Angiotensin potentiates excitatory sensory synaptic transmission to medial solitary tract nucleus neurons

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 284, Issue 5 53-5, 2003, Pages

  Barnes, Karen L ^a   DeWeese, Dannette M ^b   Andresen, Michael C ^c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b PURDUE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Cardiovascular regulation; L glutamate; Substance P, non N methyl D aspartate receptor

Indexed keywords

ANGIOTENSIN; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SUBSTANCE P;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; CARDIOVASCULAR FUNCTION; EVOKED RESPONSE; HEART RATE; MALE; MEMBRANE DEPOLARIZATION; NERVE CELL; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESSORECEPTOR REFLEX; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SENSORY SYSTEM; SOLITARY TRACT NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 0037405846     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00505.2002     Document Type: Article

References (91)

1. Aguirre JA, Covenas R, Croix D, Alonso JR, Narvaez JA, Tramu G, and Gonzalez-Baron S. Immunocytochemical study of angiotensin-II fibres and cell bodies in the brainstem respiratory areas of the cat. Brain Res 489: 311-317, 1989.
2. Allen AM, Moeller I, Jenkins TA, Zhuo J, Aldred GP, Chai SY, and Mendelsohn FAO. Angiotensin receptors in the nervous system. Brain Res Bull 47: 17-28, 1998.
3. American Physiological Society. Guiding principles for research involving animals and human beings. Am J Physiol Regul Integr Comp Physiol 283: R281-R283, 2002.
4. Andresen MC and Kunze DL. Nucleus tractus solitarius - gateway to neural circulatory control. Annu Rev Physiol 56: 93-116, 1994.
5. Andresen MC and Yang M. Non-NMDA receptors mediate sensory afferent synaptic transmission in medial nucleus tractus solitarius. Am J Physiol Heart Circ Physiol 259: H1307-H1311, 1990.
6. Andresen MC and Yang M. Dynamics of sensory afferent synaptic transmission in aortic baroreceptor regions of nucleus tractus solitarius. J Neurophysiol 74: 1518-1528, 1995.
7. Appenrodt E and Brattström A. Effects of central angiotensin II and angiotensin III on baroreflex regulation. Neuropeptides 26: 175-180, 1994.
8. Aylwin ML, Horowitz JM, and Bonham AC. NMDA receptors contribute to primary afferent transmission in the nucleus of the solitary tract. J Neurophysiol 77: 2539-2548, 1997.
9. Bacal K and Kunze DL. Dual effects of angiotensin II on calcium currents in neonatal rat nodose neurons. J Neurosci 14: 7159-7167, 1994.
10. Barnes KL. Neuropeptides in the regulation of autonomic function by the dorsal medulla. In: Nucleus of the Solitary Tract, edited by Barraco IRA. Boca Raton, FL: CRC, 1993, p. 329-339.
11. Barnes KL and DeWeese DM. Angiotensin potentiates solitary tract afferent responses in medial nucleus tractus solitarii (mnTS) neurons responsive to glutamate but not to substance P. Soc Neurosci Abstr 22: 632, 1996.
12. Barnes KL, Diz DI, and Ferrario CM. Functional interactions between angiotensin II and substance P in the dorsal medulla. Hypertension 17: 1121-1126, 1991.
13. Barnes KL, Knowles WD, and Ferrario CM. Neuronal responses to angiotensin II in the in vitro slice from the canine medulla. Hypertension 11: 680-684, 1988.
14. Barnes KL, Knowles WD, and Ferrario CM. Angiotensin II and angiotensin-(1-7) excite neurons in the canine medulla in vitro. Brain Res Bull 24: 275-280, 1990.
15. Barnes KL, McQueeney AJ, Barrett WR, and Knowles WD. Morphology and projections of neurobiotin-labeled nucleus tractus solitarii neurons recorded in vitro. Brain Res Bull 34: 339-348, 1994.
16. Barnes KL, McQueeney AJ, and Ferrario CM. Receptor subtype that mediates the neuronal effects of angiotensin II in the rat dorsal medulla. Brain Res Bull 31: 195-200, 1993.
17. Boscan P, Allen AM, and Paton JFR. Baroreflex inhibition of cardiac sympathetic outflow is attenuated by angiotensin II in the nucleus of the solitary tract. Neuroscience 103: 153-160, 2001.
18. Bradley RM and Sweazey RD. Separation of neuron types in the gustatory zone of the nucleus tractus solitarii on the basis of intrinsic firing properties. J Neurophysiol 67: 1659-1668, 1992.
19. Brattström A, Sonntag M, Listing H, Miller R, and DeJong W. Neuropeptides within the nucleus tractus solitarii modulate the central cardiovascular control process. Prog Brain Res 91: 75-79, 1992.
20. Brooks PA, Glaum SR, Miller RJ, and Spyer KM. The actions of baclofen on neurones and synaptic transmission in the nucleus tractus solitarii of the rat in vitro. J Physiol 457: 115-129, 1992.
21. Casto R and Phillips MI. Angiotensin II attenuates barore-flexes at nucleus tractus solitarius of rats. Am J Physiol Regul Integr Comp Physiol 250: R193-R198, 1986.
22. Champagnat J, Denavit-Saubié M, Grant K, and Shen KF. Organization of synaptic transmission in the mammalian solitary complex, studied in vitro. J Physiol 381: 551-573, 1986.
23. Chan JYH, Barnes CD, and Chan SHH. Tonic enhancement of the sensitivity of baroreceptor reflex response by endogenous substance P in the rat. Regul Pept 29: 199-213, 1990.
24. Chen CY, Munch PA, Quail AW, and Bonham AC. Postexercise hypotension in conscious SHR is attenuated by blockade of substance P receptors in NTS. Am J Physiol Heart Circ Physiol 283: H1856-H1862, 2002.
25. Ciriello J. Brainstem projections of aortic baroreceptor afferent fibers in the rat. Neurosci Lett 36: 37-42, 1983.
26. Ciriello J, Hochstenbach SL, and Roder S. Central projections of baroreceptor and chemoreceptor afferent fibers in the rat. In: Nucleus of the Solitary Tract, edited by Barraco IRA. Boca Raton, FL: CRC, 1993, p. 35-50.
27. Cowan AR, Dean C, Bago M, and Seagard JL. Potentiation of non-N-methyl-D-aspartate receptor-induced changes in blood pressure by substance P in rats. Neurosci Lett 278: 161-164, 2000.
28. DeWeese DM and Barnes KL. Angiotensin receptors are presynaptic to glutamate-responsive medial nucleus tractus solitarii (mnTS) neurons with solitary tract (TS) inputs. Soc Neurosci Abstr 21: 642, 1995.
29. Diz DI, Barnes KL, and Ferrario CM. Hypotensive actions of microinjections of angiotensin II into the dorsal motor nucleus of the vagus. J Hypertens 2 Suppl 3: 53-56, 1984.
30. Diz DI, Barnes KL, and Ferrario CM. Contribution of the vagus nerve to angiotensin II binding in the canine medulla. Brain Res Bull 17: 497-505, 1986.
31. Diz DI, Block CH, Barnes KL, and Ferrario CM. Correlation between angiotensin II binding sites and substance P in the canine brain stem. J Hypertens 4 Suppl 6: S468-S471, 1986.
32. Diz DI, Fantz DL, Benter IF, and Bosch SM. Acute depressor actions of angiotensin II and the nucleus of the solitary tract are mediated by substance P. Am J Physiol Regul Integr Comp Physiol 273: R28-R34, 1997.
33. 1 receptor antagonist blocks angiotensin II responses in renin transgenic rat medulla oblongata. Hypertension 31: 473-479, 1998.
34. Doyle MW and Andresen MC. Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 85: 2213-2223, 2001.
35. Duan YF, Kopin IJ, and Goldstein DS. Stimulation of the paraventricular nucleus modulates firing of neurons in the nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 277: R403-R411, 1999.
36. Ferguson AV and Renaud LP. Systemic angiotensin acts at subfornical organ to facilitate activity of neurohypophysial neurons. Am J Physiol Regul Integr Comp Physiol 251: R712-R717, 1986.
37. Ferrario CM and Averill DB. Do primary dysfunctions in neural control of arterial pressure contribute to hypertension? Hypertension 18 Suppl I: I-38-I-51, 1991.
38. Ferrario CM, Ueno Y, Diz DI, and Barnes KL. The renin-angiotensin system: physiological actions on the central nervous system. In: Handbook of Hypertension, edited by Birkenhager WB and Reid JL. Amsterdam: Elsevier/North Holland Biomedical, 1986, p. 431-454.
39. Fortin G and Champagnat J. Spontaneous synaptic activities in rat nucleus tractus solitarius neurons in vitro: evidence for re-excitatory processing. Brain Res 630: 125-135, 1993.
40. Fortin G, Velluti JC, Denavit-Saubié M, and Champagnat J. Responses to repetitive afferent activity of rat solitary complex neurons isolated in brainstem slices. Neurosci Lett 147: 89-92, 1992.
41. Fow JE, Averill DB, and Barnes KL. Mechanisms of angiotensin-induced hypotension and bradycardia in the medial solitary tract nucleus. Am J Physiol Heart Circ Physiol 267: H259-H266, 1994.
42. Gatti PJ, Shirahata M, Johnson TA, and Massari VJ. Synaptic interactions of substance P immunoreactive nerve terminals in the baro- and chemoreceptor reflexes of the cat. Brain Res 693: 133-147, 1995.
43. Gieroba ZJ, Li YW, Wesselingh SL, and Blessing WW. Transneuronal labeling of neurons in rabbit brain after injection of herpes simplex virus type 1 into the aortic depressor nerve. Brain Res 558: 264-272, 1991.
44. Glaum SR and Miller RJ. Metabotropic glutamate receptors mediate excitatory transmission in the nucleus of the solitary tract. J Neurosci 12: 2251-2258, 1992.
45. Glaum SR and Miller RJ. Metabotropic glutamate receptors depress afferent excitatory transmission in the rat nucleus tractus solitarii. J Neurophysiol 70: 2669-2672, 1993.
46. Gordon FJ and Leone C. Non-NMDA receptors in the nucleus of the tractus solitarius play the predominant role in mediating aortic baroreceptor reflexes. Brain Res 568: 319-322, 1991.
47. Gutman MB, Ciriello J, and Mogenson GJ. Effects of plasma angiotensin II and hypernatremia on subfornical organ neurons. Am J Physiol Regul Integr Comp Physiol 254: R746-R754, 1988.
48. Haas HL, Felix D, and Davis MD. Angiotensin excites hippocampal pyramidal cells by two mechanisms. Cell Mol Neurobiol 2: 21-31, 1982.
49. Hall ME, Greer RA, and Stewart JM. Effects of L-glutamate, substance P and substance P-(1-7) on cardiovascular regulation in the nucleus tractus solitarius. Regul Pept 46: 102-109, 1993.
50. Healy DP, Rettig R, and Printz MP. Evidence of an endogenous ANG II system in the rat nucleus tractus solitarius. Clin Exp Hypertens 6: 1743-1747, 1984.
51. Hegarty AA, Hayward LF, and Felder RB. Influence of circulating angiotensin II and vasopressin on neurons of the nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 270: R675-R681, 1996.
52. Higgins GA, Hoffman GE, Wray S, and Schwaber JS. Distribution of neurotensin immunoreactivity within baroreceptive portions of the nucleus of the tractus solitarius and the dorsal vagal nucleus of the rat. J Comp Neurol 226: 155-164, 1984.
53. Kasparov S and Paton JFR. Differential effects of angiotensin II in the nucleus tractus solitarii of the rat - Plausible neuronal mechanisms. J Physiol 521: 227-238, 1999.
54. King MS and Bradley RM. Relationship between structure and function of neurons in the rat rostral nucleus tractus solitarii. J Comp Neurol 344: 50-64, 1994.
55. Kubo T and Kihara M. Blood pressure modulation by substance P in the rat nucleus tractus solitarius. Brain Res 413: 379-383, 1987.
56. Legendre P, Simonnet G, and Vincent JD. Electrophysiological effects of angiotensin II on cultured mouse spinal cord neurons. Brain Res 297: 287-296, 1984.
57. 2) receptor mRNAs in the adult rat brain: a functional neuroanatomical review. Front Neuroendocrinol 18: 383-439, 1997.
58. Li DP, Averill DB, and Pan HL. Differential roles of glutamate receptor subtypes within commissural NTS in cardiac-sympathetic reflex. Am J Physiol Regul Integr Comp Physiol 281: R935-R943, 2001.
59. Li Z and Ferguson AV. Angiotensin II responsiveness of rat paraventricular and subfornical organ neurons in vitro. Neuroscience 55: 197-207, 1993.
60. Loewy AD. Central autonomic pathways. In: Central Regulation of Autonomic Functions, edited by Loewy AD and Spyer KM. New York: Oxford University Press, 1990, p. 88-103.
61. Lohmeier TE. Neurohumoral regulation of arterial pressure in hemorrhage and heart failure. Am J Physiol Regul Integr Comp Physiol 283: R810-R814, 2002.
62. Lu WY and Bieger D. Vagal afferent transmission in the NTS mediating reflex responses of the rat esophagus. Am J Physiol Regul Integr Comp Physiol 274: R1436-R1445, 1998.
63. Lukovic L, DeJong W, and DeWied D. Cardiovascular effects of substance P and capsaicin microinjected into the nucleus tractus solitarii of the rat. Brain Res 422: 312-318, 1987.
64. 2 receptor subtypes in the tonic inhibitory modulation of baroreceptor reflex response by endogenous angiotensins at the nucleus tractus solitarii in the rat. Brain Res 782: 73-82, 1998.
65. 1 receptors in the nucleus of the solitary tract to attenuate the baroreceptor reflex. Am J Physiol Regul Integr Comp Physiol 275: R1611-R1619, 1998.
66. Mazzone SB and Canning BJ. Synergistic interactions between airway afferent nerve subtypes mediating reflex bronchospasm in guinea pigs. Am J Physiol Regul Integr Comp Physiol 283: R86-R98, 2002.
67. Mendelowitz D, Yang M, Andresen MC, and Kunze DL. Localization and retention in vitro of fluorescently labeled aortic baroreceptor terminals on neurons from the nucleus tractus solitarius. Brain Res 581: 339-343, 1992.
68. Mendelsohn FAO, Quirion R, Saavedra JM, Aguilera G, and Catt KJ. Autoradiographic localization of angiotensin II receptors in rat brain. Proc Natl Acad Sci USA 81: 1575-1579, 1984.
69. Michelini LC and Bonagamba LGH. Angiotensin II as a modulator of baroreceptor reflexes in the brainstem of conscious rats. Hypertension 15 Suppl I: I-45-I-50, 1990.
70. Miles R. Frequency dependence of synaptic transmission in nucleus of the solitary tract in vitro. J Neurophysiol 55: 1076-1089, 1986.
71. Mosqueda-Garcia R, Tseng CJ, Appalsamy M, and Robertson D. Cardiovascular effects of microinjection of angiotensin II in the brainstem of renal hypertensive rats. J Pharmacol Exp Ther 255: 374-381, 1990.
72. Mutoh T, Bonham AC, and Joad JP. Substance P in the nucleus of the solitary tract augments bronchopulmonary C fiber reflex output. Am J Physiol Regul Integr Comp Physiol 279: R1215-R1223, 2000.
73. Palkovits M and Zaborszky L. Neuroanatomy of central cardiovascular control. Nucleus tractus solitarii: afferent and efferent neuronal connections in relation to the baroreceptor reflex arc. Prog Brain Res 47: 9-34, 1977.
74. Papas S, Smith P, and Ferguson AV. Electrophysiological evidence that systemic angiotensin influences rat area postrema neurons. Am J Physiol Regul Integr Comp Physiol 258: R70-R76, 1990.
75. Paton JFR and Kasparov S. Differential effects of angiotensin II on cardiorespiratory reflexes mediated by nucleus tractus solitarii - a microinjection study in the rat. J Physiol 521: 213-225, 1999.
76. Phillips MI. Functions of angiotensin in the central nervous system. Annu Rev Physiol 49: 413-435, 1987.
77. Qu L, McQueeney AJ, and Barnes KL. Presynaptic or postsynaptic location of receptors for angiotensin II and substance P in the medial solitary tract nucleus. J Neurophysiol 75: 2220-2228, 1996.
78. Rettig R, Healy DP, and Printz MP. Cardiovascular effects of microinjections of angiotensin II into the nucleus tractus solitarii. Brain Res 364: 233-244, 1986.
79. Ruggiero DA, Pickel VM, Milner TA, Anwar M, Otake K, Mtui EP, and Park D. Viscerosensory processing in nucleus tractus solitarii: structural and neurochemical substrates. In: Nucleus of the Solitary Tract, edited by Barraco IRA. Boca Raton, FL: CRC, 1994, p. 3-34.
80. Shapiro RE and Miselis RR. The central organization of the vagus nerve innervating the stomach of the rat. J Comp Neurol 238: 473-488, 1985.
81. Standish A, Enquist LW, Escardo JA, and Schwaber JS. Central neuronal circuit innervating the rat heart defined by transneuronal transport of pseudorabies virus. J Neurosci 15: 1998-2012, 1995.
82. Stauss HM. Baroreceptor reflex function. Am J Physiol Regul Integr Comp Physiol 283: R284-R286, 2002.
83. Talman WT, Perrone MH, and Reis DJ. Evidence for L-glutamate as the neurotransmitter of baroreceptor afferent nerve fibers. Science 209: 813-815, 1980.
84. Tell F and Bradley RM. Whole-cell analysis of ionic currents underlying the firing pattern of neurons in the gustatory zone of the nucleus tractus solitarii. J Neurophysiol 71: 479-492, 1994.
85. Wallach JH and Loewy AD. Projections of the aortic nerve to the nucleus tractus solitarius in the rabbit. Brain Res 188: 247-251, 1980.
86. Wamsley JK, Herblin WF, Alburges ME, and Hunt M. Evidence for the presence of angiotensin II-type 1 receptors in brain. Brain Res Bull 25: 397-400, 1990.
87. Yang CR, Phillips MI, and Renaud LP. Angiotensin II receptor activation depolarizes rat supraoptic neurons in vitro. Am J Physiol Regul Integr Comp Physiol 263: R1333-R1338, 1992.
88. Yang M and Andresen MC. Angiotensin enhances sensory afferent synaptic transmission in neurons of rat medial nucleus tractus solitarius (mNTS) in vitro (Abstract). FASEB J 5: A677, 1991.
89. Yen JC, Chan JY, and Chan SH. Differential roles of NMDA and non-NMDA receptors in synaptic responses of neurons in nucleus tractus solitarii of the rat. J Neurophysiol 81: 3034-3043, 1999.
90. Zhang J and Mifflin SW. Differential roles for NMDA and non-NMDA receptor subtypes in baroreceptor afferent integration in the nucleus of the solitary tract of the rat. J Physiol 511: 733-745, 1998.
91. Zhang J and Mifflin SW. Subthreshold aortic nerve inputs to neurons in nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 278: R1595-R1604, 2000.