Descending projections from the rostral ventromedial medulla (RVM) to trigeminal and spinal dorsal horns are morphologically and neurochemically distinct

Journal of Chemical Neuroanatomy

Volumn 43, Issue 2, 2012, Pages 103-111

  Aicher, Sue A ^a   Hermes, Sam M ^a   Whittier, Kelsey L ^a   Hegarty, Deborah M ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Confocal microscopy; Descending modulation; Electron microscopy; GABA; GAD67

Indexed keywords

GLUTAMATE DECARBOXYLASE 67;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL ULTRASTRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; GABAERGIC TRANSMISSION; IMMUNOCYTOCHEMISTRY; INTERNEURON; MALE; NERVE CELL; NEUROANATOMY; NEUROCHEMISTRY; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; ROSTRAL VENTROMEDIAL MEDULLA; SPINAL CORD DORSAL HORN; TRIGEMINAL DORSAL HORN;

ANIMALS; BRAIN CHEMISTRY; GENE TARGETING; GLUTAMATE DECARBOXYLASE; MALE; MEDULLA OBLONGATA; POSTERIOR HORN CELLS; PYRAMIDAL TRACTS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TRIGEMINAL NERVE;

EID: 84860372688     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2011.11.002     Document Type: Article

References (45)

1. Aicher S.A., Goldberg A., Sharma S., Pickel V.M. μ-Opioid receptors are present in vagal afferents and their dendritic targets in the medial nucleus tractus solitarius. J. Comp. Neurol. 2000, 422:181-190.
2. Aicher S.A., Reis D.J., Nicolae R., Milner T.A. Monosynaptic projections from the medullary gigantocellular reticular formation to sympathetic preganglionic neurons in the thoracic spinal cord. J. Comp. Neurol. 1995, 363:563-580.
3. Alvarez F.J., Kavookjian A.M., Light A.R. Synaptic interactions between GABA-immunoreactive profiles and the terminals of functionally defined myelinated nociceptors in the monkey and cat spinal cord. J. Neurosci. 1992, 12:2901-2917.
4. Alvarez F.J., Kavookjian A.M., Light A.R. Ultrastructural morphology, synaptic relationships, and CGRP immunoreactivity of physiologically identified C-fiber terminals in the monkey spinal cord. J. Comp. Neurol. 1993, 329:472-490.
5. Antal M., Petkó M., Polgár E., Heizmann C.W., Storm-Mathisen J. Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla. Neuroscience 1996, 73:509-518.
6. 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.
7. Bereiter D.A., Hirata H., Hu J.W. Trigeminal subnucleus caudalis: beyond homologies with the spinal dorsal horn. Pain 2000, 88:221-224.
8. Bottger P., Tracz Z., Heuck A., Nissen P., Romero-Ramos M., Lykke-Hartmann K. Distribution of Na/K-ATPase alpha 3 isoform, a sodium-potassium P-type pump associated with rapid-onset of dystonia parkinsonism (RDP) in the adult mouse brain. J. Comp. Neurol. 2011, 519:376-404.
9. Chan J., Aoki C., Pickel V.M. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Methods 1990, 33:113-127.
10. Edelmayer R.M., Vanderah T.W., Majuta L., Zhang E.T., Fioravanti B., De F.M., Chichorro J.G., Ossipov M.H., King T., Lai J., Kori S.H., Nelsen A.C., Cannon K.E., Heinricher M.M., Porreca F. Medullary pain facilitating neurons mediate allodynia in headache-related pain. Ann. Neurol. 2009, 65:184-193.
11. Fang F., Proudfit H.K. Spinal cholinergic and monoamine receptors mediate the antinociceptive effect of morphine microinjected in the periaqueductal gray on the rat tail, but not the feet. Brain Res. 1996, 722:95-108.
12. Fields H.L., Basbaum A.I. Brainstem control of spinal pain-transmission neurons. Annu. Rev. Physiol. 1978, 40:217-248.
13. Fields H.L., Basbaum A.I., Clanton C.H., Anderson S.D. Nucleus raphe magnus inhibition of spinal cord dorsal horn neurons. Brain Res. 1977, 126:441-453.
14. Fields H.L., Bry J., Hentall I., Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J. Neurosci. 1983, 3:2545-2552.
15. Fields H.L., Malick A., Burstein R. Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla. J. Neurophysiol. 1995, 74:1742-1759.
16. Fong A.Y., Stornetta R.L., Foley C.M., Potts J.T. Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J. Comp. Neurol. 2005, 493:274-290.
17. Guo C., Hirano A.A., Stella S.L., Bitzer M., Brecha N.C. Guinea pig horizontal cells express GABA, the GABA-synthesizing enzyme GAD 65, and the GABA vesicular transporter. J. Comp. Neurol. 2010, 518:1647-1669.
18. Haber L.H., Martin R.F., Chung J.M., Willis W.D. Inhibition and excitation of primate spinothalamic tract neurons by stimulation in region of nucleus reticularis gigantocellularis. J. Neurophysiol. 1980, 43:1578-1593.
19. Hargreaves K.M. Orofacial pain. Pain 2011, 152:S25-S32.
20. Hegarty D.M., Tonsfeldt K., Hermes S.M., Helfand H., Aicher S.A. Differential localization of vesicular glutamate transporters and peptides in corneal afferents to trigeminal nucleus caudalis. J. Comp. Neurol. 2010, 518:3557-3569.
21. Heinricher M.M., Barbaro N.M., Fields H.L. Putative nociceptive modulating neurons in the rostral ventromedial medulla of the rat: firing of on- and off-cells is related to nociceptive responsiveness. Somatosens. Mot. Res. 1989, 6:427-439.
22. Heinricher M.M., Morgan M.M., Tortorici V., Fields H.L. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neuroscience 1994, 63:279-288.
23. Heusner C.L., Beutler L.R., Houser C.R., Palmiter R.D. Deletion of GAD67 in dopamine receptor-1 expressing cells causes specific motor deficits. Genesis 2008, 46:357-367.
24. Hsu S.M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 1981, 29:557-580.
25. Jones B.E., Holmes C.J., Rodriguez-Veiga E., Mainville L. GABA-synthesizing neurons in the medulla: their relationship to serotonin-containing and spinally projecting neurons in the rat. J. Comp. Neurol. 1991, 313:349-367.
26. Kalyuzhny A.E., Wessendorf M.W. Serotonergic and GABAergic neurons in the medial rostral ventral medulla express κ-opioid receptor immunoreactivity. Neuroscience 1999, 90:229-234.
27. Kato G., Yasaka T., KAtafuchi T., Furue H., Mizuno M., Iwamoto Y., Yoshimura M. Direct GABAergic and glycinergic inhibition of the substantia gelatinosa from the rostral ventromedial medulla revealed by in vivo patch-clamp analysis in rats. J. Neurosci. 2006, 26:1787-1794.
28. Light A.R., Kavookjian A.M. The ultrastructure and synaptic connections of the spinal terminations from single, physiologically characterized axons descending in the dorsolateral funiculus from the midline, pontomedullary region. J. Comp. Neurol. 1985, 234:549-560.
29. Meng I.D., Bereiter D.A. Differential distribution of Fos-like immunoreactivity in the spinal trigeminal nucleus after noxious and innocuous thermal and chemical stimulation of rat cornea. Neuroscience 1996, 72:243-254.
30. Meng I.D., Hu J.W., Bereiter D.A. Parabrachial area and nucleus raphe magnus inhibition of corneal units in rostral and caudal portions of trigeminal subnucleus caudalis in the rat. Pain 2000, 87:241-251.
31. Millan M.J. Descending control of pain. Prog. Neurobiol. 2002, 66:355-474.
32. Millhorn D.E., Ho:kfelt T., Seroogy K., Oertel W., Verhofstad A.A.J., Wu J.-Y. Immunohistochemical evidence for colocalization of gamma-aminobutyric acid and serotonin in neurons of the ventral medulla oblongota projecting to the spinal cord. Brain Res. 1987, 410:179-185.
33. Mitchell J.L., Silverman M.B., Aicher S.A. Rat trigeminal lamina I neurons that project to thalamic or parabrachial nuclei contain the mu-opioid receptor. Neuroscience 2004, 128:571-582.
34. Morgan M.M., Whittier K.L., Hegarty D.M., Aicher S.A. Periaqueductal gray neurons project to spinally projecting GABAergic neurons in the rostral ventromedial medulla. Pain. 2008, 140:376-386.
35. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
36. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates, 4th edition 1998, Elsevier/Academic Press, London.
37. Pickel, V.M., 1981. Immunocytochemical Methods, In: Heimer, L., Robards, M.J., eds. Neuroanatomical Tract Tracing Methods. New York, NY: Plenum Publishing; p. 483-509.
38. Pozo M.A., Cervero F. Neurons in the rat spinal trigeminal complex driven by corneal nociceptors: receptive-field properties and effects of noxious stimulation of the cornea. J. Neurophysiol. 1993, 70:2370-2378.
39. Ruda M.A., Bennett G.J., Dubner R. Neurochemistry and neural circuitry in the dorsal horn. Prog. Brain Res. 1986, 66:219-268.
40. Sandkühler J., Gebhart G.F. Characterization of inhibition of a spinal nociceptive reflex by stimulation medially and laterally in the midbrain and medulla in the pentobarbital-anesthetized rat. Brain Res. 1984, 305:67-76.
41. Silverman M.B., Hermes S.M., Zadina J.E., Aicher S.A. Mu-opioid receptor is present in dendritic targets of Endomorphin-2 axon terminals in the nuclei of the solitary tract. Neuroscience 2005, 135:887-896.
42. Strassman A.M., Vos B.P. Somatotopic and laminar organization of fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J. Comp. Neurol. 1993, 331:495-516.
43. Urban M.O., Zahn P.K., Gebhart G.F. Descending facilitatory influences from the rostral medial medulla mediate secondary, but not primary hyperalgesia in the rat. Neuroscience 1999, 90:349-352.
44. Winkler C.W., Hermes S.M., Chavkin C.I., Drake C.T., Morrison S.F., Aicher S.A. Kappa opioid receptor (KOR) and GAD67 immunoreactivity are found in OFF and NEUTRAL cells in the rostral ventromedial medulla. J. Neurophysiol. 2006, 96:3465-3473.
45. Zhuo M., Gebhart G.F. Characterization of descending inhibition and facilitation from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Pain 1990, 42:337-350.