Somatic nociception activates NK1 receptors in the nucleus tractus solitarii to attenuate the baroreceptor cardiac reflex

European Journal of Neuroscience

Volumn 16, Issue 5, 2002, Pages 907-920

  Boscan, Pedro ^a   Kasparov, Sergey ^a   Paton, Julian F R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Baroreflex; Cardiovascularl; GABA; NTS; Pain; Substance P

Indexed keywords

3 (2 METHOXYBENZYLAMINO) 2 PHENYLPIPERIDINE; BICUCULLINE METHIODIDE; NEUROKININ 1 RECEPTOR; SUBSTANCE P;

ANIMAL TISSUE; ARTICLE; BRACHIAL PLEXUS; CAROTID SINUS; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; ELECTROSTIMULATION; EVOKED RESPONSE; INTERNEURON; MICROINJECTION; NERVE STIMULATION; NOCICEPTION; NONHUMAN; PRESSORECEPTOR REFLEX; PRESSURE; PRIORITY JOURNAL; RAT; SOLITARY TRACT NUCLEUS;

ANIMALS; BAROREFLEX; BICUCULLINE; ELECTROPHYSIOLOGY; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; MICROINJECTIONS; NEURAL INHIBITION; NOCICEPTORS; PAIN; PAIN MEASUREMENT; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, NEUROKININ-1; SOLITARY NUCLEUS; SUBSTANCE P;

EID: 0036457214     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02131.x     Document Type: Article

References (74)

1. Abram, S.E., Kostreva, D.R., Hopp, F.A. & Kampine, J.P. (1983) Cardiovascular responses to noxious radiant heat in anesthetized cats. Am. J. Physiol., 245, R576-R580.
2. al'Absi, M., Buchanan, T.W., Marrero, A. & Lovallo, W.R. (1999) Sex differences in pain perception and cardiovascular responses in persons with parental history for hypertension. Pain, 83, 331-338.
3. Olsen, U.B. & Lund, A. (1991) Inhibition by glutamate antagonists, MK-801 and NBQX, of cutaneo-cardiovascular pain reflex in rats. Europ. J. Pharm., 203, 133-135.
4. Bard, P. & Macht, M.B. (1958) The behaviour of cronically decerebrate cats. CIBA Foundation Symposium on Neurological Basis of Behaviour, pp. 55-78.
5. Barr, G.A. (1998) Maturation of the biphasic behavioral and heart rate response in the formalin test. Pharm. Biochem. Behav., 60, 329-335.
6. Baude, A. & Shigemoto, R. (1998) Cellular and subcellular distribution of substance P receptor immunoreactivity in the dorsal vagal complex of the rat and cat: a light and electron microscope study. J. Comp. Neurol., 402, 181-196.
7. Bennett, J.A., McWilliam, P.N. & Shepheard, S.L. (1987) A gamma-aminobutyric-acid-mediated inhibition of neurones in the nucleus tractus solitarius of the cat. J. Physiol. (Lond.), 392, 417-430.
8. Besson, J.-M. & Chaouch, A. (1987) Peripheral and spinal mechanisms of nociception. Physiol. Rev., 67, 67-186.
9. Blessing, W.W. (1997) Anatomy of the lower brainstem. In: The Lower Brainstem and Bodily Homeostasis. Oxford University Press. Oxford, pp. 29-101.
10. Boscan, P. & Paton, J.F.R. (2000a) Attenuation of the baroreceptor reflex induced by nociceptive inputs is mediated by GABAa receptors in the nucleus of the solitary tract. J. Physiol. (Lond.), 526P, 131P-132P.
11. Boscan, P. & Paton, J.F.R. (2000b) Noxious stimulation releases substance P in the nucleus of the solitary tract (NTS) which attenuates the baroreceptor reflex. J. Auton. Nerv. Sys., 82, 54P.
12. Boscan, P. & Paton, J.F.R. (2001a) Role of the solitary tract nucleus in mediating nociceptive evoked cardiorespiratory responses. Auton. Neurosc. Basic Clin., 86, 170-182.
13. Boscan, P. & Paton, J.F.R. (2002) Nociceptive afferents selectively modulate the cardiac component of the peripheral chemoreceptor reflex via actions within the solitary tract nucleus. Neuroscience, 110, 319-328.
14. Callera, J.C., Bonagamba, L.G., Nosjean, A., Laguzzi, R. & Machado, B.H. (2000) Activation of GABA receptors in the NTS of awake rats reduces the gain of baroreflex bradycardia. Auton. Neurosc. Basic Clin., 84, 58-67.
15. Cervero, F. & Plenderleith, M.B. (1985) C-fibre excitation and tonic descending inhibition of dorsal horn neurones in adult rats treated at birth with capsaicin. J. Physiol. (Lond.), 365, 223-237.
16. Ciriello, J., Hochstenbach, S.L. & Roder, S. (1994) Central projections of baroreceptor and chemoreceptor afferent fibers in the rat. In Barraco, I.R.A. (eds), Nucleus of the Solitary Tract. CRC press, Boca Raton, London, pp. 35-50.
17. Craig, A.D. (1995) Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J. Comp. Neurol., 361, 225-248.
18. Craig, A.D., Broman, J. & Blomqvist, A. (1992) Lamina I spinocervical tract terminations in the medial part of the lateral cervical nucleus in the cat. J. Comp. Neurol., 322, 99-110.
19. Deuchars, J., Li, Y.-W., Kasparov, S. & Paton, J.F.R. (2000) Morphological and electrophysiological properties of physiologically characterised baroreceptive neurones in the dorsal vagal complex of the rat. J. Comp. Neurol., 417, 233-249.
20. Esteves, F., Lima, D. & Coimbra, A. (1993) Structural types of spinal cord marginal (lamina I) neurons projecting to the nucleus of the tractus solitarius in the rat. Somatosens. Motor Res., 10, 203-216.
21. Felder, R.B. & Mifflin, S.W. (1988) Modulation of carotid sinus afferent input to nucleus tractus solitarius by parabrachial nucleus stimulation. Circulat. Res., 63, 35-49.
22. Feldman, P.D. (1995) Neurokinin1 receptor mediation of the vasodepressor effects of substance P in the nucleus of the tractus solitarius. J. Pharmacol. Exper. Therap., 273, 617-623.
23. Gamboa-Esteves, F.O., Kaye, J.C., McWilliam, P.N., Lima, D. & Batten, T.F.C. (2001) Immunohistochemical profiles of spinal lamina I neurones retrogradely labelled from the nucleus tractus solitarii in rat suggest excitatory projections. Neuroscience, 104, 523-538.
24. Izzo, P.N., Sykes, R.M. & 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.
25. Jafri, M.S. & Weinreich, D. (1996) Substance P hyperpolarizes vagal sensory neurones of the ferret. J. Physiol. (Lond.), 493, 157-166.
26. Jia, H.-G., Wang, B.-R., Shi, J.-W., Shigemoto, R., Kaneko, T. & Mizuno, N. (1996) GABAergic synapses upon neurons expressing substance P receptors in the nucleus of the solitary tract: An immunocytochemical electron microscope study in the rat. Neurosci. Lett., 210, 49-52.
27. Jordan, D., Mifflin, S.W. & Spyer, K.M. (1988) Hypothalamic inhibition of neurones in the nucleus tractus solitarius of the cat is GABA mediated. J. Physiol. (Lond.), 399, 389-404.
28. Kaneko, T., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1994) Morphological and chemical characteristics of substance P receptor-immunoreactive neurons in the rat neocortex. Neuroscience, 60, 199-211.
29. Kubo, T. & Kihara, M. (1987) Evidence for the presence of GABAergic and glycine-like systems responsible for cardiovascular control in the nucleus tractus solitarii of the rat. Neurosci. Lett., 74, 331-336.
30. Kumada, M., Nogami, K. & Sagawa, K. (1975) Modulation of carotid sinus baroreceptor reflex by sciatic nerve stimulation. Am. J. Physiol., 228, 1535- 1541.
31. Lima, D., Esteves, F. & Coimbra, A. (1994) C-fos activation by noxious input of spinal neurons projecting to the nucleus of the tractus solitarius in the rat. [7th World Pain Congress, Paris.] IASP Press, Seattle, pp. 423-434.
32. Maley, B. & Newton, B.W. (1985) Immunohistochemistry of gamma-aminobutyric acid in the cat nucleus tractus solitarius. Brain Res., 330, 364-368.
33. Mantyh, P.W., Gates, T., Mantyh, C.R. & Maggio, J.E. (1989) Autoradiographic localization and characterization of tachykinin receptor binding sites in the rat brain and peripheral tissues. J. Neurosci., 9, 258-279.
34. Massari, V.J., Shirahata, M., Johnson, T.A., Lauenstein, J.M. & Gatti, P.J. (1998) Substance P immunoreactive nerve terminals in the dorsolateral nucleus of the tractus solitarius: roles in the baroreceptor reflex. Brain Res., 785, 329-340.
35. Maubach, K.A., Cody, C. & Jones, R.S.G. (1998) Tachykinins may modify spontaneous epileptiform activity in the rat entorhinal cortex in vitro by activating GABAergic inhibition. Neuroscience, 83, 1047-1062.
36. Maubach, K.A., Martin, K., Smith, D.W., Hewson, L., Frankshun, R.A., Harrison, T. & Seabrook, G.R. (2001) Substance P stimulates inhibitory synaptic transmission in the guinea pig basolateral amygdala in vitro. Neuropharmacology, 40, 806-817.
37. McMahon, S.E., McWilliam, P.N., Robertson, J. & Kaye, J.C. (1992) Inhibition of carotid sinus baroreceptor neurones in the nucleus tractus solitarius of the anaesthetized cat by electrical stimulation of hindlimb afferent fibres. J. Physiol. (Lond.), 452, 224P.
38. McWilliam, P.N. & Shepheard, S.L. (1988) A GABA-mediated inhibition of neurones in the nucleus tractus solitarius of the cat that respond to electrical stimulation of the carotid sinus nerve. Neurosci. Lett., 94, 321-326.
39. McWilliam, P.N. & Yang, T. (1991) Inhibition of cardiac vagal component of baroreflex by group III and IV afferents. Am. J. Physiol., 260, H730-H734.
40. Meeley, M.P., Ruggiero, D.A., Ishitsuka, T. & Reis, D.J. (1985) Intrinsic gamma-aminobutyric acid neurons in the nucleus of the solitary tract and the rostral ventrolateral medulla of the rat: An immunocytochemical and biochemical study. Neurosci. Lett., 58, 83-89.
41. Menetrey, D. & Basbaum, A.I. (1987) Spinal and trigeminal projections to the nucleus of the solitary tract: A possible substrate for somatovisceral and viscerovisceral reflex activation. J. Comp. Neurol., 255, 439-450.
42. Menetrey, D. & De Pommery, J. (1991) Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur. J. Neurosci., 3, 249-259.
43. Meng, Z. & Lu, G. (2000) Projection linkage from spinal neurons to both lateral cervical nucleus and solitary tract nucleus in the cat. Biol. Signals Recept., 9, 38-44.
44. Morilak, D.A., Morris, M. & Chalmers, J. (1988) Release of substance P in the nucleus tractus solitarius measured by in vivo mirodialysis: Response to stimulation of the aortic depressor nerves in rabbit. Neurosci. Lett., 94, 131- 137.
45. Nagashima, A., Takano, Y., Tateishi, K., Matsuoka, Y., Hamaoka, T. & Kamiya, H.-O. (1989) Cardiovascular roles of tachykinin peptides in the nucleus tractus solitarii of rats. Brain Res., 487, 392-396.
46. Ness, T.J. & Gebhart, G.F. (1990) Visceral pain: a review of experimental studies. Pain, 41, 167-234.
47. Oberlander, T.F., Grunau, R.E., Pitfield, S., Whitfield, M.F. & Saul, J.P. (1999) The developmental character of cardiac autonomic responses to an acute noxious event in 4-and 8-month-old healthy infants. Pediatric Res., 45, 519-525.
48. Okada, M. & Bunag, R.D. (1995) Contrasting baroreflex effects of muscimol versus bicuculline injected into the nucleus tractus solitarius in anesthetized rats. J. Cardiovasc. Pharmacol., 26, 363-371.
49. Otsuka, M. & Yoshioka, K. (1993) Neurotransmitter functions of mammalian tachykinins. Physiol. Rev., 73, 229-308.
50. Paton, J.F.R. (1996) A working heart-brainstem preparation of the mouse. J. Neurosc. Meth., 65, 63-68.
51. Paton, J.F.R. (1997) Cerebellar control of cardiovascular activity. In Jordan, D. (ed.), Central Nervous Control of Autonomic Function. Harwood Academic Press, UK, pp. 225-257.
52. Paton, J.F.R. (1998) Importance of neurokinin-1 receptors in the nucleus tractus solitarii of mice for the integration of cardiac vagal inputs. Eur. J. Neurosci., 10, 2261-2275.
53. Paton, J.F.R. & Kasparov, S. (1999) Differential effects of angiotensin II on cardiorespiratory reflexes mediated by nucleus tractus solitarii - A microinjection study in the rat. J. Physiol. (Lond.), 521, 213-225.
54. Paton, J.F.R. & Kasparov, S. (2000) Sensory channel specific modulation in the nucleus of the solitary tract. J. Autonom. Nerv. Syst., 80, 117-129.
55. Paton, J.F.R., Silva-Carvalho, L., Thompson, C.S. & Spyer, K.M. (1990) Nucleus tractus solitarius as mediator of evoked parabrachial cardiovascular responses in the decerebrate rabbit. J. Physiol. (Lond.), 428, 693-705.
56. Perez, H., Ruiz, S., Inostroza, H. & Perretta, M. (1992) Substance P depresses bioelectrical responses evoked in the nucleus tractus solitarii: Interaction with gamma-aminobutyric acid-ergic neurons. Eur. J. Pharmacol., 213, 435-437.
57. Pezzone, M.A., Lee, W.S., Hoffman, G.E., Pezzone, M.A. & Rabin, B.S. (1993) Activation of brainstem catecholaminergic neurons by conditioned and unconditioned aversive stimuli as revealed by c-Fos immunoreactivity. Brain Res., 608, 310-318.
58. Potter, E.K. & McCloskey, D.I. (1982) Inhibition of carotid baroreceptor and chemoreceptor reflexes by brief sciatic nerve stimulation. J. Autonom. Nerv. Syst., 6, 391-394.
59. Potts, J.T. & Fuchs, I.E. (2001) Naturalistic activation of barosensitive afferents release substance P in the nucleus tractus solitarius of the cat. Brain Res., 893, 155-164.
60. Potts, J.T., Fuchs, I.E., Li, J., Leshnower, B. & Mitchell, J.H. (1999) Skeletal muscle afferent fibres release substance P in the nucleus tractus solitarii of anaesthetized cats. J. Physiol. (Lond.), 514, 829-841.
61. Quest, J.A. & Gebber, G.L. (1972) Modulation of baroreceptor reflexes by somatic afferent nerve stimulation. Am. J. Physiol., 222, 1251-1259.
62. Roizen, M.F., Horrigan, R.W. & Frazer, B.M. (1981) Anesthetic doses blocking adrenergic (stress) and cardiovascular responses to incision - MAC BAR. Anesthesiology, 54, 390-398.
63. Saha, S., Batten, T.F.C. & McWilliam, P.N. (1995) Glutamate, gamma-aminobutyric acid and tachykinin-immunoreactive synapses in the cat nucleus tractus solitarii. J. Neurocytol., 24, 55-74.
64. Sapru, H.N. (1994) Transmitter/Receptor mechanisms in cardiovascular control by the NTS: Excitatory amino acids, acetylcholine, and substance P. In Barraco, I.R.A. (ed.). Nucleus of the Solitary Tract. CRC Press, London, pp. 267-281.
65. Seagard, J.L., Dean, C. & Hopp, F.A. (2000) Modulation of the carotid baroreceptor reflex by substance P in the nucleus tractus solitarius. J. Autonom. Nerv. Syst., 78, 77-85.
66. Spyer, K.M. (1990) The central nervous organization of reflex circulatory control. In Loewy, A.D.&. Spyer, K.M, (eds), Central Regulation of Autonomic Functions. Oxford University Press, Oxford, pp. 168-188.
67. Spyer, K.M. (1994) Central nervous mechanisms contributing to cardiovascular control. J. Physiol. (Lond.), 474, 1-19.
68. Sun, M.K. & Spyer, K.M. (1991) Nociceptive inputs into rostral ventrolateral medulla-spinal vasomotor neurones in rats. J. Physiol. (Lond.), 436, 685- 700.
69. Sved, A.F. (1994) GABA Mediated neural transmission in mechanisms of cardiovascular control by the NTS. In Barraco, I.R.A (ed.), Nucleus of the Solitary Tract. CRC Press, London, pp. 245-253.
70. Sykes, R.M., Spyer, K.M. & Izzo, P.N. (1994) Central distribution of substance P, calcitonin gene-related peptide and 5-hydroxytryptamine in vagal sensory afferents in the rat dorsal medulla. Neuroscience, 59, 195- 210.
71. Toney, G.M. & Mifflin, S.W. (1995) Time-dependent inhibition of hindlimb somatic afferent transmission within nucleus tractus solitarius: An in vivo intracellular recording study. Neuroscience, 68, 445-453.
72. Toney, G.M. & Mifflin, S.W. (2000) Sensory modalities conveyed in the hindlimb somatic afferent input to nucleus tractus solitarius. J. Appl. Physiol., 88, 2062-2073.
73. Traub, R.J., Sengupta, J.N. & Gebhart, G.F. (1996) Differential c-fos expression in the nucleus of the solitary tract and spinal cord following noxious gastric distention in the rat. Neuroscience, 74, 873-884.
74. Wang, Q. & Li, P. (1988) Inhibition of baroreflex following microinjection of GABA or morphine into the nucleus tractus solitarii in rabbits. J. Autonom. Nerv. Syst., 25, 165-172.