Exp. Physiol. Cogn. Med. Sci. 66, 405-422.
79. Doucet, E., Miquel, M. C., Nosjean, A., Verge, D., Hamon, M., and Emerit, M. B. (2000). Immunolabeling of the rat central nervous system with antibodies partially selective of the short form of the 5-HT3 receptor. Neuroscience 95, 881-892.
80. Doyle, M. W., and Andresen, M. C. (2001). Reliability of monosynaptic transmission in brain stem neurons in vitro. J. Neurophysiol. 85, 2213-2223.
81. Doyle, M. W., Bailey, T. W., Jin, Y.-H., and Andresen, M. C. (2002). Vanilloid receptors presynaptically modulate visceral afferent synaptic transmission in nucleus tractus solitarius. J. Neurosci. 22, 8222-8229.
82. Drewe, J. A., Miles, R., and Kunze, D. L. (1990). Excitatory amino acid receptors of guinea pig medial nucleus tractus solitarius neurons. Am. J. Physiol. 259, H1389-H1395.
83. Ellacott, K. L., and Cone, R. D. (2004). The central melanocortin system and the integration of short- and long-term regulators of energy homeostasis. Recent Prog. Horm. Res. 59, 395-408.
84. Ezure, K., and Tanaka, I. (1996). Pump neurons of the nucleus of the solitary tract project widely to the medulla. Neurosci. Lett. 215, 123-126.
85. Fawley, J. A., Peters, J. H., and Andresen, M. C. (2011). GABAB-mediated inhibition of multiple modes of glutamate release in the nucleus of the solitary tract. J. Neurophysiol. 106, 1833-1840.
86. Fernandes, L. G., Jin, Y. H., and Andresen, M. C. (2011). Heterosynaptic crosstalk: GABA-glutamate metabotropic receptors interactively control glutamate release in solitary tract nucleus. Neuroscience 174, 1-9.
87. Foley, C. M., Vogl, H. W., Mueller, P. J., Hay, M., and Hasser, E. M. (1999). Cardiovascular response to group I metabotropic glutamate receptor activation in NTS. Am. J. Physiol. 276, R1469-R1478.
88. Fong, A. Y., Stornetta, R. L., Foley, C. M., and Potts, J. T. (2005). Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J. Comp. Neurol. 493, 274-290.
89. Foreman, R. D. (1999). Mechanisms of cardiac pain. Annu. Rev. Physiol. 61, 143-167.
90. Foreman, R. D. (2000). Integration of viscerosomatic sensory input at the spinal level. Prog. Brain Res. 122, 209-221.
91. Gamboa-Esteves, F. O., Tavares, I., Almeida, A., Batten, T. F., McWilliam, P. N., and Lima, D. (2001). Projection sites of superficial and deep spinal dorsal horn cells in the nucleus tractus solitarii of the rat. Brain Res. 921, 195-205.
92. Geerling, J. C., Shin, J. W., Chimenti, P. C., and Loewy, A. D. (2010). Paraventricular hypothalamic nucleus: axonal projections to the brainstem. J. Comp. Neurol. 518, 1460-1499.
93. Geraghty, D. P., and Mazzone, S. B. (2002). Respiratory actions of vanilloid receptor agonists in the nucleus of the solitary tract: comparison of resiniferatoxin with non-pungent agents and anandamide. Br. J. Pharmacol. 137, 919-927.
94. Glatzer, N. R., Derbenev, A. V., Banfield, B. W., and Smith, B. N. (2007). Endomorphin-1 modulates intrinsic inhibition in the dorsal vagal complex. J. Neurophysiol. 98, 1591-1599.
95. Glaum, S. R., Brooks, P. A., Spyer, K. M., and Miller, R. J. (1992). 5-Hydroxytryptamine-3 receptors modulate synaptic activity in the rat nucleus tractus solitarius in vitro. Brain Res. 589, 62-68.
96. Glaum, S. R., and Miller, R. J. (1993). Metabotropic glutamate receptors depress afferent excitatory transmission in the rat nucleus tractus solitarii. J. Neurophysiol. 70, 2669-2672.
97. Grill, H. J. (2010). Leptin and the systems neuroscience of meal size control. Front. Neuroendocrinol. 31, 61-78.
98. Grill, H. J., and Hayes, M. R. (2012). Hindbrain neurons as an essential hub in the neuroanatomically distributed control of energy balance. Cell Metab. 16, 296-309.
99. Gross, P. M., Wall, K. M., Pang, J. J., Shaver, S. W., and Wainman, D. S. (1990). Microvascular specializations promoting rapid interstitial solute dispersion in nucleus tractus solitarius. Am. J. Physiol. 259, R1131-R1138.
100. Gross, P. M., Wall, K. M., Wainman, D. S., and Shaver, S. W. (1991). Subregional topography of capillaries in the dorsal vagal complex of rats: II. Physiological properties. J. Comp. Neurol. 306, 83-94.
101. Haxhiu, M. A., and Loewy, A. D. (1996). Central connections of the motor and sensory vagal systems innervating the trachea. J. Auton. Nerv. Syst. 57, 49-56.
102. Hay, M., McKenzie, H., Lindsley, K., Dietz, N., Bradley, S. R., Conn, P. J., et al. (1999). Heterogeneity of metabotropic glutamate receptors in autonomic cell groups of the medulla oblongata of the rat. J. Comp. Neurol. 403, 486-501.
103. Heifets, B. D., and Castillo, P. E. (2009). Endocannabinoid signaling and long-term synaptic plasticity. Annu. Rev. Physiol 71, 283-306.
104. Herbert, H., Moga, M. M., and Saper, C. B. (1990). Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol. 293, 540-580.
105. Herbert, H., and Saper, C. B. (1990). Cholecystokinin-, galanin-, and corticotropin-releasing factor-like immunoreactive projections from the nucleus of the solitary tract to the parabrachial nucleus in the rat. J. Comp. Neurol. 293, 581-598.
106. Hermes, S. M., Mitchell, J. L., and Aicher, S. A. (2006). Most neurons in the nucleus tractus solitarii do not send collateral projections to multiple autonomic targets in the rat brain. Exp. Neurol. 198, 539-551.
107. Hermes, S. M., Mitchell, J. L., Silverman, M. B., Lynch, P. J., McKee, B. L., Bailey, T. W., et al. (2008). Sustained hypertension increases the density of AMPA receptor subunit, GluR1, in baroreceptive regions of the nucleus tractus solitarii of the rat. Brain Res. 1187, 125-136.
108. Higa-Taniguchi, K. T., Felix, J. V., and Michelini, L. C. (2009). Brainstem oxytocinergic modulation of heart rate control in rats: effects of hypertension and exercise training. Exp. Physiol 94, 1103-1113.
109. Hoang, C. J., and Hay, M. (2001). Expression of metabotropic glutamate receptors in nodose ganglia and the nucleus of the solitary tract. Am. J. Physiol. Heart Circ. Physiol. 281, H457-H462.
110. Hollis, J. H., Lightman, S. L., and Lowry, C. A. (2004). Integration of systemic and visceral sensory information by medullary catecholaminergic systems during peripheral inflammation. Ann. N. Y. Acad. Sci. 1018, 71-75.
111. Holzer, P. (2004). TRPV1 and the gut: from a tasty receptor for a painful vanilloid to a key player in hyperalgesia. Eur. J. Pharmacol. 500, 231-241.
112. Huang, J., Hara, Y., Anrather, J., Speth, R. C., Iadecola, C., and Pickel, V. M. (2003). Angiotensin II subtype 1A (AT1A) receptors in the rat sensory vagal complex: subcellular localization and association with endogenous angiotensin. Neuroscience 122, 21-36.
113. Huang, S. M., Bisogno, T., Trevisani, M., Al Hayani, A., De Petrocellis, L., Fezza, F., et al. (2002). Di Marzo, V. An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc. Natl. Acad. Sci. U.S.A 99, 8400-8405.
114. Izzo, P. N., Sykes, R. M., and Spyer, K. M. (1992). Gamma-aminobutyric acid immunoreactive structures in the nucleus tractus solitarius: a light and electron microscopic study. Brain Res. 591, 69-78.
115. Jackson, K., Silva, H. M., Zhang, W., Michelini, L. C., and Stern, J. E. (2005). Exercise training differentially affects intrinsic excitability of autonomic and neuroendocrine neurons in the hypothalamic paraventricular nucleus. J. Neurophysiol. 94, 3211-3220.
116. Jin, Y.-H., Bailey, T. W., and Andresen, M. C. (2004a). Cranial afferent glutamate heterosynaptically modulates GABA release onto second order neurons via distinctly segregated mGluRs. J. Neurosci. 24, 9332-9340.
117. Jin, Y.-H., Bailey, T. W., Li, B. Y., Schild, J. H., and Andresen, M. C. (2004b). Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals. J. Neurosci. 24, 4709-4717.
118. Jin, Y.-H., Bailey, T. W., Doyle, M. W., Li, B. Y., Chang, K. S. K., Schild, J. H., et al. (2003). Ketamine differentially blocks sensory afferent synaptic transmission in medial nucleus tractus solitarius (mNTS). Anesthesiology 98, 121-132.
119. Jin, Y. H., Cahill, E. A., Fernandes, L. G., Wang, X., Chen, W., Smith, S. M., et al. (2010). Optical tracking of phenotypically diverse individual synapses on solitary tract nucleus neurons. Brain Res. 1312, 54-66.
120. Jordan, D. (2005). Vagal control of the heart: central serotonergic (5-HT) mechanisms. Exp. Physiol. 90, 175-181.
121. Julius, D., and Basbaum, A. I. (2001). Molecular mechanisms of nociception. Nature 413, 203-210.
122. Kalia, M., and Mesulam, M. M. (1980). Brain stem projections of sensory and motor components of the vagus complex in the cat: I. The cervical vagus and nodose ganglion. J. Comp. Neurol. 193, 435-465.
123. Kalia, M., and Sullivan, J. M. (1982). Brainstem projections of sensory and motor components of the vagus nerve in the rat. J. Comp. Neurol. 211, 248-264.
124. Katagiri, H., Yamada, T., and Oka, Y. (2007). Adiposity and cardiovascular disorders: disturbance of the regulatory system consisting of humoral and neuronal signals. Circ. Res. 101, 27-39.
125. Katona, I., and Freund, T. F. (2012). Multiple functions of endocannabinoid signaling in the brain. Annu. Rev. Neurosci. 35, 529-558.
126. Katz, B. (1971). Quantal mechanism of neural transmitter release. Science 173, 123-126.
127. Kavalali, E. T., Chung, C., Khvotchev, M., Leitz, J., Nosyreva, E., Raingo, J., et al. (2011). Spontaneous neurotransmission: an independent pathway for neuronal signaling? Physiology (Bethesda) 26, 45-53.
128. Kenny, P. J. (2011). Common cellular and molecular mechanisms in obesity and drug addiction. Nat. Rev. Neurosci. 12, 638-651.
129. Kline, D. D., Ramirez-Navarro, A., and Kunze, D. L. (2007). Adaptive depression in synaptic transmission in the nucleus of the solitary tract after in vivo chronic intermittent hypoxia: evidence for homeostatic plasticity. J. Neurosci. 27, 4663-4673.
130. Kline, D. D., Takacs, K. N., Ficker, E., and Kunze, D. L. (2002). Dopamine modulates synaptic transmission in the nucleus of the solitary tract. J. Neurophysiol. 88, 2736-2744.
131. Korner, P. I. (2007). Essential Hypertension, and Its Causes - Neural, and Non-Neural Mechanisms. Oxford: Oxford University Press.
132. Kubin, L., Alheid, G. F., Zuperku, E. J., and McCrimmon, D. R. (2006). Central pathways of pulmonary and lower airway vagal afferents. J. Appl. Physiol. 101, 618-627.
133. Kubin, L., and Davies, R. O. (1995). "Central pathways of pulmonary, and airway vagal afferents," in Regulation of Breathing, eds J. A. Dempsey and A. I. Pack (New York: Marcel Dekker), 219-284.
134. Kubin, L., Kimura, H., and Davies, R. O. (1991). The medullary projections of afferent bronchopulmonary C fibres in the cat as shown by antidromic mapping. J. Physiol. 435, 207-228.
135. Laaris, N., and Weinreich, D. (2007). Prostaglandin E2 depresses solitary tract-mediated synaptic transmission in the nucleus tractus solitarius. Neuroscience 146, 792-801.
136. Larsen, P. J., Tang-Christensen, M., Holst, J. J., and Orskov, C. (1997). Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem. Neuroscience 77, 257-270.
137. Lawrence, A. J., and Jarrott, B. (1996). Neurochemical modulation of cardiovascular control in the nucleus tractus solitarius. Prog. Neurobiol. 48, 21-53.
138. Li, B. Y., Feng, B., Tsu, H. Y., and Schild, J. H. (2007). Unmyelinated visceral afferents exhibit frequency dependent action potential broadening while myelinated visceral afferents do not. Neurosci. Lett. 421, 62-66.
139. Li, B. Y., Glazebrook, P., Kunze, D. L., and Schild, J. H. (2011). KCa1.1 channel contributes to cell excitability in unmyelinated but not myelinated rat vagal afferents. Am. J. Physiol. Cell Physiol. 300, C1393-C1403.
140. Li, B. Y., and Schild, J. H. (2007). Electrophysiological and pharmacological validation of vagal afferent fiber type of neurons enzymatically isolated from rat nodose ganglia. J. Neurosci. Methods 164, 75-85.
141. Liu, Z., Chen, C. Y., and Bonham, A. C. (1998). Metabotropic glutamate receptors depress vagal and aortic baroreceptor signal transmission in the NTS. Am. J. Physiol. 275, H1682-H1694.
142. Llewellyn-Smith, I. J., Reimann, F., Gribble, F. M., and Trapp, S. (2011). Preproglucagon neurons project widely to autonomic control areas in the mouse brain. Neuroscience 180, 111-121.
143. Loewy, A. D. (1990). "Central autonomic pathways," in Central Regulation of Autonomic Functions, eds A. D. Loewy and K. M. Spyer (New York: Oxford University Press), 88-103.
144. Loewy, A. D., and Burton, H. (1978). Nuclei of the solitary tract: efferent projections to the lower brain stem and spinal cord of the cat. J. Comp. Neurol. 181, 421-449.
145. Mascarucci, P., Perego, C., Terrazzino, S., and De Simoni, M. G. (1998). Glutamate release in the nucleus tractus solitarius induced by peripheral lipopolysaccharide and interleukin-1β. Neuroscience 86, 1285-1290.
146. Mazda, T., Yamamoto, H., Fujimura, M., and Fujimiya, M. (2004). Gastric distension-induced release of 5-HT stimulates c-fos expression in specific brain nuclei via 5-HT3 receptors in conscious rats. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G228-G235.
147. McDougall, S. J., and Andresen, M. C. (2012). Low fidelity GABA transmission within a dense excitatory network of the solitary tract nucleus. J. Physiol. (Lond.) 590, 5677-5689.
148. McDougall, S. J., and Andresen, M. C. (2013). Independent transmission of convergent visceral primary afferents in the solitary tract nucleus. J. Neurophysiol. (in press).
149. McDougall, S. J., Peters, J. H., and Andresen, M. C. (2009). Convergence of cranial visceral afferents within the solitary tract nucleus. J. Neurosci. 29, 12886-12895.
150. Mendelowitz, D., Yang, M., Andresen, M. C., and Kunze, D. L. (1992). Localization and retention in vitro of fluorescently labeled aortic baroreceptor terminals on neurons from the nucleus tractus solitarius. Brain Res. 581, 339-343.
151. Michelini, L. C. (2007). Differential effects of vasopressinergic and oxytocinergic pre-autonomic neurons on circulatory control: reflex mechanisms and changes during exercise. Clin. Exp. Pharmacol. Physiol. 34, 369-376.
152. Michelini, L. C., and Morris, M. (1999). Endogenous vasopressin modulates the cardiovascular responses to exercise. Ann. N. Y. Acad. Sci. 897, 198-211.
153. Michelini, L. C., and Stern, J. E. (2009). Exercise-induced neuronal plasticity in central autonomic networks: role in cardiovascular control. Exp. Physiol. 94, 947-960.
154. Mifflin, S. W. (1996). Convergent carotid sinus nerve and superior laryngeal nerve afferent inputs to neurons in the NTS. Am. J. Physiol. Regul. Integr. Comp. Physiol. 271, R870-R880.
155. Moechars, D., Weston, M. C., Leo, S., Callaerts-Vegh, Z., Goris, I., Daneels, G., et al. (2006). Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J. Neurosci. 26, 12055-12066.
156. Motter, A. L., and Ahern, G. P. (2008). TRPV1-null mice are protected from diet-induced obesity. FEBS Lett. 582, 2257-2262.
157. Mountjoy, K. G. (2010). Functions for pro-opiomelanocortin-derived peptides in obesity and diabetes. Biochem. J. 428, 305-324.
158. Nakamura, K., and Morrison, S. F. (2008). A thermosensory pathway that controls body temperature. Nat. Neurosci. 11, 62-71.
159. Nirenberg, M. J., Liu, Y., Peter, D., Edwards, R. H., and Pickel, V. M. (1995). The vesicular monoamine transporter 2 is present in small synaptic vesicles and preferentially localizes to large dense core vesicles in rat solitary tract nuclei. Proc. Natl. Acad. Sci. U.S.A. 92, 8773-8777.
160. Paton, J. F. R. (1998). Pattern of cardiorespiratory afferent convergence to solitary tract neurons driven by pulmonary vagal C-fiber stimulation in the mouse. J. Neurophysiol. 79, 2365-2373.
161. Paton, J. F. R., Li, Y. W., Deuchars, J., and Kasparov, S. (2000). Properties of solitary tract neurons receiving inputs from the sub- diaphragmatic vagus nerve. Neuroscience 95, 141-153.
162. Perez-Tilve, D., Stern, J. E., and Tschop, M. (2006). The brain and the metabolic syndrome: not a wireless connection. Endocrinology 147, 1136-1139.
163. Peters, J. H. (2011). TRPV1 independent mechanisms of spontaneous, and asynchronous glutamate release at synapses between primary afferents, and second-order neurons in the nucleus of the solitary tract. Soc. Neurosci. Abstr. 446, 18.
164. Peters, J. H., McDougall, S. J., Fawley, J. A., and Andresen, M. C. (2011). TRPV1 marks synaptic segregation of multiple convergent afferents at the rat medial solitary tract nucleus. PLoS ONE 6:e25015. doi:10.1371/journal.pone.0025015
165. Peters, J. H., McDougall, S. J., Fawley, J. A., Smith, S. M., and Andresen, M. C. (2010). Primary afferent activation of thermosensitive TRPV1 triggers asynchronous glutamate release at central neurons. Neuron 65, 657-669.
166. Peters, J. H., McDougall, S. J., Kellett, D. O., Jordan, D., Llewellyn-Smith, I. J., and Andresen, M. C. (2008). Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. J. Neurosci. 28, 11731-11740.
167. Pickel, V. M., Chan, J., and Milner, T. A. (1989). Ultrastructural basis for interactions between central opioids and catecholamines. II. Nuclei of the solitary tracts. J. Neurosci. 9, 2519-2535.
168. Pingle, S. C., Matta, J. A., and Ahern, G. P. (2007). "Capsaicin receptor: TRPV1 a promiscuous TRP channel," in Transient Receptor Potential (TRP) Channels, eds V. Flockerzi and B. Nilius (Berlin: Springer), 155-171.
169. Price, T. J., Patwardhan, A., Akopian, A. N., Hargreaves, K. M., and Flores, C. M. (2004). Modulation of trigeminal sensory neuron activity by the dual cannabinoid-vanilloid agonists anandamide, N-arachidonoyl-dopamine and arachidonyl-2-chloroethylamide. Br. J. Pharmacol. 141, 1118-1130.
170. Ramirez, D. M., and Kavalali, E. T. (2011). Differential regulation of spontaneous and evoked neurotransmitter release at central synapses. Curr. Opin. Neurobiol. 21, 275-282.
171. Riche, D., De Pommery, J., and Menetrey, D. (1990). Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J. Comp. Neurol. 293, 399-424.
172. Rinaman, L. (2007). Visceral sensory inputs to the endocrine hypothalamus. Front. Neuroendocrinol. 28, 50-60.
173. Rinaman, L. (2010). Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure. Brain Res. 1350, 18-34.
174. Rinaman, L., Card, J. P., Schwaber, J. S., and Miselis, R. R. (1989). Ultrastructural demonstration of a gastric monosynaptic vagal circuit in the nucleus of the solitary tract in rat. J. Neurosci. 9, 1985-1996.
175. Ritter, R. C. (2004). Gastrointestinal mechanisms of satiation for food. Physiol. Behav. 81, 249-273.
176. Rother, E., Konner, A. C., and Bruning, J. C. (2008). Neurocircuits integrating hormone and nutrient signaling in control of glucose metabolism. Am. J. Physiol. Endocrinol. Metab. 294, E810-E816.
177. Sabatini, B. L., and Regehr, W. G. (1999). Timing of synaptic transmission. Annu. Rev. Physiol. 61, 521-542.
178. Sant'Ambrogio, G. (1987). Nervous receptors of the tracheobronchial tree. Annu. Rev. Physiol. 49, 611-627.
179. Saper, C. B. (2002). The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu. Rev. Neurosci. 25, 433-469.
180. Scherer, T., and Buettner, C. (2009). The dysregulation of the endocannabinoid system in diabesity-a tricky problem. J. Mol. Med. 87, 663-668.
181. Schild, J. H., Clark, J. W., Canavier, C. C., Kunze, D. L., and Andresen, M. C. (1995). Afferent synaptic drive of rat medial nucleus tractus solitarius neurons: dynamic simulation of graded vesicular mobilization, release, and non-NMDA receptor kinetics. J. Neurophysiol. 74, 1529-1548.
182. Schild, J. H., Clark, J. W., Hay, M., Mendelowitz, D., Andresen, M. C., and Kunze, D. L. (1994). A- and C-type nodose sensory neurons: model interpretations of dynamic discharge characteristics. J. Neurophysiol. 71, 2338-2358.
183. Schild, J. H., and Kunze, D. L. (1997). Experimental and modeling study of Na+ current heterogeneity in rat nodose neurons and its impact on neuronal discharge. J. Neurophysiol. 78, 3198-3209.
184. Schild, J. H., and Kunze, D. L. (2012). Differential distribution of voltage-gated channels in myelinated and unmyelinated baroreceptor afferents. Auton. Neurosci. 172, 4-12.
185. Schwartz, M. W., Woods, S. C., Porte, D. Jr., Seeley, R. J., and Baskin, D. G. (2000). Central nervous system control of food intake. Nature 404, 661-671.
186. Seagard, J. L., Dean, C., and Hopp, F. A. (1999). Role of glutamate receptors in transmission of vagal cardiac input to neurones in the nucleus tractus solitarii in dogs. J. Physiol. 520, 243-253.
187. Seagard, J. L., Dean, C., Patel, S., Rademacher, D. J., Hopp, F. A., Schmeling, W. T., et al. (2004). Anandamide content and interaction of endocannabinoid/GABA modulatory effects in the NTS on baroreflex-evoked sympathoinhibition. Am. J. Physiol. Heart Circ. Physiol. 286, H992-H1000.
188. Seagard, J. L., Hopp, F. A., Hillard, C. J., and Dean, C. (2005). Effects of endocannabinoids on discharge of baroreceptive NTS neurons. Neurosci. Lett. 381, 334-339.
189. Sekizawa, S., and Bonham, A. C. (2006). Group I metabotropic glutamate receptors on second-order baroreceptor neurons are tonically activated and induce a Na+-Ca2+ exchange current. J. Neurophysiol. 95, 882-892.
190. Semyanov, A., Walker, M. C., Kullmann, D. M., and Silver, R. A. (2004). Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci. 27, 262-269.
191. Serrats, J., Schiltz, J. C., Garcia-Bueno, B., van Rooijen, N., Reyes, T. M., and Sawchenko, P. E. (2010). Dual roles for perivascular macrophages in immune-to-brain signaling. Neuron 65, 94-106.
192. Shoudai, K., Peters, J. H., McDougall, S. J., Fawley, J. A., and Andresen, M. C. (2010). Thermally active TRPV1 tonically drives central spontaneous glutamate release. J. Neurosci. 30, 14470-14475.
193. Silva-Carvalho, L., Paton, J. F. R., Rocha, I., Goldsmith, G. E., and Spyer, K. M. (1998). Convergence properties of solitary tract neurons responsive to cardiac receptor stimulation in the anesthetized cat. J. Neurophysiol. 79, 2374-2382.
194. Simpson, K., Parker, J., Plumer, J., and Bloom, S. (2012). CCK, PYY, and PP: the control of energy balance. Handb. Exp. Pharmacol. 209-230
195. Spiegelman, B. M., and Flier, J. S. (2001). Obesity and the regulation of energy balance. Cell 104, 531-543.
196. Spyer, K. M. (1990). "The central nervous organization of reflex circulatory control," in Central Regulation of Autonomic Functions, eds A. D. Loewy and K. M. Spyer (New York: Oxford University Press), 168-188.
197. Stern, J. E., Sonner, P. M., Son, S. J., Silva, F. C., Jackson, K., and Michelini, L. C. (2012). Exercise training normalizes an increased neuronal excitability of NTS-projecting neurons of the hypothalamic paraventricular nucleus in hypertensive rats. J. Neurophysiol. 107, 2912-2921.
198. Stornetta, R. L., and Guyenet, P. G. (1999). Distribution of glutamic acid decarboxylase mRNA-containing neurons in rat medulla projecting to thoracic spinal cord in relation to monoaminergic brainstem neurons. J. Comp. Neurol. 407, 367-380.
199. Stornetta, R. L., Sevigny, C. P., and Guyenet, P. G. (2002). Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J. Comp. Neurol. 444, 191-206.
200. Sumal, K. K., Blessing, W. W., Joh, T. H., Reis, D. J., and Pickel, V. M. (1983). Synaptic interaction of vagal afferents and catecholaminergic neurons in the rat nucleus tractus solitarius. Brain Res. 277, 31-40.
201. Szallasi, A., Cortright, D. N., Blum, C. A., and Eid, S. R. (2007). The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat. Rev. Drug Discov. 6, 357-372.
202. Takagishi, M., Waki, H., Bhuiyan, M. E., Gouraud, S. S., Kohsaka, A., Cui, H., et al. (2010). IL-6 microinjected in the nucleus tractus solitarii attenuates cardiac baroreceptor reflex function in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R183-R190.
203. Tognetto, M., Amadesi, S., Harrison, S., Creminon, C., Trevisani, M., Carreras, M., et al. (2001). Anandamide excites central terminals of dorsal root ganglion neurons via vanilloid receptor-1 activation. J. Neurosci. 21, 1104-1109.
204. Travagli, R. A., Hermann, G. E., Browning, K. N., and Rogers, R. C. (2006). Brainstem circuits regulating gastric function. Annu. Rev. Physiol. 68, 279-305.
205. Tsuji, F., Murai, M., Oki, K., Seki, I., Ueda, K., Inoue, H., et al. (2010). Transient receptor potential vanilloid 1 agonists as candidates for anti-inflammatory, and immunomodulatory agents. Eur. J. Pharmacol. 627, 332-339.
206. Ulrich-Lai, Y. M., and Herman, J. P. (2009). Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10, 397-409.
207. Velley, L., Milner, T. A., Chan, J., Morrison, S. F., and Pickel, V. M. (1991). Relationship of Met-enkephalin-like immunoreactivity to vagal afferents and motor dendrites in the nucleus of the solitary tract: a light and electron microscopic dual labeling study. Brain Res. 550, 298-312.
208. Waki, H., Gouraud, S. S., Maeda, M., and Paton, J. F. (2008). Specific inflammatory condition in nucleus tractus solitarii of the SHR: novel insight for neurogenic hypertension? Auton. Neurosci. 142, 25-31.
209. Wan, S., and Browning, K. N. (2008). Glucose increases synaptic transmission from vagal afferent central nerve terminals via modulation of 5-HT3 receptors. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G1050-G1057.
210. Wan, S., Browning, K. N., Coleman, F. H., Sutton, G., Zheng, H., Butler, A., et al. (2008). Presynaptic melanocortin-4 receptors on vagal afferent fibers modulate the excitability of rat nucleus tractus solitarius neurons. J. Neurosci. 28, 4957-4966.
211. Wan, S., Coleman, F. H., and Travagli, R. A. (2007). Glucagon-like peptide-1 excites pancreas-projecting preganglionic vagal motoneurons. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1474-G1482.
212. Wang, Y., and Wang, D. H. (2009). Aggravated renal inflammatory responses in TRPV1 gene knockout mice subjected to DOCA-salt hypertension. Am. J. Physiol. Renal Physiol. 297, F1550-F1559.
213. Weston, M., Wang, H., Stornetta, R. L., Sevigny, C. P., and Guyenet, P. G. (2003). Fos expression by glutamatergic neurons of the solitary tract nucleus after phenylephrine-induced hypertension in rats. J. Comp. Neurol. 460, 525-541.
214. Wong, G. Y., and Gavva, N. R. (2009). Therapeutic potential of vanilloid receptor TRPV1 agonists and antagonists as analgesics: recent advances and setbacks. Brain Res. Rev. 60, 267-277.
215. Xia, L., Bartlett, D. Jr., and Leiter, J. C. (2011). TRPV1 channels in the nucleus of the solitary tract mediate thermal prolongation of the LCR in decerebrate piglets. Respir. Physiol. Neurobiol. 176, 21-31.
216. Xia, L., Damon, T., Leiter, J. C., and Bartlett, D. Jr. (2008). Elevated body temperature exaggerates laryngeal chemoreflex apnea in decerebrate piglets. Adv. Exp. Med. Biol. 605, 249-254.
217. Xia, L., Damon, T. A., Leiter, J. C., and Bartlett, D. Jr. (2007). Focal warming in the nucleus of the solitary tract prolongs the laryngeal chemoreflex in decerebrate piglets. J. Appl. Physiol. 102, 54-62.
218. Xia, L., Leiter, J. C., and Bartlett, J. (2010). Gestational nicotine exposure exaggerates hyperthermic enhancement of laryngeal chemoreflex in rat pups. Respir. Physiol. Neurobiol. 171, 17-21.
219. Yamamoto, H., Lee, C. E., Marcus, J. N., Williams, T. D., Overton, J. M., Lopez, M. E., et al. (2002). Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. J. Clin. Invest. 110, 43-52.
220. Yang, H., and Chen, C. (2008). Cyclooxygenase-2 in synaptic signaling. Curr. Pharm. Des 14, 1443-1451.
221. Zhang, W., and Mifflin, S. W. (1995). Excitatory amino-acid receptors contribute to carotid sinus and vagus nerve evoked excitation of neurons in the nucleus of the tractus solitarius. J. Auton. Nerv. Syst. 55, 50-56.
222. Zhang, W., and Mifflin, S. W. (2007). Modulation of synaptic transmission to second-order peripheral chemoreceptor neurons in caudal nucleus tractus solitarius by {alpha}1-adrenoreceptors. J. Pharmacol. Exp. Ther. 320, 670-677.
223. Zhou, Y. H., Sun, L. H., Liu, Z. H., Bu, G., Pang, X. P., Sun, S. C., et al. (2010). Functional impact of the hyperpolarization-activated current on the excitability of myelinated A-type vagal afferent neurons in the rat. Clin. Exp. Pharmacol. Physiol. 37, 852-861.
224. Zhuo, H., Ichikawa, H., and Helke, C. J. (1997). Neurochemistry of the nodose ganglion. Prog. Neurobiol. 52, 79-107.