Sensory afferent and hypoxia-mediated activation of nucleus tractus solitarius neurons that project to the rostral ventrolateral medulla

Neuroscience

Volumn 167, Issue 2, 2010, Pages 510-527

  Kline, D D ^a,b   King, T L ^a   Austgen, J R ^a,b   Heesch, C M ^a,b   Hasser, E M ^a,b,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c University of Missouri   (United States)

Author keywords

Cardiovascular; Chemoreflex; Fos; Respiration; Retrograde

Indexed keywords

POTASSIUM; PROTEIN FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BRAIN ELECTROPHYSIOLOGY; CATECHOLAMINERGIC SYSTEM; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HYPOXIA; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; MONOSYNAPTIC POTENTIAL; NERVE CELL STIMULATION; NONHUMAN; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; ROSTRAL VENTROLATERAL MEDULLA; SENSORY NERVE; SOLITARY TRACT NUCLEUS;

ACTION POTENTIALS; AFFERENT PATHWAYS; CAROTID BODY; CATECHOLAMINES; CELL HYPOXIA; CELL MEMBRANE; EXCITATORY POSTSYNAPTIC POTENTIALS; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; NEURONS; POTASSIUM CHANNELS; PROTO-ONCOGENE PROTEINS C-FOS; SOLITARY NUCLEUS;

EID: 77950863892     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.02.012     Document Type: Article

References (48)

1. Aicher S.A., Saravay R.H., Cravo S.L., Jeske I., Morrison S.F., Reis D.J., Milner T.A. Monosynaptic projections from the nucleus tractus solitarii to C1 adrenergic neurons in the rostral ventrolateral medulla: comparison with input from the caudal ventrolateral medulla. J Comp Neurol 1996, 373:62-75.
2. Andresen M.C., Kunze D.L. Nucleus tractus solitarius-gateway to neural circulatory control. Annu Rev Physiol 1994, 56:93-116.
3. Austgen J.R., Fong A.Y., Foley C.M., Mueller P.J., Kline D.D., Heesch C.M., Hasser E.M. Expression of group I metabotropic glutamate receptors on phenotypically different cells within the nucleus of the solitary tract in the rat. Neuroscience 2008, 159:701-716.
4. Aylwin M.L., Horowitz J.M., Bonham A.C. NMDA receptors contribute to primary visceral afferent transmission in the nucleus of the solitary tract. J Neurophysiol 1997, 77:2539-2547.
5. Bailey T.W., Hermes S.M., Andresen M.C., Aicher S.A. 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 2006, 26:11893-11902.
6. Berquin P., Bodineau L., Gros F., Larnicol N. Brainstem and hypothalamic areas involved in respiratory chemoreflexes: a Fos study in adult rats. Brain Res 2000, 857:30-40.
7. 1-area) in the rabbit. Brain Res 1987, 419:336-340.
8. Bonham A.C., Chen C.-Y. Glutamatergic neural transmission in the nucleus tractus solitarius: N-methyl-d-aspartate receptors. Clin Exp Pharmacol Physiol 2002, 29:497-502.
9. Chan R.K.W., Sawchenko P.E. Organization and transmitter specificity of medullary neurons activated by sustained hypertension: implications for understanding baroreceptor reflex circuitry. J Neurosci 1998, 18:371-387.
10. Chen C.Y., Horowitz J.M., Bonham A.C. A presynaptic mechanism contributes to depression of autonomic signal transmission in NTS. Am J Physiol 1999, 277:H1350-H1360.
11. Dampney R.A.L. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 1994, 74:323-364.
12. Dampney R.A.L. The subretrofacial vasomotor nucleus: anatomical, chemical and pharmacological properties and role in cardiovascular regulation. Prog Neurobiol 1994, 42:197-227.
13. Dekin M.S., Getting P.A. In vitro characterization of neurons in the ventral part of the nucleus tractus solitarius. II. Ionic basis for repetitive firing patterns. J Neurophysiol 1987, 58:215-229.
14. Dekin M.S., Getting P.A., Johnson S.M. In vitro characterization of neurons in the ventral part of the nucleus tractus solitarius. I. Identification of neuronal types and repetitive firing properties. J Neurophysiol 1987, 58:195-214.
15. Doyle M.W., Andresen M.C. Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 2001, 85:2213-2223.
16. Doyle M.W., Bailey T.W., Young-Ho J., Appleyard S.M., Low M.J., Andresen M.C. Strategies for cellular identification in nucleus tractus solitarius slices. J Neurosci Methods 2004, 137:37-48.
17. Dragunow M., Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 1989, 29:261-265.
18. Erickson J.T., Millhorn D.E. Hypoxia and electrical stimulation of the carotid sinus nerve induce Fos-like immunoreactivity within catecholaminergic and serotoninergic neurons of the rat brainstem. J Comp Neurol 1994, 348:161-182.
19. Gozal D., Xue Y.D., Simakajornboon N. Hypoxia induces c-Fos protein expression in NMDA but not AMPA glutamate receptor labeled neurons within the nucleus tractus solitarii of the conscious rat. Neurosci Lett 1999, 262:93-96.
20. Guyenet P.G. The sympathetic control of blood pressure. Nat Rev Neurosci 2006, 7:335-346.
21. Hancock M.B. Evidence for direct projections from the nucleus of the solitary tract onto medullary adrenaline cells. J Comp Neurol 1988, 276:460-467.
22. Hermes S.M., Mitchell J.L., Aicher S.A. Most neurons in the nucleus tractus solitarii do not send collateral projections to multiple autonoic targets in the rat brain. Exp Neurol 2006, 198:539-551.
23. Hirooka Y., Polson J.W., Potts P.D., Dampney R.A.L. Hypoxia-induced Fos expression in neurons projecting to the pressor region in the rostral ventrolateral medulla. Neuroscience 1997, 80:1209-1224.
24. Kantzides A., Badoer E. Activation of NADPH-diaphorase-positive projections to the rostral ventrolateral medulla following cardiac mechanoreceptor stimulation in the conscious rat. Am J Physiol Regul Integr Comp Physiol 2006, 290:R1626-R1638.
25. Kantzides A., Owens N.C., de Matteo R., Badoer E. Right atrial stretch activates neurons in autonomic brain regions that project to the rostral ventrolateral medulla in the rat. Neuroscience 2005, 133:775-786.
26. Katz L.C., Burkhalter A., Dreyer W.J. Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 1984, 310:498-500.
27. Kiely J.M., Gordon F.J. Non-NMDA receptors in the rostral ventrolateral medulla mediate somatosympathetic pressor responses. J Auton Nerv Syst 1993, 43:231-240.
28. Kline D.D. Plasticity in glutamatergic NTS neurotransmission. Respir Physiol Neurobiol 2008, 164:105-111.
29. Kline D.D., Takacs K.N., Ficker E., Kunze D.L. Dopamine modulates synaptic transmission in the nucleus of the solitary tract. J Neurophysiol 2002, 88:2736-2744.
30. Koshiya N., Guyenet P.G. NTS neurons with carotid chemoreceptor inputs arborize in the rostral ventrolateral medulla. Am J Physiol 1996, 270:R1273-R1278.
31. Koshiya N., Huangfu D., Guyenet P.G. Ventrolateral medulla and sympathetic chemoreflex in the rat. Brain Res 1993, 609:174-184.
32. 2 depresses solitary tract-mediated synaptic transmission in the nucleus tractus solitarius. Neuroscience 2007, 146:792-801.
33. Li D.P., Yang Q. Membrane and synaptic properties of nucleus tractus solitarius neurons projecting to the caudal ventrolateral medulla. Auton Neurosci 2007, 136:69-81.
34. Massari V.J., Shirahata M., Johnson T.A., Gatti P.J. Carotid sinus nerve terminals which are tyrosine hydroxylase immunoreactive are found in the commissural nucleus of the tractus solitarius. J Neurocytol 1996, 25:197-208.
35. May O.L., Erisir A., Hill D.L. Ultrastructure of primary afferent terminals and synapses in the rat nucleus of the solitary tract: comparison among the greater superficial petrosal, chorda tympani, and glossopharyngeal nerves. J Comp Neurol 2007, 502:1066-1078.
36. A inhibition of the RVLM following hindlimb unloading in rats. Am J Physiol Regul Integr Comp Physiol 2002, 283:R604-R614.
37. Monnier A., Alheid G.F., McCrimmon D.R. Defining ventral medullary respiratory compartments with a glutamate receptor agonist in the rat. J Physiol 2003, 548:859-874.
38. Otake K., Ezure K., Lipski J., Wong She R.B. Projections from the commissural subnucleus of the nucleus of the solitary tract: an anterograde tracing study in the cat. J Comp Neurol 1992, 324:365-378.
39. Paxinos G., Watson C. The Rat Brain in stereotaxic coordinates 1997, Academic Press, San Diego.
40. Ross C.A., Ruggiero D.A., Reis D.J. Projections from the nucleus tractus solitarii to the rostral ventrolateral medulla. J Comp Neurol 1985, 242:511-534.
41. Spyer K.M. Central nervous mechanisms contributing to cardiovascular control. J Physiol 1994, 474:1-19.
42. Suwabe T., Bradley R.M. Characteristics of rostral solitary tract nucleus neurons with identified afferent connections that project to the parabrachial nucleus in rats. J Neurophysiol 2009, 102:546-555.
43. Takakura A.C., Moreira T.S., Colombari E., West G.H., Stornetta R.L., Guyenet P.G. Peripheral chemoreceptor inputs to retrotrapezoid nucleus (RTN) CO2-sensitive neurons in rats. J Physiol 2006, 572:503-523.
44. Tell F., Bradley R.M. Whole-cell analysis of ionic currents underlying the firing pattern of neurons in the gustatory zone of the nucleus tractus solitarii. J Neurophysiol 1994, 71:479-492.
45. Teppema L.J., Veening J.G., Kranenburg A., Dahan A., Berkenbosch A., Olievier C. Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J Comp Neurol 1997, 388:169-190.
46. Van Bockstaele E.J., Pieribone V.A., Aston-Jones G. Diverse afferents converge on the nucleus paragigantocellularis in the rat ventrolateral medulla: retrograde and anterograde tracing studies. J Comp Neurol 1989, 290:561-584.
47. Vincent A., Tell F. Postnatal changes in electrophysiological properties of rat nucleus tractus solitarii neurons. Eur J Neurosci 1997, 9:1612-1624.
48. Weston M., Wang H., Stornetta R.L., Sevigny C.P., Guyenet P.G. Fos expression by glutamatergic neurons of the solitary tract nucleus after phenylephrine-induced hypertension in rats. J Comp Neurol 2003, 460:525-541.