Trigeminal autonomic pathways involved in nociception-induced reflex cardiovascular responses

Reflex cardiovascular responses elicited by noxious oro-facial stimulation are well known but the neural pathways that underlie trigeminal cardiovascular reflex reactions remain to be elucidated. In previous studies, we have shown that noxious electrical stimulation of the mandibular incisor in the anesthetized rat elicits increases in mean arterial blood pressure and heart rate (Allen, G.V., Barbrick, B. and Esser, M.J., Trigeminal parabrachial connections: possible pathway for nociception-induced cardiovascular reflex responses, Brain Res., 715 (1996) 125-135). In this study, microinjections of the presynaptic blocker, cobalt chloride, or the anesthetic agent, lidocaine, were made into selected brainstem sites to identify neural pathways that are involved in mediation of the reflex pressor responses. Ipsilateral and bilateral injections of chemical blocker into the dorsomedial spinal trigeminal nucleus, pars caudalis, lateral parabrachial nucleus and the rostral ventral lateral medulla/caudal A5 region attenuated the reflex cardiovascular response. Bilateral injections of cobalt chloride into the dorsomedial subnucleus caudalis resulted in 70-100% attenuation of the reflex pressor response. Bilateral injections of cobalt chloride and/or lidocaine into the lateral parabrachial nucleus or the rostral ventral lateral medulla/A5 region resulted in 43-57% and 44-100% attenuation of the reflex pressor response, respectively. There were no significant differences in the degree or duration of attenuation of the reflex pressor responses produced by cobalt chloride compared to that produced by lidocaine injections. The reflex pressor responses usually returned to baseline levels approximately 60 min following injection of the chemical blocker substance. The results indicate that noxious electrical stimulation of the mandibular incisor elicits a reflex increase in mean arterial blood pressure which is initially mediated in the dorsomedial spinal trigeminal nucleus, pars caudalis and is subsequently mediated in the lateral parabrachial nucleus and the rostral ventral lateral medulla/caudal A5 region.

[1]  C. Saper,et al.  Spinal and trigeminal dorsal horn projections to the parabrachial nucleus in the rat , 1985, The Journal of comparative neurology.

[2]  R. Schmidt,et al.  Somatosympathetic reflexes: afferent fibers, central pathways, discharge characteristics. , 1973, Physiological reviews.

[3]  P. Guyenet,et al.  Afferent and efferent connections of the A5 noradrenergic cell group in the rat , 1987, The Journal of comparative neurology.

[4]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[5]  Peter H. Schiller,et al.  A method of reversible inactivation of small regions of brain tissue , 1979, Journal of Neuroscience Methods.

[6]  A. Woda,et al.  Is electrical stimulation of the rat incisor an appropriate experimental nociceptive stimulus? , 1986, Experimental Neurology.

[7]  K. M. Spyer,et al.  Central regulation of autonomic functions , 1990 .

[8]  D. Reis,et al.  Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Pat Levitt,et al.  Origin and organization of brainstem catecholamine innervation in the rat , 1979, The Journal of comparative neurology.

[10]  L. Wang,et al.  Formalin induced FOS-like immunoreactive neurons in the trigeminal spinal caudal subnucleus project to contralateral parabrachial nucleus in the rat , 1994, Brain Research.

[11]  A. Goodchild,et al.  Role of ventrolateral medulla in vasomotor regulation: a correlative anatomical and physiological study , 1982, Brain Research.

[12]  F. M. Clark,et al.  The projections of noradrenergic neurons in the A5 catecholamine cell group to the spinal cord in the rat: anatomical evidence that A5 neurons modulate nociception , 1993, Brain Research.

[13]  S. White,et al.  Nasopharyngeal reflexes: integrative analysis of evoked respiratory and cardiovascular effects. , 1973, The Australian journal of experimental biology and medical science.

[14]  D. L. Brown,et al.  Cardiovascular neurons of brain stem with projections to spinal cord. , 1984, The American journal of physiology.

[15]  C. Saper,et al.  Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat , 1990, The Journal of comparative neurology.

[16]  H. Hayashi,et al.  Pulpal and cutaneous inputs to somatosensory neurons in the parabrachial area of the cat , 1990, Brain Research.

[17]  G. Gebhart,et al.  Characterization of descending modulation of nociception from the A5 cell group , 1991, Brain Research.

[18]  H. Andersen The reflex nature of the physiological adjustments to diving and their afferent pathway. , 1963, Acta physiologica Scandinavica.

[19]  T. Ness,et al.  Colorectal distension as a noxious visceral stimulus: physiologic and pharmacologic characterization of pseudaffective reflexes in the rat , 1988, Brain Research.

[20]  Electrophysiological evidence for the modular organization of the reticular formation: sympathetic controlling circuits , 1987, Brain Research.

[21]  H. Hayashi A problem in electrical stimulation of incisor tooth pulp in rats , 1980, Experimental Neurology.

[22]  J. Sagen,et al.  Alterations in nociception following lesions of the A5 catecholamine nucleus , 1986, Brain Research.

[23]  D. Reis,et al.  The trigeminal depressor response: a cardiovascular reflex originating from the trigeminal system , 1975, Brain Research.

[24]  C. Marfurt,et al.  The central projections of tooth pulp afferent neurons in the rat as determined by the transganglionic transport of horseradish peroxidase , 1984, The Journal of comparative neurology.

[25]  S. Andersson,et al.  Is a selective stimulation of the rat incisor tooth pulp possible? , 1983, Pain.

[26]  A. Sakai,et al.  Effects of tooth pulp stimulation in trigeminal nucleus caudalis and adjacent reticular formation in rat , 1976, Brain Research.

[27]  A. Loewy,et al.  Efferent connections of the ventral medulla oblongata in the rat , 1981, Brain Research Reviews.

[28]  A. Loewy,et al.  Effects of kainic acid applied to the ventral surface of the medulla oblongata on vasomotor tone, the baroreceptor reflex and hypothalamic autonomic responses , 1982, Brain Research.

[29]  C. Marfurt,et al.  Trigeminal primary afferent projections to “non‐trigeminal” areas of the rat central nervous system , 1991, The Journal of comparative neurology.

[30]  R. Dubner,et al.  Spinal and trigeminal mechanisms of nociception. , 1983, Annual review of neuroscience.

[31]  D. Reis,et al.  The trigeminal depressor response: A novel vasodepressor response originating from the trigeminal system , 1977, Brain Research.

[32]  J. Sandkühler,et al.  Relative contributions of the nucleus raphe magnus and adjacent medullary reticular formation to the inhibition by stimulation in the periaqueductal gray of a spinal nociceptive reflex in the pentobarbital-anesthetized rat , 1984, Brain Research.

[33]  T. Sugimoto,et al.  Topographic organization of central terminal region of different sensory branches of the rat mandibular nerve , 1987, Experimental Neurology.

[34]  H. Herbert,et al.  Topographic organization ot spinal ana trigeminal somatosensory pathways to the rat parabrachial and Kölliker—fuse nuclei , 1995, The Journal of comparative neurology.

[35]  D. Bereiter,et al.  Caudal portions of the spinal trigeminal complex are necessary for autonomic responses and display Fos-like immunoreactivity after corneal stimulation in the cat , 1994, Brain Research.

[36]  J. Malpeli Activity of cells in area 17 of the cat in absence of input from layer a of lateral geniculate nucleus. , 1983, Journal of neurophysiology.

[37]  D. Reis,et al.  Neurons of rostral ventrolateral medulla mediate somatic pressor reflex. , 1989, The American journal of physiology.

[38]  J. Jhamandas,et al.  Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin , 1993, Brain Research Bulletin.

[39]  D. Armstrong,et al.  Adrenaline neurons in the rostral ventrolateral medulla innervate thoracic spinal cord: A combined immunocytochemical and retrograde transport demonstration , 1981, Neuroscience Letters.

[40]  V. Lebedev,et al.  Electrophysiological study of sympathoexcitatory structures of the bulbar ventrolateral surface as related to vasomotor regulation , 1986, Neuroscience.

[41]  James W. Hu Response properties of nociceptive and non-nociceptive neurons in the rat's trigeminal subnucleus caudalis (medullary dorsal horn) related to cutaneous and deep craniofacial afferent stimulation and modulation by diffuse noxious inhibitory controls , 1990, Pain.

[42]  M. D. Egger,et al.  Organization of HRP‐labeled trigeminal mandibular, primary afferent neurons in the rat , 1983, The Journal of comparative neurology.

[43]  J. Besson,et al.  The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. , 1990 .

[44]  A. Loewy,et al.  Electrophysiological evidence that the A5 catecholamine cell group is a vasomotor center , 1979, Brain Research.

[45]  J. Arvidsson,et al.  Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin , 1988, The Journal of comparative neurology.

[46]  W. M. Panneton Trigeminal mediation of the diving response in the muskrat , 1991, Brain Research.

[47]  A. Loewy,et al.  A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections , 1989, Brain Research.

[48]  W. M. Panneton,et al.  Trigeminal projections to the peribrachial region in the muskrat , 1994, Neuroscience.

[49]  H. Hayashi,et al.  Physiological properties of sensory neurons of the interstitial nucleus in the spinal trigeminal tract , 1989, Experimental Neurology.

[50]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[51]  Cechetto Df,et al.  Central representation of visceral function. , 1987 .

[52]  D. Reis,et al.  Phenylethanolamine N-methyltransferase-containing terminals synapse directly on sympathetic preganglionic neurons in the rat , 1988, Brain Research.

[53]  G. Allen,et al.  Trigeminal-parabrachial connections: possible pathway for nociception-induced cardiovascular reflex responses , 1996, Brain Research.

[54]  J. T. Hackett,et al.  Sympathoexcitatory neurons of rostral ventrolateral medulla exhibit pacemaker properties in the presence of a glutamate-receptor antagonist , 1988, Brain Research.

[55]  A. Light,et al.  Spinal cord and trigeminal projections to the pontine parabrachial region in the rat as demonstrated with Phaseolus vulgaris leucoagglutinin , 1994, The Journal of comparative neurology.

[56]  M. Daly,et al.  Reflex respiratory and cardiovascular effects of stimulation of receptors in the nose of the dog , 1972, The Journal of physiology.

[57]  C. Saper,et al.  Direct projections from the A5 catecholamine cell group to the intermediolateral cell column , 1979, Brain Research.

[58]  B. Johansson Circulatory responses to stimulation of somatic afferents with special reference to depressor effects from muscle nerves. , 1962, Acta physiologica Scandinavica. Supplementum.

[59]  A. Loewy,et al.  Decreases in blood pressure in response to L-Glutamate microinjections into the A5 catecholamine cell group , 1982, Brain Research.