Brain afferents to the medullary dorsal reticular nucleus: A retrograde and anterograde tracing study in the rat

European Journal of Neuroscience

Volumn 16, Issue 1, 2002, Pages 81-95

  Almeida, Armando ^a,b   Cobos, Angeles ^c   Tavares, Isaura ^a   Lima, Deolinda ^a  

^a Inst of Pharmacol and Therapeutics   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Amygdala; Antinociceptive system; Extrapyramidal system; Hypothalamus; Pain modulation; Prefrontal cortex; Sensorimotor cortex

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN NUCLEUS; BRAIN STEM; CELL ACTIVITY; CHEMICAL LABELING; CONTROLLED STUDY; DIENCEPHALON; MALE; MEDULLA OBLONGATA; MEDULLARY DORSAL RETICULAR NUCLEUS; MESENCEPHALON; NERVE PROJECTION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; RED NUCLEUS; RETROGRADE NERVE FIBER TRANSPORT; SENSORY NERVE; SOLITARY TRACT NUCLEUS; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS; TRIGEMINAL NUCLEUS;

AFFERENT PATHWAYS; ANIMALS; CEREBELLUM; DIENCEPHALON; HISTOLOGICAL TECHNIQUES; MALE; MEDULLA OBLONGATA; MESENCEPHALON; PAIN; PONS; RATS; RATS, WISTAR; TELENCEPHALON;

EID: 0036458809     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02058.x     Document Type: Article

References (82)

1. Allen, G.V. & Cechetto, D.F. (1992) Functional and anatomical organization of cardiovascular pressor and depressor sites in the lateral hypothalamic area. I. Descending projections. J. Comp. Neurol., 315, 313-332.
2. Almeida, A. & Lima, D. (1997) Activation by cutaneous or visceral noxious stimulation of spinal neurons projecting to the medullary dorsal reticular nucleus in the rat: A c-fos study. Eur. J. Neurosci., 9, 686-695.
3. Almeida, A., Storkson, R., Lima, D., Hole, K. & Tjolsen, A. (1999a) The medullary dorsal reticular nucleus facilitates pain behaviour induced by formalin in the rat. Eur. J. Neurosci., 11, 110-122.
4. Almeida, A., Cobos, A. & Lima, D. (1999b) Brain afferents to the medullary dorsal reticular nucleus. A CTb retrograde tracing study in the rat [Abstract]. 9th World Congress on Pain (Vienna, 1999), 172.
5. Almeida, A., Tavares, I. & Lima, D. (1995) Projection sites of superficial or deep dorsal horn in the dorsal reticular nucleus. Neuroreport, 6, 1245-1248.
6. Almeida, A., Tavares, I. & Lima, D. (2000) Reciprocal connections between the medullary dorsal reticular nucleus and the spinal dorsal horn in the rat. Eur. J. Pain, 4, 373-387.
7. 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.
8. Almeida, A., Tjolsen, A., Lima, D., Coimbra, A. & Hole, K. (1996) The medullary dorsal reticular nucleus facilitates acute nociception in the rat. Brain Res. Bull., 39, 7-15.
9. Angelucci, A., Clascá, F. & Sur, M. (1996) Anterograde axonal tracing with the subunit B of cholera toxin: A highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains. J. Neurosci. Meth., 65, 101-112.
10. Basbaum, A.I. & Fields, H.L. (1984) Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci., 7, 309-338.
11. Berendse, H.W. & Groenewegen, H.J. (1990) Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J. Comp. Neurol., 299, 187-228.
12. Bian, D., Ossipov, M.H., Malan,T.P. Jr & Porreca, F. (1998) Tactile allodynia, but not thermal hyperalgesia, of the hindlimbs is blocked by spinal transection in rats with nerve injury. Neurosci. Lett., 241, 79-82.
13. Bouhassira, D., Villanueva, L., Bing, Z. & Le Bars, D. (1992) Involvement of the subnucleus reticularis dorsalis in diffuse noxious inhibitory controls in the rat. Brain Res., 595, 353-357.
14. Cervero, F., Schaible, H.G. & Schmidt, R.F. (1991) Tonic descending inhibition of spinal cord neurons driven by joint afferents in normal cats and in cats with inflamed knee-joint. Expl. Brain Res., 83, 675-678.
15. Chen, S. & Aston-Jones, G. (1996) Extensive projections from the midbrain periaqueductal gray to the caudal ventrolateral medulla: A retrograde and anterograde tracing study in the rat. Neuroscience, 71, 443-459.
16. Desbois, C., Le Bars, D. & Villanueva, L. (1999) Organization of cortical projections to the medullary subnucleus reticularis dorsalis: A retrograde and anterograde tracing study in the rat. J. Comp. Neurol., 410, 178-196.
17. Desbois, C. & Villanueva, L. (2001) The organization of lateral ventromedial thalamic connections in the rat: A link for the distribution of nociceptive signals to widespread cortical regions. Neuroscience, 102, 885-898.
18. Donoghue, J.P. & Parham, C. (1983) Afferent connections of the lateral agranular field of the rat motor cortex. J. Comp. Neurol., 217, 390-404.
19. Donovick, P.J. (1974) A metachromatic stain for neural tissue. Stain Technol., 49, 49-51.
20. Dugast, C., Almeida, A. & Lima, D. (2000) The medullary dorsal reticular nucleus (DRt) increases the response of lumbar nociceptive neurons to electrical stimulation. Soc. Neurosci. Abstr., 26, 652.
21. Dugast, C., Almeida, A. & Lima, D. (2001) Wind-up of spinal cord wide-dynamic-range neurons is influenced by the medullary dorsal reticular nucleus. Soc. Neurosci. Abstr., 27, 171.1.
22. Esser, M.J., Pronych, S.P. & Allen, G.V. (1998) Trigeminal-reticular connections: possible pathways for nociception-induced cardiovascular reflex responses in the rat. J. Comp. Neurol., 391, 526-544.
23. Fasmer, O.B., Berge, O.G., Tveiten, L. & Hole, K. (1986) Changes in nociception after 6-hydroxydopamine lesions of the descending catecholaminergic pathways in mice. Pharmacol. Biochem. Behav., 24, 1441-1444.
24. Fields, H.L. & Basbaum, A.I. (1999) Central nervous system mechanisms of pain modulation. In Wall, P.D. & Melzack, C. (eds), Textbook of Pain, 4th Edn. Churchill Livingstone, New York, pp. 309-329.
25. Fields, H.L., Bry, J., Hentall, I. & Zorman, G. (1983) The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J. Neurosci., 3, 2545-2552.
26. Fritschy, J.-M. & Grzanna, R. (1990) Distribution of locus coeruleus axons within the rat brainstem demonstrated by Phaseolus vulgaris leucoagglutinin anterograde tracing in combination with dopamine-β-hydroxylase immunofluorescence. J. Comp. Neurol., 293, 616-631.
27. Gebhart, G.F. & Randich, A. (1990) Brainstem modulation of nociception. In Klemm, W.R. & Vertes, R.P. (eds), Brainstem Mechanisms of Behavior. John Wiley & Sons, New York, pp. 315-352.
28. Hammond, D.L. (1986) Control systems for nociceptive afferent processing; the descending inhibitory pathways. In Yaksh, T.L. (ed.), Spinal Afferent Processing. Plenum Press, New York, pp. 363-390.
29. Herbert, H., Moga, M.M. & Saper, C.B. (1990) Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol., 293, 540-580.
30. Herkenham, M. (1979) The afferent and efferent connections of the ventromedial thalamic nucleus in the rat. J. Comp. Neurol., 183, 487-518.
31. Jones, S.L. (1992) Descending control of nociception. In Light, A.R. (ed.), The Initial Processing of Pain and its Descending Control.: Spinal and Trigeminal Systems. Karger, New York, pp. 203-295.
32. Jones, B.E. & Yang, T.-Z. (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J. Comp. Neurol., 242, 56-92.
33. Kauppila, T., Kontinen, V.K. & Pertovaara, A. (1998) Influence of spinalization on spinal withdrawal reflex responses varies depending on the submodality of the test stimulus and the experimental pathophysiological condition in the rat. Brain Res., 797, 234-242.
34. Kovelowski, C.J., Ossipov, M.H., Sun, H., Lai, J., Malan,T.P. Jr & Porreca, F. (2000) Supraspinal cholecystokinin may drive tonic descending facilitation mechanisms to maintain neuropathic pain in the rat. Pain, 87, 265-273.
35. Krukoff, T.L., Harris, K.H. & Jhamandas, J.H. (1993) Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Res. Bull., 30, 163-172.
36. Lima, D. (1990) A spinomedullary projection terminating in the dorsal reticular nucleus of the rat. Neuroscience, 34, 577-589.
37. Lima, D. (1998) Anatomical basis for the dynamic processing of nociceptive input. Eur. J. Pain, 2, 195-202.
38. Lima, D. & Almeida, A. (2002) The medullary dorsal reticular nucleus as a pronociceptive centre of the pain control system. Prog. Neurobiol., 66, 81-108.
39. Lima, D. & Coimbra, A. (1988) The spinothalamic system of the rat: Structural types of retrogradely labelled neurons in the marginal zone (lamina I). Neuroscience, 27, 215-230.
40. Lima, D., Mendes-Ribeiro, J.A. & Coimbra, A. (1991) The spino-latero-reticular system of the rat: Projections from the superficial dorsal horn and structural characterization of marginal neurons involved. Neuroscience, 45, 137-152.
41. Loewy, A.D. (1990) Central autonomic pathways. In Loewy, A.D. & Spyer, K.M. (eds), Central Regulation of Autonomic Functions. Oxford University Press, New York, pp. 88-103.
42. Lopes-da-Silva, F.H., Witter, M.P., Boeijinga, P.H. & Lohman, A.M. (1990) Anatomic organization and physiology of the limbic cortex. Physiol. Rev., 70, 453-511.
43. Luiten, P.G.M., Ter Horst, G.J. & Steffens, A.B. (1985) The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Res., 329, 374-378.
44. Luppi, P.H., Fort, P. & Jouvet, M. (1990) Iontophoretic application of unconjugated cholera toxin B subunit (CTb) combined with immunocytochemistry of neurochemical substances: A method for transmitter identification of retrogradely labeled neurons. Brain Res., 534, 209-224.
45. Martin, W.J., Gupta, N.K., Loo, C.M., Rohde, D.S. & Basbaum, A.I. (1999) Differential effects of neurotoxic destruction of descending noradrenergic pathways on acute and persistent nociceptive processing. Pain, 80, 57-65.
46. McKellar, S. & Loewy, A.D. (1982) Efferent projections of the A1 catecholamine cell group in the rat: An autoradiographic study. Brain Res., 241, 11-29.
47. McNally, G.P. (1999) Pain facilitatory circuits in the mamalian central nervous system: Their behavioral significance and role in morphine analgesic tolerance. Neurosci. Biobehav. Rev., 23, 1059-1078.
48. Melzack, R. & Casey, K.L. (1968) Sensory, motivational, and central control determinants of pain. A new conceptual model. In Kenshalo, D.R. (ed.), The skin senses. Thomas, Springfield, pp. 423-443.
49. Millan, M.J. (1999) The induction of pain: an integrative review. Prog. Neurobiol., 57, 1-164.
50. Monconduit, L., Bourgeais, L., Bernard, J.-F., Le Bars, D. & Villanueva, L. (1999) Ventromedial thalamic neurons convey nociceptive signals from the whole body surface to the dorsolateral neocortex. J. Neurosci., 15, 9063-9072.
51. Ness, T.J., Fillingim, R.B., Randich, A., Backensto, E.M. & Faught, E. (2000) Low intensity vagal stimulation lowers human thermal pain thresholds. Pain, 86, 81-85.
52. Odeh, F. & Antal, M. (2001) The projections of the midbrain periaqueductal grey to the pons and medulla oblongata in rats. Eur. J. Neurosci., 14, 1275-1286.
53. Ottersen, O.P. & Ben-Ari, Y. (1979) Afferent connections to the amygdaloid complex of the rat and cat. J. Comp. Neurol., 187, 401-424.
54. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd Edn. Academic Press, New York.
55. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th Edn. Academic Press, New York.
56. Proudfit, H.K. & Hammond, D.L. (1981) Alterations in nociceptive threshold and morphine-induced analgesia produced by intrathecally administered amine antagonists. Brain Res., 218, 393-399.
57. Ren, K., Randich, A. & Gebhart, G.F. (1990) Modulation of spinal nociceptive transmission from nuclei tractus solitarii: A relay for effects of vagal afferent stimulation. J. Neurophysiol., 63, 971-986.
58. Roy, J.-C., Bing, Z., Villanueva, L. & Le Bars, D. (1992) Convergence of visceral and somatic inputs onto subnucleus reticularis dorsalis neurones in the rat medulla. J. Physiol. (Lond.), 458, 235-246.
59. Saper, C.B. & Loewy, A.D. (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res., 197, 291-317.
60. Schaible, H.G., Neugebauer, V., Cervero, F. & Schmidt, R.F. (1991) Changes in tonic descending inhibition of spinal neurons with articular input during the development of acute arthritis in the cat. J. Neurophysiol., 66, 1021-1032.
61. Shepherd (1990) The Synaptic Organization of the Brain. Oxford University Press, London.
62. Su, H.-S. & Bentivoglio, M. (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J. Comp. Neurol., 297, 582-593.
63. Swanson, L.W. (1998) Brain Maps: Structure of the Rat Brain. Elsevier, New York.
64. 5 noradrenergic cells which project to the spinal cord dorsal horn are reciprocally connected with the caudal ventrolateral medulla in the rat. Eur. J. Neurosci., 9, 2452-2461.
65. Teune, T.M., van der Burg, J., van der Moer, J., Voogd, J. & Ruigrok, T.J. (2000) Topography of cerebellar nuclear projections to the brain stem in the rat. Prog. Brain Res., 124, 141-172.
66. Tjølsen, A., Berge, O.-G. & Hole, K. (1991) Lesions of bulbo-spinal serotonergic or noradrenergic pathways reduce nociception as measured by the formalin test. Acta Physiol. Scand., 142, 229-236.
67. Todd, A.J. & Spike, R.C. (1993) Localization of classical neurotransmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog. Neurobiol., 41, 609-645.
68. Urban, M.O. & Gebhart, G.F. (1999) Supraspinal contributions to hyperalgesia. Proc. Natl. Acad. Sci., 96, 7687-7692.
69. Veazey, R.B. & Severin, C.M. (1980) Efferent projections of the deep mesencephalic nucleus (pars medialis) in the rat. J. Comp. Neurol., 190, 245-258.
70. Veenman, C.L., Reiner, A. & Honig, M.G. (1992) Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J. Neurosci. Meth., 41, 239-254.
71. Villanueva, L., Bernard, J.F. & Le Bars, D. (1995) Distribution of spinal cord projections from the medullary subnucleus reticularis dorsalis and the adjacent cuneate nucleus: A Phaseolus vulgaris-leucoagglutinin study in the rat. J. Comp. Neurol., 352, 11-32.
72. Villanueva, L., Bing, Z., Bouhassira, D. & Le Bars, D. (1989) Encoding of electrical, thermal, and mechanical noxious stimuli by subnucleus reticularis dorsalis neurons in the rat medulla. J. Neurophysiol., 61, 391-402.
73. 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.
74. Villanueva, L., Desbois, C., Le Bars, D. & Bernard, J.-F. (1997) Organization of diencephalic projections from the medullary subnucleus reticularis dorsalis and the adjacent cuneate nucleus: A retrograde and anterograde tracer study in the rat. J. Comp. Neurol., 390, 133-160.
75. Wei, F., Dubner, R. & Ren, K. (1999) Nucleus gigantocellularis and nucleus raphe magnus in the brain stem exert opposite effects on behavioral hyperalgesia and spinal fos protein expression after peripheral inflammation. Pain, 80, 127-141.
76. Westlund, K.N. & Coulter, J.D. (1980) Descending projections of the locus coeruleus and subcoeruleus/medial parabrachial nuclei in monkey: Axonal transport studies and dopamine-beta-hydroxylase immunocytochemistry. Brain Res., 2, 235-264.
77. Woodson, W. & Angaut, P. (1984) The distribution and origin of the ipsilateral descending limb of the brachium conjunctivum. An autoradiographic and horseradish peroxidase study in the rat. Expl. Brain Res., 56, 167-182.
78. Wouterlood, F.G. & Jorritsma-Byham, B. (1993) The anterograde neuroanatomical tracer biotinylated dextran-amine: Comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. J. Neurosci. Meth., 48, 75-87.
79. Yaksh, T.L. (1985) Pharmacology of spinal adrenergic systems which modulate spinal nociceptive processing. Pharmacol. Biochem. Behav., 22, 845-858.
80. Zhuo, M. & Gebhart, G.F. (1992) Characterization of descending facilitation and inhibition of spinal nociceptive transmission from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. J. Neurophysiol., 67, 1599-1614.
81. Zhuo, M. & Gebhart, G.F. (1997) Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat. J. Neurophysiol., 78, 746-758.
82. Zimmermann, M. (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain, 16, 109-110.