Evidence of γ-aminobutyric acidergic control over the catecholaminergic projection from the medulla oblongata to the central nucleus of the amygdala

Journal of Comparative Neurology

Volumn 381, Issue 3, 1997, Pages 262-281

  Jia, Hong Ge ^a,b   Rao, Zhi Ren ^a   Shi, Ji Wu ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

nucleus of the solitary tract; synapse; tyrosine hydroxylase; ventrolateral medulla; aminobutyric acid

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; CATECHOLAMINE NERVE CELL; ELECTRON MICROSCOPY; FEMALE; GABAERGIC SYSTEM; IMMUNOCYTOCHEMISTRY; MALE; MEDULLA OBLONGATA; MICROSCOPY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0030891407     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970512)381:3<262::AID-CNE2>3.0.CO;2-0     Document Type: Article

References (64)

1. Beaulieu, C., and P. Somogyi (1991) Enrichment of cholinergic synaptic terminals on neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J. Comp. Neurol. 304:666-680.
2. Broman, J., and O.P. Ottersen (1992) Cervicothalamic tract terminals are enriched in glutamate-Iike immunoreactivity: an electron microscopic double-labelling study in the cat. J. Neurosci. 12:204-215.
3. Cassell, M.D., T.S. Gray, and J.Z. Kiss (1986) Neuronal architecture in the rat central nucleus of the amygdala: A cytological, hodological and immunocytochemical study. J. Comp. Neurol. 246:478-499.
4. Chen, L.W., Z.R. Rao, and J.W. Shi (1994) Visceral noxious stimulation induced Fos expression of catecholaminergic neurons in the "medullary visceral zone" projecting to the central amygdaloid nucleus. Chin. J. Neuroanat. 10:139-144.
5. Cohen, R.S., R.K. Carlin, D.J. Grab, and P. Siekevitz (1982) Phosphoproteins on postsynaptic densities. Progr. Brain Res. 56:49-76.
6. Cox, G.E., D. Jordan, P. Moruzzi, J.S. Schwaber, K.M. Spyer, and S.A. Turner (1986) Amygdaloid influence on brain-stem neurons in the rabbit. J. Physiol. 381-135-148.
7. Dahlström, A., and K. Fuxe (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand. 62(Suppl. 232):1-55.
8. Davis, M., D. Rainnie, and M.D. Cassell (1994) Neurotransmission in the rat amygdala related to fear and anxiety. TINS 17:208-214.
9. Dong, Y.X., K.H. Xiong, Z.R. Rao, and J.W. Shi (1996) Catecholaminergic neurons in medullary projecting to the paraventricular nucleus of the hypothalamus displaying Fos expression to visceral noxious stimulation of stomach in the rat. Acta Anat. Sin. 27:20-25.
10. Gray, T.S., and D.J. Magnuson (1987) Neuropeptide neuronal efferents from the bed nucleus of the stria terminals and central amygdaloid nucleus to the dorsal vagal complex in the rat. J. Comp. Neurol. 262:365-374.
11. Groenewegen, H.J., and F.G. Wouterlood (1990) Light and electron microscopic tracing of neuronal connections with Phaseolus vulgaris-leucoagglutinin (PHA-L), and combinations with other neuroanatomical techniques. In F.G. Wouterlood and A.N. van der Pol (eds): Analysis of Neuronal Microcircuits and Synaptic Interactions. Handbook of Chemical Neuroanatomy, Vol. 8. Amsterdam: Elsevier, pp. 47-124.
12. Han, Z.A., Z.R. Rao, H.M. Li, and J.W. Shi (1996) Visceral noxious stimulation induced Fos expression in catecholaminergic neurons of the medulla projecting to the bed nucleus of the stria terminalis in the rat. Chin. J. Neuroanat. 12:51-56.
13. Harper, R.M., R.C. Frysinger, R.B. Trelease, and J.D. Mark (1984) State-dependent alteration of respiratory cycle timing by stimulation of the central nucleus of the amygdala. Brain Res. 306:1-8.
14. Helmstetter, F.J., P.S. Bellgowan, and S.A. Tershner (1993) Inhibition of the tail flick reflex following microinjection of morphine into the amygdala. Neuroreport 4:471-474.
15. Hyden, H., and A. Cupello (1987) Inhibition in the mammalian brain: A new theory of GABA mechanism of action. Acta Physiol. Scand. 130(Suppl. 561):1-73.
16. Jia, H.G., Z.R. Rao, and J.W. Shi (1992a) Tyrosine-hydroxylase-containing neurons in the nucleus of the solitary tract send projection fibers to the central and basolateral amygdaloid nuclei. Chin. J. Neuroanat. 8:233-237.
17. Jia, H.G., Z.R. Rao, and J.W. Shi (1992b) Projection from the ventrolateral medullary neurons containing tyrosine hydroxylase to the central amygdaloid nucleus in the rat. Brain Res. 589:167-170.
18. Jia, H.G., Z.R. Rao, and J.W. Shi (1994a) The parabrachial neurons receive both visceral input from the nucleus tractus solitarii and GABAergic input from the central amygdaloid nucleus in the rat. Chin. J. Neuroanat. 10:299-303.
19. Jia, H.G., Z.R. Rao, and J.W. Shi (1994b) An indirect projection from the nucleus of the solitary tract to the central nucleus of the amygdala via the parabrachial nucleus in the rat: a light and electron microscopic study. Brain Res. 663:181-190.
20. Jia, H.G., Zhi-Ren Rao, and J.W. Shi (1994c) Evidence of GABAergic control over the catecholaminergic projection from the medulla oblongata to the central nucleus of the amygdala. Chin. J. Anat. Suppl. 17:201.
21. Jia, H.G., B.R. Wang, Z.R. Rao, J.W. Shi, R. Shigemoto, T. Kaneko, and N. Miznuo (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.
22. Jin, G.R., Z.R. Rao, and J.W. Shi (1994) Visceral noxious stimulation induced expression of Fos protein in medullary catecholaminergic neurons projecting to nucleus accumbens in the rat: a study with triple labeling method of HRP tracing combined with Fos and TH immunohistochemistry. Brain Res. 648:196-202.
23. Kalia, M., and J.M. Sullivan (1982) Brainstem projections of sensory and motor components of the vagus nerve in the rat. J. Comp. Neurol. 277:248-264.
24. Kalia, M., K. Fuxe, and M. Goldstein (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.
25. Kapp, B.S., M. Gallagher, M.D. Underwood, C.L. McNall, and D. Whitehorn (1982) Cardiovascular responses elicited by electrical stimulation of the amygdala central nucleus in the rabbit. Brain Res. 234:251-262.
26. Kapp, B.S., C.G. Markgraf, J.S. Schwaber, and T. Bilyk-Spafford (1989) The organization of dorsal medullary projections to the central amygdaloid nucleus and parabrachial nuclei in the rabbit. Neuroscience 30:717-732.
27. Liang, F.Y., and X.C. Wan (1989) Improvement of the tetramethyl benzidine reaction with ammonium molybdate as a stabilizer for light and electron microscopic ligand-HRP neurohistochemistry and double-labeling. J. Neurosci. Methods 28:150-162.
28. Livingston, C.A., and A.J. Berger (1989) Immunocytochemical localization of GABA neurons projecting to the ventrolateral nucleus of the solitary tract. Brain Res. 494:143-150.
29. Maskati, H.A.A., and A.W. Zbroayma (1989) Cardiovascular and motor components of the defense reaction elicited in rats by electrical and chemical stimulation in amygdala. J. Auton. Nerv. Syst. 28:127-132.
30. Meeley, M.P., D.A. Ruggiero, T. Ishitsuka, and D.J. Reis (1985) Intrinsic gamma-aminobutyric acid neurons in the nucleus of the solitary tract and rostral ventrolateral medulla of the rat: An immunocytochemical and biochemical study. Neurosci. Lett. 58:83-89.
31. Milner, T.A., V.M. Pickel, J. Chan, V.J. Massari, W.H. Oertel, D.H. Park, T.H. Joh, and D.J. Reis (1987) Phenylethanolamine N-methyltransferase-containing neurons in the rostral ventrolateral medulla. II. Synaptic relationship with GABAergic terminals. Brain Res. 477:46-57.
32. Mugnaini, E., and W.H. Oertel (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In A. Björklund, and T. Hökfelt (eds): Handbook of Chemical Neuroanatomy Vol. 4: GABA and Neuropeptides in the CNS. Part 1. Amsterdam: Elsevier, pp. 436-622.
33. Nitecka, L., and Y. Ben-Ari (1987) Distribution of GABA-like immunoreactivity in the rat amygdaloid complex. J. Comp. Neurol. 266:45-55.
34. Oertel, W.H., and E. Mugnaini (1984) Immunocytochemical studies of GABAergic neurons in the rat basal ganglia and their relations to other neuronal system. Neurosci. Lett. 47:233-238.
35. Oertel, W.H., G. Reithmuller, E. Mugnaini, D.E. Schmechel, A. Weindl, C. Gramsch, and A. Herz (1983) Opioid peptide-like immunoreactivity localized in GABAergic neurons of rat neostriatum and central amygdaloid nucleus. Life Sci. 33(Suppl I):73-76.
36. Onai, T., M. Saji, and M. Piura (1987) Functional subdivisions of the nucleus tractus solitarii of the rat as determined by circulatory and respiratory responses to electrical stimulation of the nucleus. J. Auton. Nerv. Syst. 27:195-202.
37. Otake, K., Y. Nakamura, and K. Ezure (1993) Projections from the commissural subnucleus of the solitary tract onto catecholamine cell groups of the ventrolateral medulla. Neurosci. Lett. 149:213-216.
38. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. 2nd Ed. Sydney: Academic Press.
39. Peters, A., S.L. Palay, and H.D. Webster (1991) Synapses. In: The Fine Structure of the Nervous System: Neurons and Their Supporting Cells, 3nd Ed. London: Oxford University Press, pp. 138-211.
40. Phend, K.D., R.J. Weinberg, and A. Rustioni (1992) Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J. Histochem. Cytochem. 40:1011-1020.
41. Pickel, V.M., J. Chan, and T.A. Milner (1989) Cellular substrates for interactions between neurons containing phenylethanolamine N-methyhransferase and GABA in the nuclei of the solitary tract. J. Comp. Neurol. 286:243-259.
42. Ricardo, J.A., and E.T. Koh (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala and other forebrain structures in the rat. Brain Res. 153:1-26.
43. Riche, D., J. de Pommery, and D. Menetrey (1990) Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J. Comp. Neurol, 293:399-424.
44. Roder, S., and J. Ciriello (1993) Innervation of the amygdaloid complex by catecholaminergic cell groups of the ventrolateral medulla. J. Comp. Neurol. 332:105-322.
45. Rogers, R.C., and D.L. Fryman (1988) Direct connections between the central nucleus of the amygdala and the nucleus of the solitary tract: an electrophysiological study in the rat. J. Auton. Nerv. Syst. 22:83-87.
46. Rohrer, H., A.L. Acheson, J. Thibault, and H. Thoenen (1986) Developmental potential of quail dorsal root ganglion cells analyzed in vitro and in vivo. J. Neurosci. 6:2616-2624.
47. Ross, C.A., D.A. Ruggiero, and D.J. Reis (1985) projections from the nucleus of the tractus solitarii to the rostral ventrolateral medulla. J. Comp. Neurol. 242:511-534.
48. Ruggiero, D.A., M.P. Meeley, M. Anwar, and D.J. Reis (1985) Newly identified GABAergic neurons in regions of the ventrolateral medulla that regulate blood pressure. Brain Res. 339:171-177.
49. Rye, D.B., C.B. Saper, and B.H. Wainer (1984) Stabilization of the tetramethyl benzidine (TMB) reaction product: application for retrograde and anterograde tracing and combination with immunocytochemistry J. Histochem. Cytochem. 52:1145-1153.
50. Schwaber, J.S., B.S. Kapp, G.A. Higgins, and P.R. Rapp (1982) Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J. Neurosci. 2:1424-1438.
51. Seguela, P., M. Geffard, R.M. Buijs, and M. Le Moal (1984) Antibodies against gamma-aminobutyric acid: Specificity studies and immunocytochemical results. Proc. Natl. Acad. Sci. USA 81:3888-3892.
52. Smith, Y., and J.P. Bolam (1990) The output neurons and the dopaminergic neurons of the substantia nigra receive a GABA-contaimng input from the globus pallidus in the rat. J. Comp. Neurol. 296:47-64.
53. Spyer, K.M. (1989) Neural mechanisms involved in cardiovascular control during affective behaviour. TINS 12:506-513.
54. Sun, N., and M.D. Cassell (1993) Intrinsic GABAergic neurons in the rat central extended amygdala. J. Comp. Neurol. 330:381-404.
55. Sun, N., H. Yi, and M.D. Cassell (1994) Evidence for a GABAergic interface between cortical afferents and brainstem projection neurons in the rat central extended amygdala. J. Comp. Neurol. 340:43-64.
56. Takayama, K., J. Okada, and M. Miura (1990) Evidence that neurons of the central amygdaloid nucleus directly project to the site concerned with circulatory and respiratory regulation in the ventrolateral nucleus of the cat: A WGA-HRP study. Neurosci. Lett. 109:241-246.
57. Thompson, R.L., and M.D. Cassell (1989) Differential distribution and non-coliateralization of central amygdaloid neurons projecting to different medullary regions. Neurosci. Lett. 97:245-21.
58. Valtschanoff, J.G., R.J. Weinberg, and A. Rustioni (1993) Amino acid immunoreactivity in corticospinal terminals. Exp. Brain Res. 93: 95-103.
59. van der Kooy, D., L.Y. Koda, J.F. McGinty, C.R. Gerfen, and F.E. Bloom (1984) The organiaation of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in the rat. J. Comp. Neurol, 224:1-24.
60. Veening, J.G., L.W. Swanson, and P.E. Sawchenko (1984) The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: A combined retrograde transport-immunohistochemical study, Brain Res. 303:337-357.
61. Wang, Z.J., Z.R. Rao, and J.W. Shi (1992) Tyrosine hydroxylase-, neurotensin-, or cholecystokinin-containing neurons in the nucleus tractus solitarii send projection fibers to the nucleus accumbeus in the rat. Brain Res. 578:347-350.
62. Zardetto-Smith, A.M., and T.S. Gray (1990) Organization of peptidergic and catechulaminergic efferents from the nucleus of the solitary tract to the rat amygdala. Brain Res. Bull. 25:875-887.
63. Zardetto-Smith, A.M., and T.S. Gray (1995) Catecholamine and NPY efferents from the ventrolateral medulla to the amygdala in the rat. Brain Res, Bull. 38:253-260.
64. Zhang, N., F. Walberg, J.H. Laake, B.S. Meldrum, and O.P. Ottersen (1990) Aspartate-like and glutamate-like immunoreactivities in the inferior olive and climbing fiber system: A light microscopic and semiquantitative electron microscopic study in rat and baboon (Papio anubis). Neuroscience 38:61-80.