Serotonergic transmission in the periaqueductal gray matter in relation to aversive behaviour: Morphological evidence for direct modulatory effects on identified output neurons

Neuroscience

Volumn 95, Issue 3, 1999, Pages 763-772

  Lovick, T A ^a   Parry, D M ^b   Stezhka, V V ^a   Lumb, B M ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

5 hydroxytryptamine; Aversion; Biocytin; Periaqueductal gray matter; Ultrastructure; Volume transmission

Indexed keywords

BIOCYTIN; SEROTONIN;

ANIMAL EXPERIMENT; ARTICLE; AVERSIVE BEHAVIOR; CELL MEMBRANE; DENDRITE; GLIA CELL; GRAY MATTER; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; SEROTONINERGIC NERVE CELL; SYNAPSE VESICLE;

ANIMALS; AVOIDANCE LEARNING; ELECTROPHYSIOLOGY; IMMUNOLOGIC TECHNIQUES; LYSINE; MALE; NEURONS; PERIAQUEDUCTAL GRAY; RATS; RATS, WISTAR; SEROTONIN; STAINING AND LABELING; SYNAPTIC TRANSMISSION;

EID: 0032761468     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00480-7     Document Type: Article

References (56)

1. Aghajanian G., Vandermaelen C.P. Intracellular identification of central noradrenergic and serotonergic neurons by a new double labeling procedure. J. Neurosci. 2:1982;1786-1792.
2. Agnati L.F., Stromberg G., Fuxe K. Intercellular communication in the brain: wiring versus volume transmission. Neuroscience. 69:1995;711-726.
3. Alvarez F.J., Pearson J.C., Harrington D., Dewey D., Torbeck L., Fyffe R.E.W. Distribution of 5-hydroxytryptamine-immunoreactive boutons on motoneurons in the lumbar spinal cord of adult cats. J. comp. Neurol. 39:1998;69-83.
4. Bach-y-Rita P. Neurotransmission by diffusion through the extracellular fluid - a review. NeuroReport. 4:1993;343-350.
5. Bandler R. and Depaulis A. (1991) Midbrain periaqueductal gray control of defensive behaviour in the cat and the rat. In The Midbrain Periaqueductal Gray Matter. Functional, Anatomical and Neurochemical Organisation (eds Depaulis A. and Bandler R.), pp. 175-198. Plenum, New York.
6. Beaudet A., Descarries L. Quantitative data on serotonin nerve terminals in adult rat neocortex. Brain Res. 111:1976;301-309.
7. 1 receptor agonists administered into the periaqueductal grey. Psychopharmacology. 108:1992;110-114.
8. Behbehani M.M., Liu H., Jiang M., Pun R.Y.K., Shipley M.T. Activation of serotonin 1A receptors inhibits midbrain periaqueductal gray neurons in the rat. Brain Res. 612:1993;56-60.
9. Beitz A.J., Clements J.R., Mullett M., Ecklund L. Differential origin of brainstem serotonergic projections to the midbrain periaqueductal gray and superior colliculus in the rat. J. comp. Neurol. 250:1986;498-509.
10. Beitz A.J., Shepard R.D. The midbrain periaqueductal gray in the rat. II. A Golgi analysis. J. comp. Neurol. 237:1985;460-475.
11. Buma P., Veening J., Hafmans T., Joosten H., Nieuwenhuys R. Ultrastructure of the periaqueductal grey of the rat: an electron microscopical and horseradish peroxidase study. J. comp. Neurol. 319:1992;519-535.
12. Cameron A.A., Khan I.A., Westlund K.N., Willis W.D. The efferent projections of the periaqueductal gray in the rat: a Phaseolis vulgaris-leucoagglutinin study. II. Descending projections. J. comp. Neurol. 351:1995;585-601.
13. Chazal C., Ralston H.J. Serotonin-containing structures in the nucleus raphe dorsalis of the cat - an ultrastructural analysis of dendrites, presynaptic densities, and axon terminals. J. comp. Neurol. 259:1987;317-329.
14. Clements J.R., Beitz A.J., Fletcher T.F., Mullett M.A. Immunocytochemical localisation of serotonin in the rat periaqueductal grey: a quantitative light and electron microscope study. J. comp. Neurol. 236:1985;60-70.
15. Consolazione A., Milstein C., Wright B., Cuello A.C. Immunocytochemical detection of serotonin with monoclonal antibodies. J. Histochem. Cytochem. 29:1981;1425-1430.
16. Corvaja M., Doucet G., Bolam J.P. Ultrastructure and synaptic targets of the raphe-nigral projection in the rat. Neuroscience. 55:1993;417-427.
17. Dahlström A., Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system. 1. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta physiol. scand. 62:(Suppl. 232):1964;1-55.
18. Descarries L., Watkins K.C., Garcia S., Beaudet A. The serotonin neurons in nucleus raphe dorsalis of adult rat: a light and electron microscope radioautographic study. J. comp. Neurol. 207:1982;239-254.
19. Fornal C., Auerbach S., Jacobs B.L. Activity of serotonin-containing neurons in nucleus raphe magnus in freely moving cats. Expl Neurol. 88:1985;590-608.
20. Fuxe K. and Agnati L. F. (1991) Two principal modes of electrochemical communication within the brain: volume versus wiring transmission. In Volume Transmission in the Brain (eds Fuxe K. and Agnati L. F.), pp. 1-9. Raven, New York.
21. Ginsberg S.D., Martin L.J. Ultrastructural analysis of the progression of neurodegeneration in the septum following fimbria-fornix transection. Neuroscience. 86:1998;1259-1272.
22. Gioia M., Tredici G., Bianchi T. A golgi study of the periaqueductal gray matter in the cat. Neuronal types and their distribution. Expl Brain Res. 58:1985;318-332.
23. Graeff F.G., Brandao M.L., Audi A.E., Schutz M.T. Modulation of the midbrain aversive system by GABAergic and serotonergic mechanisms. Behav. Brain Res. 21:1986;65-72.
24. Hamalainen M.M., Lovick T.A. Involvement of nitric oxide and serotonin in modulation of antinociception and pressor responses evoked by serotonin in the dorsolateral region of the periaqueductal gray matter in the rat. Neuroscience. 80:1997;821-827.
25. Heym J., Steinfels G.F., Jacobs B.L. Activity of serotonin-containing neurons in the nucleus raphe pallidus of freely moving cats. Brain Res. 251:1982;259-276.
26. 3 receptors. Psychopharmacology. 97:1989;489-495.
27. Jones K.L., Duvica T.E., Jacob S.K. Gonadal steroid preservation of central synpatic input to hamster facial motoneurones following peripheral axotomy. J. Neurocytol. 26:1997;257-266.
28. Kiser R., German C., Lebowitz R.M. Serotonergic reduction of dorsal central gray stimulation-produced aversion. Pharmac. Biochem. Behav. 9:1978;27-32.
29. Krout K.E., Jansen A.S.P., Loewy A.D. Periaqueductal gray matter projection to the parabrachial nucleus in rat. J. comp. Neurol. 401:1998;437-454.
30. Liu R.P.C., Hamilton B.L. Neurons of the periaqueductal gray matter as revealed by Golgi study. J. comp. Neurol. 189:1980;413-418.
31. Lovick T.A. Serotonergic influence from nucleus raphe obscurus on neurones in the periaqueductal grey matter in the rat. Brain Res. 606:1993;92-98.
32. Lovick T.A. Influence of the dorsal and median raphe nuclei on neurons in the periaqueductal gray matter: role of 5-hydroxytryptamine. Neuroscience. 59:1994;993-1000.
33. Lovick T.A. Role of nitric oxide in medullary raphe-evoked inhibition of neuronal activity in the periaqueductal gray matter. Neuroscience. 75:1996;1203-1209.
34. 1A receptors are involved in inhibition of the midbrain-evoked cardiovascular defence response by nucleus raphe obscurus. Br. J. Pharmac. 117:1996;P94.
35. Lovick T.A., Stezhka V.V. Neurones in the dorsolateral periaqueductal grey matter in coronal slices of rat midbrain: electrophysiological and morphological characteristics. Expl Brain Res. 124:1999;53-58.
36. Marlier L., Sandillon F., Poulat P., Rajaofetra N., Geffard M., Privat A. Serotonergic innervation of the dorsal horn of the rat spinal cord - light and electron-microscopic immunocytochemical study. J. Neurocytol. 20:1991;310-322.
37. Maxwell D., Jankowska E. Synaptic relationships between serotonin-immunoreactive axons and dorsal horn spinocerebellar tract cells in the cat spinal cord. Neuroscience. 70:1996;247-253.
38. Milner T.A., Veznedaroglu E. Serotonin-containing terminals synapse on septohippocampal neurons in the rat. J. Neurosci. Res. 36:1993;260-271.
39. Moukhles H., Bosler O., Bolam J.P., Vallee A., Umbriaco D., Geffard M., Doucet G. Quantitative and morphometric data indicate precise cellular interactions between serotonin terminals and post-synaptic targets in rat substantia nigra. Neuroscience. 76:1997;1159-1171.
40. Nashold B.S., Wilson W.P., Slaughter D.G. Sensations evoked by stimulation in the midbrain of man. J. Neurosurg. 30:1969;14-24.
41. Nogueira R.L., Graeff F.G. Role of 5-HT receptor subtypes in the modulation of dorsal periaqueductal gray generated aversion. Pharmac. Biochem. Behav. 52:1995;1-6.
42. Onstott D., Mayer R.B., Beitz A.J. Nitric oxide synthase immunoreactive neurons anatomically define a longitudinal dorsolateral column within the midbrain periaqueductal grey of the rat - analysis using laser confocal microscopy. Brain Res. 610:1993;317-324.
43. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic, New York.
44. Reynolds E.S. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17:1963;208-213.
45. Ridet J.L., Rajaofetra N., Teilhac J.R., Geffard M., Privat A. Evidence for nonsynaptic serotonergic and noradrenergic innervation of the rat dorsal horn and possible involvement of neuron-glia interactions. Neuroscience. 52:1993;143-157.
46. Schenberg L.C., Lovick T.A. Attenuation of the midbrain evoked defense reaction by selective stimulation of medullary raphe neurons in rats. Am. J. Physiol. 269:1995;R1378-R1389.
47. Schmitt P., Sandner G., Colpaert F., DeWitte P. Effects of dorsal raphe stimulation on escape produced by medial hypothalamic or central gray stimulation. Behav. Brain Res. 8:1983;289-307.
48. Schutz M.T.B., DeAguiar J.C., Graeff F.G. Antiaversive role of serotonin in the dorsal PAG. Psychopharmacology. 85:1985;345-430.
49. Semenenko F.M., Lumb B.M., Lovick T.A. Projections from nucleus raphe obscurus to the periaqueductal grey matter in the rat. Neurosci. Lett. 170:1994;9-12.
50. Smiley J.F., Goldman Rakic P.S. Serotonergic axons in monkey prefrontal cerebral cortex synapse predominantly on interneurones as demonstrated by serial section electron microscopy. J. comp. Neurol. 367:1996;431-443.
51. Stezhka V.V., Lovick T.A. Inhibitory and excitatory projections from the dorsal raphe nucleus to the dorsolateral PAG in slices of midbrain maintained in vitro. Neuroscience. 62:1994;177-187.
52. Umbriaco D., Garcia S., Beaulieu C., Descarries L. Relational features of acteylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus. Hippocampus. 5:1995;605-620.
53. Van Bockstaele E.J., Pickel V.M. Ultrastructure of serotonin-immunoreactive terminals in the core and shell of rat nucleus accumbens - cellular substrates for interactions with catecholamine afferents. J. comp. Neurol. 334:1993;601-617.
54. Vincent S.R., Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience. 46:1992;755-784.
55. Young R.F. Brain stimulation: how and to whom! Clin. Neurosurg. 35:1989;429-447.
56. Zifa E., Fillion G. 5-Hydroxytryptamine receptors. Pharmac. Rev. 44:1992;401-458.