Abstract
The location of neurons in the caudal medulla oblongata that project to the superficial or deep dorsal horn was studied in the rat, by means of retrograde labelling from confined spinal injection sites. The tracer cholera toxin subunit B was injected into laminae I–III (fuve rats) or I–V (three rats) at C4–7 spinal segments. Neurons projecting to the superficial dorsal horn were located in the dorsomedial part of the dorsal reticular nucleus ipsilaterally, the subnucleus commissuralis of the nucleus tractus solitarius bilaterally, and a region occupying the lateralmost part of the ventrolateral reticular formation between the lateral reticular nucleus and the caudal pole of the spinal trigeminal nucleus, pars caudalis, bilaterally. Neurons projecting to the deep dorsal horn, which were only labelled when laminae I–V were filled by the tracer, occurred in the dorsomedial and ventrolateral parts of the dorsal reticular nucleus and in the ventral reticular nucleus bilaterally. A few cells were located in the above described lateralmost portion of the ventrolateral reticular formation bilaterally and in the ventral portion of the ipsilateral cuneate nucleus. In the light of previous data demonstrating that dorsal horn neurons project to the dorsal reticular nucleus, the ventrolateral reticular formation, and the nucleus tractus solitarius, and that neurons in these three medullary regions are involved in pain inhibition at the spinal level, the descending projections demonstrated here suggest the occurrence of spino-medullary-spinal loops mediating the analgesic actions elicited in each nucleus upon the arrival of nociceptive input from the dorsal horn.
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Aicher SA, Randich A (1990) Antinociception and cardiovascular responses produced by electrical stimulation in the nucleus tractus solitarius, nucleus reticularis ventralis and the caudal medulla. Pain 42:103–119
Almeida A, Tavares I, Lima D, Coimbra A (1993) Descending projections from the medullary dorsal reticular nucleus make synaptic contacts with spinal cord lamina I cells projecting to that nucleus: an electron microscopic tracer study in the rat. Neuroscience 55:1093–1106
Andrezik JA, Beitz AJ (1985) Reticular formation, central grey and related tegmental nuclei. In: Paxinos G (eds) The rat nervous system, vol. II. Academic, Sydney, pp 1–28
Bandler R, Tork I (1987) Midbrain periaqueductal grey region in the cat has afferent and efferent connections with solitary tract nuclei. Neurosci Lett 74:1–6
Basbaum AI, Fields H (1984) Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7:309–338
Beitz AJ (1982) The nuclei of origin of brain stem enkephalin and substance P projections to the rodent nucleus raphe magnus. Neuroscience 7:2753–2768
Bernard JF, Villanueva L, Carroué J, Le Bars D (1990) Efferent projections from the subnucleus reticularis dorsalis (SRD): a Phaseolus vulgaris leucoagglutinin study in the rat. Neurosci Lett 116:257–262
Bouhassira D, Villanueva L, Bing Z, Le Bars D (1992) Involvement of subnucleus reticularis dorsalis in diffuse noxious inhibitory controls in the rat. Brain Res 595:353–357
Burton H, Loewy AD (1977) Projections to the spinal cord from medullary somatosensory relay nuclei. J Comp Neurol 173:773–792
Burton H, Craig AD, Poulos DA, Molt JT (1979) Efferent projections from temperature sensitive recording loci within the marginal zone of the nucleus caudalis of the spinal trigeminal complex in the cat. J Comp Neurol 183:753–778
Cervero F, Iggo A, Ogawa H (1976) Nociceptor-driven dorsal horn neurones in the lumbar spinal cord of the cat. Pain 2:5–24
Christensen B, Perl ER (1970) Spinal neurones specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J Neurophysiol 33:293–307
Clements JR, Magnusson KR, Beitz AJ (1990) Ultrastructural description of glutamate-, aspartate-, taurine-, and glycine-like immunoreactive terminals from five rat brain regions. J Electron Microsc Tech 15:49–66
Colonnier M (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9:268–287
Donovick JP (1974) A metachromatic stain for neural tissue. Stain Technol 49:49–51
Du H-J, Zhou S-Y (1990) Involvement of solitary tract nucleus in control of nociceptive transmission in cat spinal cord neurons. Pain 40:323–331
Eccles JC (1964) The physiology of synapses. Springer, Berlin Heidelberg New York
Ericson H, Blomqvist A (1988) Tracing of neuronal connections with cholera toxin subunit B: light and electron microscopic immunohistochemistry using monoclonal antibodies. J Neurosci Methods 24:225–235
Esteves F, Lima D, Coimbra A (1993) Structural types of spinal cord marginal (lamina I) neurons projecting to the nucleus of the tractus soiltarius in the rat. Somatosens Mot Res 10:203–216
Fleetwood-Walker SM, Coote JH, Gibley MP (1983) Identification of spinally projecting neurones in the A1 catecholamine cell group of the ventrolateral medulla. Brain Res 273:25–33
Gebhart GF, Ossipov M (1986) Characterization of inhibition of the nociceptive tail-flick reflex in the rat from the medullary lateral reticular nucleus. J Neurosci 6:701–713
Gray EG (1969) Electron microscopy of excitatory and inhibitory synapses: a brief review. Brain Res 31:141–156
Hall JG, Duggan AW, Morton CR, Johnson SM (1983) The location of brainstem neurones tonically inhibiting dorsal horn neurones of the cat. Brain Res 244:215–222
Janss AJ, Gebhart GF (1987) Spinal monoaminergic receptors mediate the antinociception produced by glutamate in the medullary lateral reticular nucleus. J Neurosci 7:2862–2873
Janss AJ, Gebhart GF (1988) Quantitative characterization and spinal pathway mediating inhibition of spinal nociceptive transmission from the lateral reticular nucleus in the rat. J Neurophysiol 59:226–247
Kalia M, Fuxe K (1985) Rat medulla oblongata. I. Cytoarchitectonic considerations. J Comp Neurol 233:285–307
Kalia M, Fuxe K, Goldstein M (1985) Rat medulla oblongata. II. Dopaminergic, noradrenergic (A1 and A2) and adrenergic neurons, nerve fibers and presumptive terminal processes. J Comp Neurol 233:308–332.
Kneisley LW, Biber MP, LaVail JH (1978) A study of the origin of brainstem projections to monkey spinal cord using the retrograde transport method. Exp Neurol 60:116–139
Kumazawa T, Perl ER (1978) Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: indications of their place in dorsal horn functional organization. J Comp Neurol 177:417–434
Kuypers HGM, Maisky VA (1975) Retrograde axonal transport of horseradish peroxidase from spinal cord to brain stem cell groups in the cat. Neurosci Lett 1:9–14
Kwiat GC, Basbaum AI (1992) The origin of brainstem noradrenergic and serotoninergic projections to the spinal cord dorsal horn in the rat. Somatosens. Mot Res 9:157–173
Laird JMA, Cervero F (1989) A comparative study of the changes in receptive-field properties of multireceptive and nocicreceptive rat dorsal horn neurons following noxious mechanical stimulation. J Neurophysiol 62:854–863
LeBars D, Dickenson AH, Besson JM (1979a) Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 283–304
LeBars D, Dickenson AH, Besson JM (1979b) Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain 6:305–327
Leong SK, Shieh JY, Wong WC (1984) Localizing spinal-cordprojecting neurons in adult albino rats. J Comp Neurol 228:1–17
Lewis JW, Baldrighi G, Akil H (1987) A possible interface between autonomic function and pain control: opioid analgesia and the nucleus tractus solitarius. Brain Res 424:65–70
Lima D (1990) A spinomedullary projection terminating in the dorsal reticular nucleus of the rat. Neuroscience 34:577–589
Lima D, Coimbra A (1991) Neurons in the substantia gelatinosa rolandi (lamina II) project to the caudal ventrolateral reticular formation of the medulla oblongata in the rat. Neurosci Lett 132:16–18
Lima D, Mendes-Ribeiro J, Coimbra A (1991) The spino-lateroreticular system of the rat: projections from the superficial dorsal horn and structural characterization of marginal neurons involved. Neuroscience 45:137–152
Lima D, Esteves F, Coimbra A (1993) C-fos activation by noxious input of spinal neurons projecting to the nucleus of the tractus solitarius in the rat. Proceedings of the 7th World Congress of Pain (in press)
Liu RH, Jing-Shi T, Zong-Lian H (1989) Electrophysiological identification of spinally projecting neurons in the lateral reticular nucleus of the rat. Brain Res 481:350–355
Loewy AD, Burton H (1978) Nuclei of the solitary tract: efferent projections to the lower brain stem and spinal cord of the cat. J Comp Neurol 181:421–450
Masson RL, Sparkes ML, Ritz LA (1991) Descending projections to the rat sacrocaudal spinal cord. J Comp Neurol 307:120–130
McKellar S, Loewy AD (1982) Efferent projections of the A1 catecholamine cell group in the rat: an autoradiographic study. Prog Brain Res 241:11–29
Menétrey D, Basbaum AI (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
Menétrey D, Pommery J de (1991) Origins of ascending pathways that reach central areas involved in visceroreception and visceronociception in the rat. Eur J Neurosci 3:249–259
Menétrey D, Giesler GJ Jr, Besson JM (1977) An analysis of response properties of spinal cord dorsal horn neurones to non-noxious and noxious stimuli in the spinal rat. Exp Brain Res 27:15–33
Menétrey D, Roudier F, Besson JM (1983) Spinal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase. J Comp Neurol 220:439–452
Menétrey D, Pommery J de, Besson JM (1984) Electrophysiological characteristics of lumbar spinal cord neurons backfired from lateral reticular nucleus in the rat. J Neurophysiol 52:595–611
Menétrey D, Pommery J de, Thomasset M, Baimbridge KG (1992) Calbindin-D28 K (CaBP28 K)-like immunoreactivity in ascending projections. II. Spinal projections to brain stem and mesencephalic areas. Eur J Neurosci 4:70–76
Morgan MM, Sohn JH, Lohof AM, Ben-Eliyah S, Liebeskind JC (1989) Characterization of stimulation produced analgesia from the nucleus tractus solitarius in the rat. Brain Res 486:175–180
Morton CR, Johnson SM, Duggan AW (1983) Lateral reticular regions and the descending control of dorsal horn neurones of the cat: selective inhibition by electrical stimulation. Brain Res 275:13–21
Ness TJ, Gebhart GF (1989) Characterization of superficial T13-L2 dorsal horn neurons encoding for colorectal distension in the rat: comparison with neurons in deep laminae. Brain Res 486:301–309
Newman DB (1985) Distinguishing rat brainstem reticulospinal nuclei by their neuronal morphology. I. Medullary nuclei. J Hirnforsch 26:187–226
Norgren R (1978) Projections from the nucleus of the solitary tract in the rat. Neuroscience 3:207–218
Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic, Sydney
Randich A, Roose MG, Gebhart G F (1988) Characterization of antinociception produced by glutamate microinjection in the nucleus tractus soiltarius and the nucleus reticularis ventralis. J Neurosci 8:4675–4684
Ren K, Randich A, Gebhart GF (1990) Modulation of spinal nociceptive transmission from nuclei tractus solitarii: a relay for effects of vagal afferent stimulation. J Neurophysiol 63:971–986
Romagnano MAA, Harshbarger RJ, Hamill RW (1991) Brainstem enkephalinergic projections to spinal autonomic nuclei. J Neurosci 11:3539–3555
Satoh K, Tohyama M, Yamamoto K, Sakumoto T, Shimizu N (1977) Noradrenaline innervation of the spinal cord studied with monoamine oxidase method combined with monoamine oxidase staining. Exp Brain Res 30:175–186
Shupliakov O, Brodin L, Culheim S, Ottersen OP, Storm-Mathisen J (1992) Immunogold quantification of glutamate in two types of excitatory synapse with different firing patterns. J Neurosci 12:3789–3803
Smolen AJ, Glazer EJ, Ross LL (1979) Horseradish peroxidase histochepmmistry combined with glyoxylic acid-induced fluorescence used to identify brain stem catecholaminergic neurons which project to the chick thoracic spinal cord. Brain Res 160:353–357
Tavares I, Lima D, Coimbra A (1993) Neurons in the superficial dorsal horn of the rat spinal cord projecting to the medullary ventrolateral reticular formation express c-fos after noxious stimulation of the skin. Brain Res 623:278–286
Toyhama M, Sakai K, Salvert D, Touret M, Jouvet M (1979) Spinal projections from the lower brain stem in the cat as demonstrated by the horseradish peroxidase technique. I. Origins of the reticulospinal tracts and their funicular trajectories. Brain Res 173:383–403
Uchizono K (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the rat. Nature 207:642–643
Villanueva L, Bouhassira D, Bing Z, Le Bars D (1988) Convergence of heterotopic nociceptive information onto subnucleus reticularis dorsalis neurons in the rat medulla. J Neurophysiol 60:980–1009
Villanueva L, dePommery J, Menétrey D, Le Bars D (1991) Spinal afferent projections to subnucleus reticularis dorsalis in the rat. Neurosci Lett 134:98–102
Westlund KN, Bowker RM, Ziegler MG, Dan J (1981) Origins of spinal noradrenergic pathways demonstrated by retrograde transport of antibody to dopamine-β-hydroxylase. Neurosci Lett 25:243–249
Westlund KN, Bowker RM, Ziegler MG, Coulter JD (1983) Noradrenergic projections to the spinal cord of the rat. Brain Res 263:15–31
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Tavares, I., Lima, D. Descending projections from the caudal medulla oblongata to the superficial or deep dorsal horn of the rat spinal cord. Exp Brain Res 99, 455–463 (1994). https://doi.org/10.1007/BF00228982
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DOI: https://doi.org/10.1007/BF00228982