Ultrastructure of the Serotonin Innervation in the Mammalian Central Nervous System

Handbook of Behavioral Neuroscience

Volumn 21, Issue C, 2010, Pages 65-101

  Descarries, Laurent ^a,b   Riad, Mustapha ^a   Parent, Martin ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

Author keywords

axon terminals; cytochemistry; electron microscopy; immunocytochemistry; radioautography

Indexed keywords

EID: 78951491221     PISSN: 15697339     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1569-7339(10)70072-2     Document Type: Chapter

References (345)

1. G.K. Aghajanian F.E. Bloom Localization of tritiated serotonin in rat brain by electron microscopic radioautography J. Pharmacol. Exp. Ther. 156 1967 23 30
2. G.K. Aghajanian D.W. Gallager Raphe origin of serotonergic nerves terminating in the cerebral ventricles Brain Res. 88 1975 221 231
3. G.K. Aghajanian R.B. McCall Serotonergic synaptic input to facial motoneurons: localization by electron-microscopic radioautography Neuroscience 5 1980 2155 2161
4. B.K. Aghajanian F.E. Bloom M.H. Sheard Electron microscopy of degeneration within the serotonin pathway of rat brain Brain Res. 13 1969 266 273
5. G.K. Aghajanian H.J. Haigler F.E. Bloom Lysergic acid diethylamine and serotonin direct action on serotonin containing neurons Life Sci. 11 1972 615 622
6. K. Ajika J. Ochi Serotonin fibers in the rat hypothalamus, as revealed with pharmacological tools E. Yamada Proc. Xth Intl Congr 1975 Anatomists, Science Council of Japan Tokyo 257
7. F.J. Alvarez J.C. Pearson D. Harrington D. Dewey L. Torbeck R.E.W. Fyffe Distribution of 5-hydroxytryptamine-immunoreactive boutons on α-motoneurons in the lumbar spinal cord of adult cats J. Comp. Neurol. 393 1998 69 83
8. N.-E. Andén A. Dahlström K. Fuxe K. Larsson L. Olson U. Ungerstedt Ascending monoamine neurons to the telencephalon and diencepohalon Acta Physiol. Scand. 67 1966 313 326
9. K.J. Anderson V.R. Holets P.C. Mazur R.S. Lasher C.W. Cotman Immunocytochemical localization of serotonin in the rat dentate gyrus following raphe transplants Brain Res. 369 1986 21 28
10. D. André G. Vuillon-Cacciuttolo O. Bosler GABA nerve endings in the rat red nucleus: combined detection with serotonin terminals using dual immunocytochemistry Neuroscience 23 1987 1095 1102
11. N.M. Appel M.W. Wessendorf R.P. Elde Coexistence of serotonin and substance P-like immunoreactivity in nerve fibers apposing identified sympathoadrenal preganglionic neurons in rat intermediolateral cell column Neurosci. Lett. 65 1986 241 246
12. N.M. Appel M.W. Wessendorf R.P. Elde Thyrotropin-releasing hormone in spinal cord: coexistence with serotonin and with substance P in fibers and terminals apposing identified preganglionic sympathetic neurons Brain Res. 415 1987 137 143
13. R. Arai N. Karasawa K. Kurokawa H. Kanai K. Horiike A. Ito Differential subcellular location of mitochondria in rat serotonergic neurons depends of the presence and the absence of monoamine oxidase type B Neuroscience 114 2002 825 835
14. 3H]-serotonin into the olfactory bulb. II. Radioautographic study Brain Res. 196 1980 417 427
15. E.A. Arce C.A. Bennett-Clarke R.D. Mooney R.W. Rhoades Synaptic organization of the serotoninergic input to the superficial gray layer of the hamster's superior colliculus Synapse 11 1992 67 75
16. E.A. Arce R.W. Rhoades R.D. Mooney Effects of neonatal and adult enucleation on the synaptic organization of the serotoninergic projection to the superficial gray layer of the hamster's superior colliculus Brain Res. Dev. Brain Res. 90 1995 168 173
17. 3H]5-hydroxytryptamine Neuroscience 5 1980 229 240
18. D.M. Armstrong R.J. Miller A. Beaudet V.M. Pickel Enkephalin-like immunoreactivity in rat area postrema: ultrastructural localization and coexistence with serotonin Brain Res. 310 1984 269 278
19. M.A. Audet L. Descarries G. Doucet Quantified regional and laminar distribution of the serotonin innervation in the anterior half of adult rat cerebral cortex J. Chem. Neuroanat. 2 1989 29 44
20. M.C. Austin R.E. Whitehead C.L. Edgar J.E. Janovsky D.A. Lewis Localized decrease in serotonin transporter-immunoreactive axons in the prefrontal cortex of depressed subjects committing suicide Neuroscience 114 2002 807 815
21. E. Azmitia P.J. Gannon The ultrastructural localization of serotonin immunoreactivity in myelinated and unmyelinated axons within the medial forebrain bundle of rat and monkey J. Neurosci. 3 1983 2083 2090
22. E. Azmitia P.J. Gannon The primate serotonergic system: a review of human and animal studies and a report on Macaca fascicularis S. Fahn C.D. Marsden M.H. van Woert Myoclonus, Vol. 43, Advances in Neurology 1986 Raven Press New York, NY 407 468
23. 3H-5-HT): a morphological, biochemical and pharmacological approach to specificity J. Histochem. Cytochem. 28 1980 636 644
24. E.C. Azmitia M.J. Segal An radioautographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat J. Comp. Neurol. 179 1978 641 667
25. M.D. Bauman D.G. Amaral The distribution of serotonergic fibers in the macaque monkey amygdala: an immunohistochemical study using antisera to 5-hydroxytryptamine Neuroscience 136 2005 193 203
26. H.G. Baumgarten L. Lachenmayer Indoleamine-containing nerve terminals in the rat median eminence Z. Zellforsch. 147 1974 285 292
27. A. Beaudet High resolution radioautography of central 5-hydroxytryptamine (5-HT) neurons J. Histochem. Cytochem. 30 1982 765 768
28. A. Beaudet L. Descarries Quantitative data on serotonin nerve terminals in adult rat neocortex Brain Res. 111 1976 301 309
29. A. Beaudet L. Descarries The monoamine innervation of rat cerebral cortex: synaptic and non-synaptic relationships Neuroscience 3 1978 851 860
30. A. Beaudet L. Descarries Radioautographic characterization of a serotonin-accumulating nerve cell group in adult rat hypothalamus Brain Res. 160 1979 231 243
31. A. Beaudet L. Descarries The fine structure of central serotonin neurons J. Physiol. (Paris) 77 1981 193 203
32. A. Beaudet L. Descarries Fine structure of monoamine terminals in cerebral cortex Neurol. Neurobiol. 10 1984 77 93
33. A. Beaudet L. Descarries Ultrastructural identification of serotonin neurons H.W.M. Steinbusch Methods in Neuroscience, Monoaminergic Neurons: Light Microscopy and Ultrastructure 1987 John Wiley & Sons Chichester 265 313
34. A. Beaudet C. Sotelo Synaptic remodeling of serotonin axon terminals in rat agranular cerebellum Brain Res. 206 1981 305 329
35. A.J. Beitz J.R. Clements M.A. Mullett L.J. Ecklund Differential origin of brainstem serotoninergic projections to the midbrain periaqueductal gray and superior colliculus of the rat J. Comp. Neurol. 250 1986 498 509
36. G.A. Bishop R.H. Ho Cell bodies of origin of serotonin-immunoreactive afferents to the inferior olivary complex of the rat Brain Res. 399 1986 369 373
37. A. Björklund O. Lindvall Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals Brain Res. 83 1975 531 537
38. A. Blomqvist J. Broman Serotoninergic innervation of the dorsal column nuclei and its relation to cytoarchitectonic subdivisions: an immunohistochemical study in cats and monkeys (Aotus trivirgatus). J Comp. Neurol. 327 1993 584 596
39. F.E. Bloom B.J. Hoffer G.R. Siggins J.L. Barker R.A. Nicoll Effects of serotonin on central neurons: microiontophoretic administration Fed. Proc. 31 1972 97 106
40. P. Bobillier F. Petitjean D. Salvert M. Ligier S. Seguin Differential projections of the raphe nucleus, raphe dorsalis and nucleus raphe centralis as revealed by radioautography Brain Res. 85 1975 205 210
41. P. Bobillier S. Seguin F. Petitjean D. Salvert M. Touret M. Jouvet The raphe nuclei of the cat brain stem: a topographical atlas of their efferent projections as revealed by radioautography Brain Res. 113 1976 449 486
42. O. Bosler Radioautographic identification of serotonin axon terminals in the rat organum vasculosum laminae terminalis Brain Res. 150 1978 177 181
43. O. Bosler Radioautographie des systèmes monoaminergiques centraux. Nouvelle possibilité d'investigation des neurones dopaminergiques. Les Entretiens du Carla, 1980 Centre de recherche Pierre Fabre Castres 31 45
44. O. Bosler A. Beaudet Relations ultrastructurales entre systèmes monoaminergiques et peptidergiques dans l'hypothalamus Ann. Endocrinol. (Paris) 46 1985 19 26
45. O. Bosler A. Beaudet VIP neurons as prime synaptic targets for serotonin afferents in rat suprachiasmatic nucleus: a combined radioautographic and immunocytochemical study J. Neurocytol. 14 1985 749 763
46. O. Bosler L. Descarries Monoamine innervation of the organum vasculosum laminae terminalis (OVLT): a high resolution radioautographic study in the rat J. Comp. Neurol. 272 1988 545 561
47. O. Bosler A. Nieoullon B. Onteniente N. Dusticier In vitro radioautographic study of the monoaminergic innervation of cat red nucleus. Identification of serotoninergic terminals Brain Res. 259 1983 288 292
48. O. Bosler A. Beaudet M. Tappaz Morphological evidence for cellular interactions between serotoninergic terminals and VIP and GABAergic elements in rat suprachiasmatic nucleus Excerp. Med. 7th Intl Congr. Endocrinol. 652 1984 486
49. O. Bosler T.H. Joh A. Beaudet Ultrastructural relationships between serotonin and dopamine neurons in the rat arcuate nucleus and medial zona incerta: a combined radioautographic and immunocytochemical study Neurosci. Lett. 48 1984 279 285
50. O. Bosler A. Beaudet V.M. Pickel Characterization of chemically defined neurons and their cellular relationships by combined immunocytochemistry and radioautographic localization of transmitter uptake sites J. Electr. Microsc. Techn. 4 1986 21 39
51. C. Bouchaud Evidence for a multiple innervation of sub-commissural ependymocytes in the rat Neurosci. Lett. 12 1979 253 258
52. C. Bouchaud M. Arluison Serotoninergic innervation of ependymal cells in the rat subcommissural organ. A fluorescence, electron microscopic and radioautographic study Biol. Cell. 30 1977 65 72
53. C. Bouchaud O. Bosler The circumventricular organs of the mammalian brain with special reference to monoaminergic innervation Intl. Rev. Cytol. 105 1986 283 327
54. S. Boulaïch A. Daszuta M. Geffard O. Bosler Synaptic connectivity of serotonin graft efferents in the suprachiasmatic and supraoptic nuclei of the hypothalamus Exp. Brain Res. 101 1994 353 364
55. P. Boulenguez J. Abdelkefi R. Pinard A. Christolomme L.J. Segu Effects of retinal deafferentation on serotonin receptor types in the superficial gray layer of the superior colliculus of the rat Chem. Neuroanat. 6 1993 167 175
56. P. Boulenguez R. Pinard L. Segu Subcellular localization of 5-HT1B binding sites in the stratum griseum superficiale of the rat superior colliculus: an electron microscopic quantitative autoradiographic study Synapse 24 1996 203 212
57. R.M. Bowker Intrinsic 5-HT-immunoreactive neurons in the spinal cord of the fetal non-human primate Develop. Brain Res. 28 1986 137 143
58. R.M. Bowker Serotonergic and peptidergic inputs to the primate ventral spinal cord as visualized with multiple chromagens on the same tissue section Brain Res. 375 1986 345 350
59. R.M. Bowker K.N. Westlund J.D. Coulter Origins of serotonergic projections to the spinal cord in rat: an immunocytochemical-retrograde transport study Brain Res. 226 1981 187 199
60. R.M. Bowker V.K. Reddy S.J. Fung J.Y.H. Chan C.D. Barnes Serotonergic and non-serotonergic raphe neurons projecting to the feline lumbar and cervical spinal cord: a quantitative horseradish peroxidase-immunocytochem-ical study Neurosci. Lett. 75 1987 31 37
61. A. Brusco S. Peressini J. Pecci Saavedra Serotoninlike immunoreactivity and anti-5-hydroxytryptamine (5-HT) antiobodies: ultrastructural application in the central nervous system J. Histochem. Cytochem. 31 1983 524 530
62. M.A. Bunin R.M. Wightman Quantitative evaluation of 5-hydroxytryptamine (serotonin) release and uptake: an investigation of extrasynaptic transmission J. Neurosci. 18 1998 4854 4860
63. A. Calas Radioautographic studies of aminergic neurons terminating in the median eminence E. Costa G.L. Gessa Advances in Biochemical Pharmacology 1977 Raven Press New York, NY 79 88
64. A. Calas L. Ségu Radioautographic localization and identification of monoaminergic neurons in the central nervous system J. Microsc. Biol. Cell. 27 1976 249 252
65. A. Calas G. Alonso E. Arnauld J.D. Vincent Demonstration of indolaminergic fibres in the median eminence of the duck, rat and monkey Nature 250 1974 241 243
66. 3H]monoamines in the rat caudate nucleus: identification of serotoninergic fibers Brain Res. 118 1976 1 13
67. A. Calas O. Bosler M. Arluison C. Bouchaud Serotonin as a neurohormone in circumventricular organs and supraependymal fibers D.E. Scott G.P. Kozlowski A. Weindl Brain-Endocrine Interactions III. Neural Hormones and Reproduction. 3rd Intl Symp. Würzburg 1978 S. Karger A.G. Basel 238 250
68. A. Calas J.-J. Dupuy H. Gamrani J. Gonella C. Mourre M. Condamin J.-F. Pellissier P. Van den Bosch Radioautographic identification of serotonin cells Adv. Exp. Med. Biol. 133 1981 51 66
69. M.J. Campbell D.A. Lewis S.L. Foote J.H. Morrison Distribution of choline acetyltransferase-, serotonin, dopamine-beta-hydroxylase-, and tyrosine hydroxylase-immunoreactive fibers in monkey primary auditory cortex J. Comp. Neurol. 261 1987 209 220
70. O. Cases C. Lebrand B. Giros T. Vitalis E. De Maeyer M.G. Caron D.J. Price P. Gaspar I. Seif Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knock-outs J. Neurosci. 18 1998 6914 6927
71. B. Cauli X.-K. Tong A. Rancillac N. Serluca B. Lambolez J. Rossier E. Hamel Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways J. Neurosci. 24 2004 8940 8949
72. V. Chan-Palay Fine structure of labelled axons in the cerebellar cortex and nuclei of rodents and primates after intraventricular infusions with tritiated serotonin Anat. Embryol. 148 1975 235 265
73. V. Chan-Palay Serotonin axons in the supra- and sub-ependymal plexuses and in the leptomeninges: their roles in local alterations of cerebrospinal fluid and vasomotor activity Brain Res. 102 1976 103 130
74. V. Chan-Palay Cerebellar Dentate Nucleus: Organization, Cytology and Transmitters 1977 Springer-Verlag Berlin
75. V. Chan-Palay The paratrigeminal nucleus. II. Identification and inter-relations of catecholamine axons, indoleamine axons, and substance P immunoreactive cells in the neuropil J. Neurocytol. 7 1978 419 442
76. V. Chan-Palay Morphological correlates for transmitter synthesis, transport, release, uptake and catabolism: a study of serotonin neurons in the nucleus paragigantocellularis lateralis F. Fonnum Amino Acids as Chemical Transmitters 1978 Plenum New York, NY 1 30
77. 3H-serotonin Neurol. Neurobiol. 1 1982 357 386
78. G. Chazal W. Ma A ultrastructural analysis of serotoninergic neurons in the nucleus raphe magnus of the rat Neuroscience 33 1989 301 310
79. G. Chazal P.T. O'Hara Vesicle-containing dendrites in the nucleus raphe dorsalis of the cat. A serial electron microscopic analysis J. Neurocytol. 15 1986 777 787
80. G. Chazal H.J. Ralston III Serotonin-containing structures in the nucleus raphe dorsalis of the cat: an ultrastructural analysis of dendrites, presynaptic dendrites, and axon terminals J. Comp. Neurol. 259 1987 317 329
81. A. Cheramy V. Leviel J. Glowinski Dendritic release of dopamine in the substantia nigra Nature 289 1981 537 542
82. T. Chiba S. Masuko Synaptic structure of the monoamine and peptide nerve terminals in the intermediolateral nucleus of the guinea pig thoracic spinal cord J. Comp. Neurol. 262 1987 242 255
83. J.R. Clements A.J. Beitz T.F. Fletcher M.A. Mullett Immunocytochemical localization of serotonin in the rat periaqueductal gray: a quantitative light and electron microscopic study J. Comp. Neurol. 236 1985 60 70
84. Z. Cohen M. Ehret M. Maître E. Hamel Ultrastructural analysis of tryptophane hydroxylase immunoreactive nerve terminals in the rat cerebral cortex and hippocampus: their associations with local blood vessels Neuroscience 66 1995 555 569
85. K.G. Commons R.J. Valentino Cellular basis for the effects of substance P in the periaqueductal gray and raphe dorsalis J. Comp. Neurol. 447 2002 82 97
86. K.G. Commons S.G. Beck V.W. Bey Two populations of glutamatergic axons in the rat raphe dorsalis defined by the vesicular glutamate transporters 1 and 2 Eur. J. Neurosci. 21 2005 1577 1586
87. L.C.A. Conrad C.M. Leonard D.W. Pfaff Connections of the median and dorsal raphe nuclei in the rat: an radioautographic and degeneration study J. Comp. Neurol. 156 1974 179 206
88. J.C. Copray R.S. Liem G.J. Ter Horst J.D. van Willigen Origin, distribution and morphology of serotonergic afferents to the mesencephalic trigeminal nucleus of the rat Neurosci. Lett. 121 1991 97 101
89. N. Corvaja G. Doucet J.P. Bolam Ultrastructure and synaptic targets of the raphe-nigral projection in the rat Neuroscience 55 1993 417 427
90. R.S. Crissman E.A. Arce C.A. Bennett-Clarke R.D. Mooney R.W. Rhoades Reduction in the percentage of serotoninergic axons making synapses during the development of the superficial layers of the hamster's superior colliculus Brain Res. Dev. Brain Res. 75 1993 131 135
91. E.C. Cropper J.S. Eisenman E.C. Azmitia An immunocytochemical study of the serotonergic innervation of the thalamus of the rat J. Comp. Neurol. 224 1984 38 50
92. A. Dahlström K. Fuxe Evidence for the existence of monoamine neurons in the central nervous system. IV. Demonstration of monoamines in the cell body of brain stem neurons Acta Physiol. Scand. 62 Suppl. 232 1964 1 55
93. A. Dahlstrom K. Fuxe L. Olson U. Ungerstedt On the distribution and possible function of monoamine nerve terminals in the olfactory bulb of the rabbit Life Sci. 4 1965 2071 2074
94. A. Daszuta G. Chazal S. Garcia S. Oleskevich L. Descarries Ultrastructural features of serotonin neurons grafted to adult rat hippocampus. An immunocytochemical analysis of their cell bodies and axon terminals Neuroscience 42 1991 793 811
95. G. Daval D. Vergé A.I. Basbaum S. Bourgoin M. Hamon Radioautographic evidence of serotonin1 binding sites on primary afferent fibres in the dorsal horn of the rat spinal cord Neurosci. Lett. 83 1987 71 76
96. R. Davis P.C. Vaughan Pharmacological properties of feline red nucleus Int. J. Neuropharmacol. 8 1969 475 488
97. J. De Felipe E.G. Jones A light and electron microscopic study of serotonin-immunoreactive fibers and terminals in the monkey sensorimotor cortex Exp. Brain Res. 71 1988 171 182
98. J. De Felipe S.H.C. Hendry T. Hashikawa E.G. Jones Synaptic relationships of serotonin-immunoreactive terminal baskets of GABA neurons in the cat auditory cortex Cereb. Cortex 1 1991 117 133
99. I.S. De La Manche M. Arluison C. Bouchaud Experimental ultrastructural modifications of the content of serotoninergic supra-ependymal nerve fibres in the rat J. Physiol. (Paris) 77 1981 225 231
100. A.D. De Lima W. Singer The serotoninergic fibers in the dorsal geniculate nucleus of the cat: distribution and synaptic connections demonstrated with immunocytochemistry J. Comp. Neurol. 258 1987 339 351
101. A.D. De Lima W. Singer The brainstem projection to the lateral geniculate nucleus in the cat: distribution and synaptic connections demonstrated with immunocytochemistry J. Comp. Neurol. 259 1987 92 127
102. A.D. De Lima F.E. Bloom J.H. Morrison Synaptic organization of serotonin-immunoreactive fibers in primary visual cortex of the Macaque monkey J. Comp. Neurol. 274 1988 280 294
103. L. Descarries A. Beaudet The serotonin innervation of adult rat hypothalamus J.D. Vincent C. Kordon Biologie Cellulaire des Processus Neurosécrétoires, Coll. Internat. CNRS, Ed 1978 CNRS Paris 135 153
104. L. Descarries A. Beaudet The use of radioautography for investigating transmitter-specific neurons A. Björklund T. Hökfelt Handbook of Chemical Neuroanatomy, Vol. I, Methods 1983 Elsevier/North-Holland Amsterdam 286 364
105. L. Descarries L. Léger Serotonin nerve terminals in the locus coeruleus of the adult rat S. Garattini J.F. Pujol R. Samanin Interactions Between Putative Neurotransmitters 1978 Raven Press New York, NY 355 367
106. L. Descarries N. Mechawar Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system, Prog Brain Res. 125 2000 27 47
107. L. Descarries N. Mechawar Structural organization of monoamine and acetylcholine neuron systems in the rat CNS A. Lajtha E.S. Vizi Handbook of Neurochemistry and Molecular Neurobiology, 3rd edn., Neurotransmitter Systems 2008 Springer New York, NY 1 20
108. L. Descarries D. Umbriaco Ultrastructural basis of monoamine and acetylcholine function in CNS Seminars Neurosci. 7 1995 309 318
109. L. Descarries A. Beaudet K.C. Watkins Serotonin nerve terminals in adult rat neocortex Brain Res. 100 1975 563 588
110. L. Descarries K.C. Watkins S. Garcia A. Beaudet The serotonin neurons in nucleus raphe dorsalis of adult rat: a light and electron microscope radioautographic study J. Comp. Neurol. 207 1982 239 254
111. L. Descarries F. Berthelet S. Garcia A. Beaudet Dopaminergic projection from nucleus raphe dorsalis to neostriatum in the rat J. Comp. Neurol. 249 1986 511 520
112. L. Descarries M.A. Audet G. Doucet S. Garcia S. Oleskevich P. Séguéla J.-J. Soghomonian K.C. Watkins Morphology of central serotonin neurons Ann. NY Acad. Sci. 600 1990 81 92
113. L. Descarries P. Séguéla K.C. Watkins Nonjunctional relationships of monoamine axon terminals in the cerebral cortex of adult rat Adv. Neurosci. 1 1991 53 62
114. L. Descarries J.-J. Soghomonian S. Garcia G. Doucet J.P. Bruno Ultrastructural analysis of the serotonin hyperinnervation in adult rat neostriatum following neonatal dopamine denervation with 6-hydroxydopamine Brain Res. 569 1992 1 13
115. L. Descarries V. Cornea-Hébert M. Riad Cellular and subcellular localization of serotonin receptors in the central nervous system B.L. Roth The Serotonin Receptors: From Molecular Pharmacology to Human Therapeutics 2006 Humana Press Totowa, NJ 277 317
116. A. Dinopoulos I. Dori The development of the serotonergic fiber network of the lateral ventricles of the rat brain: a light and electron microscopic immunocytochemical analysis Exp. Neurol. 133 1995 73 84
117. A. Dinopoulos I. Dori J.G. Parnavelas Serotonergic innervation of the mature and developing lateral septum of the rat: a light and electron microscopic immunocytochemical analysis Neuroscience 55 1993 209 222
118. A. Dinopoulos I. Dori J.G. Parnavelas Serotonergic innervation of the lateral geniculate nucleus of the rat during postnatal development: a light and electron microscopic immunocytochemical analysis J. Comp. Neurol. 363 1995 532 544
119. A. Dinopoulos I. Dori J.G. Parnavelas The serotonin innervation of the basal forebrain shows a transient phase during development Brain Res. Dev. Brain Res. 99 1997 38 52
120. I.E. Dori A. Dinopoulos J.G. Parnavelas Regional differences in the ontogeny of the serotonergic preojection to the cerebral cortex Exp. Neurol. 138 1996 1 14
121. I.E. Dori A. Dinopoulos M.E. Blue J.G. Parnavelas The development of the synaptic organization of the serotonergic system differs in brain areas with different functions Exp. Neurol. 154 1998 113 125
122. G. Doucet L. Descarries M.A. Audet S. Garcia B. Berger Radioautographic method for quantifying regional monoamine innervations in the rat brain. Application to the cerebral cortex Brain Res. 441 1988 233 259
123. R. Elde B. Maley V. Holets V. Seybold Peptidergic and serotinergic neurons in neuroendocrine and central autonomic circuits Neurol. Neurobiol. 1 1982 331 340
124. J.H. Fallon S.E. Loughlin Monoamine innervation of the forebrain Collateralization. Brain Res. Bull. 9 1982 295 307
125. H.C. Fibiger J.J. Miller An anatomical and electrophysiological investigation of the serotonergic projections from the raphe dorsalis to the substantia nigra in the rat Neuroscience 2 1977 975 987
126. M. Frankfurt A. Beaudet Ultrastructural organization of regenerated serotonin axons in the dorsomedial hypothalamus of the adult rat J. Neurocytol. 16 1987 799 809
127. M. Frankfurt A. Beaudet Reinnervation of dopamine neurons by regenerating serotonin axons in the rat medial zona incerta Exp. Brain Res. 72 1988 473 480
128. M. Frankfurt J.M. Lauder E.C. Azmitia The immunocytochemical localization of serotonergic neurons in the rat hypothalamus Neurosci. Lett. 24 1981 227 232
129. T.F. Freund A.L. Gulyás L. Acsády T. Gorcs K. Tóth Serotonergic control of the hippocampus via local inhibitory interneurons Proc. Natl. Acad. Sci. USA 87 1990 8501 8505
130. K. Fuxe Evidence for the existence of monoamine neurons in the central nervous system. IV. Distribution of monoamine nerve terminals in the central nervous system Acta Physiol. Scand. 65 Suppl. 247 1965 37 85
131. K. Fuxe G. Jonnson A modification of the histochemical fluorescence method for the improved localization of 5-hydroxytryptamine Histochemie 11 1967 161 166
132. K. Fuxe C. Owman Cellular localization of monoamines in the area postrema of certain mammals J. Comp. Neurol. 125 1965 337 353
133. K. Fuxe U. Ungerstedt Histochemical studies on the distribution of catecholamines and 5-hydroxytryptamine after intraventricular injections Histochemie 13 1968 16 28
134. H. Gamrani M.F. Belin M. Aguera A. Calas J.F. Pujol Radioautographic evidence for an innervation of the subcommissural organ by GABA-containing nerve fibres J. Neurocytol. 10 1981 411 424
135. H. Gamrani M. Harandi M.F. Bélin M.P. Dubois A. Calas Direct electron microscopic evidence for the coexistence of GABA uptake and endogenous serotonin in the same rat central neurons by coupled radioautographic and immunocytochemical procedures Neurosci. Lett. 48 1984 25 30
136. 3H]serotonin are presynaptic to enkephalin immunoreactive neurons in cat dorsal horn Brain Res. 298 1984 386 391
137. B.P. Guiard M. El Mansari Z. Merali P. Blier Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoamine lesions Intl. J. Neuropsychopharmacol. 11 2008 625 639
138. N. Halász A. Ljungdahl T. Hökfelt O. Johansson M. Goldstein D. Park P. Biberfeld Transmitter histochemistry of the rat olfactory bulb. I. Immunohistochemical localization of monoamine synthesizing enzymes. Support for intrabulbar, periglomerular dopamine neurons Brain Res. 126 1977 455 474
139. N. Halász A. Ljungdahl T. Hökfelt Transmitter histochemistry of the rat olfactory bulb. II. Fluorescence histochemical, radioautographic and electron microscopic localization of monoamines Brain Res. 154 1978 253 271
140. 3 receptor binding sites are on capsaicin-sensitive fibres in the rat spinal cord Eur. J. Pharmacol. 164 1989 315 322
141. S.R. Hansson E. Mezey B.J. Hoffman Serotonin transporter messenger RNA in the developing rat brain: early expression in serotonergic neurons and transient expression in non-serotonergic neurons Neuroscience 83 1998 1185 1201
142. 3H]GABA accumulation Brain Res. 370 1986 241 249
143. D.H. Harkness M.S. Brownfield A thyrotropin-releasing hormone-containing system in the rat dorsal horn separate from serotonin Brain Res. 384 1986 323 333
144. D. Hervé V.M. Pickel T.H. Joh A. Beaudet Serotonin axon terminals in the ventral tegmental area of the rat: fine structure and synaptic input to dopaminergic neurons Brain Res. 435 1987 71 83
145. F. Héry M. Faudon J.P. Ternaux In vivo release of serotonin in two raphe nuclei (raphe dorsalis and magnus) of the cat Brain Res. Bull. 8 1982 123 129
146. M.J. Hoffert V. Miletic M.A. Ruda R. Dubner Immunocytochemical identification of serotonin axonal contacts on characterized neurons in laminae I and II of the cat dorsal horn Brain Res. 267 1983 361 364
147. T. Hökfelt Electron microscopic studies on brain slices from regions rich in catecholamine nerve terminals Acta Physiol. Scand. 69 1967 119 120
148. T. Hökfelt K. Fuxe Cerebellar monoamine nerve terminals, a new type of afferent fibers in the cortex cerebelli Exp. Brain Res. 9 1969 63 72
149. J.R. Holtman Jr. D.S. Vascik B.E. Maley Ultrastructural evidence for serotonin-immunoreactive terminals contacting phrenic motoneurons in the cat Exp. Neurol. 109 1990 269 272
150. T. Honda K. Semba Serotonergic input to cholinergic neurons in the rat mesopontine tegmentum Brain Res. 647 1994 299 306
151. 2A receptors J. Neurocytol. 31 2002 667 679
152. J. Huang A.D. Spier V.M. Pickel 5-HT3 receptor subunits in the rat medial nucleus of the solitary tract: sub-cellular distribution and relation to the serotonin transporter Brain Res. 1028 2004 156 169
153. J.L.K. Hylden H. Hayashi M.A. Ruda R. Dubner Serotonin innervation of physiologically identified lamina I projection neurons Brain Res. 370 1986 401 404
154. B.L. Jacobs W.L. Wise K.M. Taylor Differential behavioral and neurochemical effects following lesions of the dorsal or median raphe nuclei in rats Brain Res. 79 1974 353 361
155. B.L. Jacobs S.L. Foote N. Rajaofetra Differential projections of neurons within the raphe dorsalis of the rat: a horseradish peroxidase (HRP) study Brain Res. 147 1978 149 153
156. E. Jankowska D.J. Maxwell S. Dolk A. Dahlstrom A confocal and electron microscopic study of contacts between 5-HT fibres and feline dorsal horn interneurons in pathways from muscle afferents J. Comp. Neurol. 387 1997 430 438
157. L. Jennes W.C. Beckman W.E. Stumpf R. Grzanna Anatomical relationships of serotoninergic and noradrenalinergic projections with the GnRH system in septum and hypothalamus Exp. Brain Res. 46 1982 331 338
158. I. Jensen I.J. Llewellyn-Smith P. Pilowsky J.B. Minson J. Chalmers Serotonin inputs to rabbit sympathetic preganglionic neurons projecting to the superior cervical ganglion or adrenal medulla J. Comp. Neurol. 353 1995 427 438
159. 3H]aspartate tracing Brain Res. 360 1985 285 297
160. S.E. Kapadia N.C. De Lanerolle C.C. LaMotte Immunocytochemical and electron microscopic study of serotonin neuronal organization in the raphe dorsalis of the monkey Neuroscience 15 1985 729 746
161. H. Kawano K. Decker S. Reuss Is there a direct retina-raphe-suprachiasmatic nucleus pathway in the rat? Neurosci. Lett. 212 1996 143 146
162. V.N. Kazakov P.Ya. Kravtsov E.D. Krakhotkina V.A. Maisky Sources of cortical, hypothalamic and spinal serotonergic projections: topical organization within the nucleus raphe dorsalis Neuroscience 56 1993 157 164
163. M. Ke R.D. Mooney R.W. Rhoades Increased serotonin in the developing superior colliculus affects receptive-field size of retinotectal afferents but not that of postsynaptic neurons Vis. Neurosci. 16 1999 121 130
164. K.J. Kellar P.A. Brown J. Madrid M. Bernstein J. Vernikos Danellis W.R. Melher Origins of serotonin innervation of forebrain structure; Exp Neurol. 56 1977 52 62
165. J.S. King R.H. Ho R.W. Burry The distribution and synaptic organization of serotoninergic elements in the inferior olivary complex of the opossum J. Comp. Neurol. 227 1984 357 368
166. J. Kiss B. Halász Demonstration of serotoninergic axons terminating on luteinizing hormone-releasing hormone neurons in the preoptic area of the rat using a combination of immunocytochemistry and high resolution radioautography Neuroscience 14 1985 69 78
167. J. Kiss B. Halász Synaptic connections between serotoninergic axon terminals and tyrosine hydroxylase-immunoreactive neurons in the arcuate nucleus of the rat hypothalamus. A combination of electron microscopic radioautography and immunocytochemistry Brain Res. 364 1986 284 294
168. J. Kiss C. Léránth B. Halász Serotoninergic endings on VIP neurons in the suprachiasmatic nucleus and on ACTH-neurons in the arcuate nucleus of the rat hypothalamus. A combination of high resolution radioautography and electron microscopic immunocytochemistry Neurosci. Lett. 44 1984 119 124
169. M.J. Kuhar B.K. Aghajanian R.H. Roth Tryptophan hydroxylase activity and synaptosomal uptake of serotonin in discrete brain regions after midbrain raphe lesions: correlations with serotonin levels and histochemical fluorescence Brain Res. 44 1972 165 176
170. C.C. LaMotte N.C. De Lanerolle Ultrastructure of chemically defined neuron systems in the dorsal horn of the monkey. III. Serotonin immunoreactivity Brain Res. 274 1983 65 77
171. C.C. LaMotte D.R. Johns N.C. de Lanerolle Immunohistochemical evidence of indolamine neurons in monkey spinal cord J. Comp. Neurol. 206 1982 359 370
172. B. Lavoie A. Parent Immunohistochemical study of the serotoninergic innervation of the basal ganglia in the squirrel monkey J. Comp. Neurol. 299 1990 1 16
173. B. Lavoie A. Parent Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study J. Comp. Neurol. 312 1991 1 18
174. N.E. Lazarov C.N. Chouchkov Serotonin-containing projections to the mesencephalic trigeminal nucleus of the cat Anat. Rec. 241 1995 136 142
175. C. Lebrand O. Cases C. Adelbrecht A. Doye C. Alvarez S. El Mestikawy I. Seif P. Gaspar Transient uptake and storage of serotonin in developing thalamic neurons Neuron 17 1996 823 835
176. C. Lebrand O. Cases R. Wehrlé R.D. Blakely R.H. Edwards P. Gaspar Transient developmental expression of monoamine transporters in the rodent forebrain J. Comp. Neurol. 401 1998 506 524
177. L. Léger L. Descarries Serotonin nerve terminals in the locus coeruleus of adult rat: a radioautographic study Brain Res. 145 1978 1 13
178. L. Léger A.M. Degueurce J.F. Pujol Origin of the serotoninergic innervation of the rat locus coeruleus C. R. Acad. Sci. Paris, série D. 290 1980 807 810
179. L. Léger A. Degueurce J.J. Lundberg J.F. Pujol K. Møllgård Origin and influence of the serotoninergic innervation of the subcommissural organ in the rat Neuroscience 10 1983 411 423
180. C. Léránth R.P. Vertes Median raphe serotonergic innervation of medial septum/diagonal band of Broca (MSDB) parvalbumin-containing neurons: possible involvement of the MSDB in the desynchronization of the hippocampal EEG J. Comp. Neurol. 410 1999 586 598
181. J.-L. Li T. Kaneko S. Nomura Y.-Q. Li N. Mizuno Association of serotonin-like immunoreactive axons with nociceptive projection neurons in the caudal spinal trigeminal nucleus of the rat J. Comp. Neurol. 384 1997 127 141
182. F. Licata G. Li Volsi L. Ciranna G. Maugeri F. Santangelo 5-Hydroxytryptamine modifies neuronal responses to glutamate in the red nucleus of the rat Exp. Brain Res. 118 1998 61 70
183. H.G.W. Lidov R. Grzanna M.E. Molliver The serotonin innervation of the cerebral cortex in the rat: an immunohistochemical analysis Neuroscience 5 1980 207 227
184. R.S.B. Liem J.C.V.M. Copray Immunogold localization of serotonin within synaptic terminals in the rat mesencephalic trigeminal nucleus Acta Anat. (Basel) 155 1996 50 56
185. R.S.B. Liem J.C.V.M. Copray J.D. van Willigen Serotonin-immunoreactive terminals in the mesencephalic trigeminal nucleus of the rat: an electron microscopic immunocytochemical study Acta Anat. (Basel) 148 1993 34 41
186. A.R. Light A.M. Kavoodjian P. Petrusz The ultrastructure and synaptic connections of serotonin-immunoreactive terminals in spinal laminae I and II Somatosensory Res. 1 1983 33 50
187. O. Lindvall A. Björklund General organization of cortical monoamine systems Neurol. Neurobiol. 1 1984 9 40
188. Z. Liposits C. Phelix W.K. Paull Synaptic interaction of serotonergic axons and corticotropin releasing factor (CRF) synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. A light and electron microscopic immunocytochemical study Histochemistry 86 1987 541 549
189. X.B. Liu E.G. Jones The fine structure of serotonin and tyrosine hydroxylase immunoreactive terminals in the ventral posterior thalamic nucleus of cat and monkey Exp. Brain Res. 85 1991 507 518
190. A. Ljungdahl T. Hökfelt N. Halasz O. Johansson M. Goldstein Olfactory bulb dopamine neurons – the A15 catecholamine cell group; Acta Physiol Scand. 452 Suppl. 1977 31 34
191. J.J. López Costa S. Averill J.P. Pecci Saavedra J.V. Priestley Serotonin innervation of enkephalin containing neurones in the rat spinal trigeminal nucleus Neurosci. Lett. 168 1994 167 171
192. S.A. Lorens H.C. Guldberg Regional 5-hydroxytryptamine following selective midbrain raphe lesions in the rat Brain Res. 78 1974 45 56
193. H.P. Lorez J.G. Richards Distribution of indolealkylamine nerve terminals in the ventricles of the rat brain Z. Zellforsch. 144 1973 511 522
194. H.P. Lorez J.G. Richards 5-HT nerve terminals in the fourth ventricule of the rat brain: their identification and distribution studied by fluorescence histochemistry and electron microscopy Cell Tissue Res. 165 1975 37 48
195. H.P. Lorez J.G. Richards Supra-ependymal serotoninergic nerves in mammalian brain: morphological, pharmacological and functional studies Brain Res. Bull. 9 1982 727 741
196. T.A. Lovick D.M. Parry V.V. Stezhka B.M. Lumb Serotonergic transmission in the periaqueductal gray matter in relation to aversive behaviour: morphological evidence for direct modulatory effects on identified output neurons Neuroscience 95 2000 763 772
197. J.I. Luebke R.W. Greene K. Semba A. Kamondi R.W. McCarley P.B. Reiner Serotonin hyperpolarizes cholinergic low-threshold burst neurons in the rat laterodorsal tegmental nucleus in vitro Proc. Natl. Acad. Sci. USA 89 1992 743 747
198. B. Maley R. Elde The ultrastructural localization of serotonin immunoreactivity within the nucleus of the solitary tract of the cat J. Neurosci. 2 1982 1499 1506
199. B.E. Maley M.G. Engle S. Humphreys D.A. Vascik K.A. Howes B.W. Newton R.P. Elde Monoamine synaptic structure and localization in the central nervous system J. Electr. Microsc. Techn. 15 1990 20 33
200. L. Marlier F. Sandillon P. Poulat N. Rajaofetra M. Geffard A. Privat Serotonergic innervation of the dorsal horn of rat spinal cord: light and electron microscopic immunocytochemical study J. Neurocytol. 20 1991 310 322
201. L. Marlier P. Poulat N. Rajaofetra F. Sandillon A. Privat Plasticity of serotonergic innervation of the dorsal horn of the rat spinal cord following neonatal capsaicin treatment J. Neurosci. Res. 31 1992 346 358
202. F. Mascagni A.J. McDonald A novel subpopulation of 5-HT type 3A receptor subunit immunoreactive interneurons in the rat basolateral amygdala Neuroscience 144 2007 1015 1024
203. D.J. Maxwell E. Jankowska Synaptic relationships between serotonin-immunoreactive axons and dorsal horn spinocerebellar tract cells in the cat spinal cord Neuroscience 70 1996 247 253
204. D.J. Maxwell Cs. Léránth A.A.J. Verhofstad Fine structure of serotonin-containing axons in the marginal zone of the rat spinal cord Brain Res. 266 1983 253 259
205. D.J. Maxwell C. Léránth A.A.J. Verhofstad Synaptic arrangements formed by serotonin-immunoreactive axons in the substantia gelatinosa of the rat spinal cord Q. J. Exp. Physiol. 70 1985 377 388
206. R. McCall G.K. Aghajanian Serotonergic facilitation of facial motoneuron excitation Brain Res. 169 1979 11 27
207. A.J. McDonald F. Mascagni Neuronal localization of 5-HT type 2A receptor immunoreactivity in the rat basolateral amygdala Neuroscience 146 2007 306 320
208. R.M. McPeek E.L. Keller Deficits in saccade target selection after inactivation of superior colliculus Nat. Neurosci. 7 2004 757 763
209. V. Miletic M.J. Hoffert M.A. Ruda R. Dubner Y. Shigenaga Serotinergic axonal contacts on identified car spinal dorsal horn neurons and their correlation with nucleus raphe magnus stimulation J. Comp. Neurol. 228 1984 129 141
210. T.A. Milner E. Veznedaroglu Serotonin-containing terminals synapse on septohippocampal neurons in the rat J. Neurosci. Res. 36 1993 260 271
211. L.H. Miner S. Schroeter R.D. Blakely S.R. Sesack Ultrastructural localization of the serotonin transporter in superficial and deep layers of the rat prelimbic prefrontal cortex and its spatial relationships to dopamine terminals J. Comp. Neurol. 427 2000 220 234
212. R.R. Mize L.H. Horner Origin, distribution, and morphology of serotonergic afferents to the cat superior colliculus: a light and electron microscope immunocytochemistry study Exp. Brain Res. 75 1989 83 98
213. K. Mizukawa Y. Takeuchi Electron microscopic investigation of monoaminergic terminals to alpha-moto-neurons in the anterior horn of the cat spinal cord Acta Med. Okayama 36 1982 85 93
214. K. Mizukawa N. Otsuka T. Hattori Serotonin-containing nerve fibers in the rat spinal cord: electron microscopic immunohistochemistry Acta Med. Okayama 40 1986 1 10
215. K. Møllgärd L. Wiklund Serotoninergic synapses on ependymal and hypendymal cells of the rat subcommissural organ J. Neurocytol. 8 1979 445 467
216. M.E. Molliver R. Grzanna H.G.W. Lidov J.H. Morrisson J.A. Olschowka Monoamine systems in the cerebral cortex Neurol. Neurobiol. 1 1982 255 278
217. R.Y. Moore Organum vasculosum laminae terminalis: innervation by serotonin neurons of the midbrain raphe Neurosci. Lett. 5 1977 297 302
218. R.Y. Moore A.E. Halaris Hippocampal innervation by serotonin neurons of the midbrain raphe in the rat J. Comp. Neurol. 164 1975 171 183
219. R.Y. Moore A.E. Halaris B.E. Jones Serotonin neurons of the midbrain raphe: ascending projections J. Comp. Neurol. 180 1978 417 438
220. 3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon J. Neurosci. 17 1997 3157 3167
221. S. Mori T. Matsuura T. Takino Y. Sano Light and electron microscopic immunohistochemical studies of serotonin nerve fibers in the substantia nigra of the rat, cat and monkey Anat. Embryol. 176 1987 13 18
222. J.H. Morrison S.L. Foote Noradrenergic and serotoninergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys J. Comp. Neurol. 243 1986 117 138
223. J.H. Morrison S.L. Foote M.E. Molliver F.E. Bloom H.G.W. Lidov Noradrenergic and serotoninergic fibers innervate complementary layers in monkey primary visual cortex: an immunohistochemical study Proc. Natl. Acad. Sci. USA 79 1982 2401 2405
224. J.H. Morrison S.L. Foote F.E. Bloom Regional, laminar, developmental and functional characteristics of noradrenaline and serotonin innervation patterns on monkey cortex Neurol. Neurobiol. 10 1984 61 75
225. S.S. Mosko D. Haubrich B.L. Jacobs Serotonergic afferents to the raphe dorsalis: evdience from HRP and synaptosomal uptake studies Brain Res. 119 1977 269 290
226. H. Moukhles O. Bosler J.P. Bolam A. Vallée D. Umbriaco M. Geffard G. Doucet Quantitative and morphometric data indicate precise cellular interactions between serotonin terminals and postsynaptic targets in rat substantia nigra Neuroscience 76 1997 1159 1171
227. A. Mrini J.-P. Soucy F. Lafaille P. Lemoine L. Descarries Quantification of the serotonin hyperinnervation in adult rat neostriatum after neonatal 6-hydroxydopamine lesion of nigral dopamine neurons Brain Res. 669 1995 303 308
228. J.F. Muller F. Mascagni A.J. McDonald Coupled networks of parvalbumin-immunoreactive interneurons in the rat basolateral amygdala J. Neurosci. 25 2005 7366 7376
229. J.F. Muller F. Mascagni A.J. McDonald Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala J. Comp. Neurol. 505 2007 314 335
230. K.A. Mulligan I. Tork Serotonergic axons form basket-like terminals in cerebral cortex Neurosci. Lett. 81 1987 7 12
231. K.A. Mulligan I. Tork Serotoninergic innervation of the cat cerebral cortex J. Comp. Neurol. 270 1988 86 110
232. Y. Nagase M. Moritani S. Nakagawa A. Yoshida M. Takemura L.-F. Zhang H. Kida Y. Shigenaga Serotonergic axonal contacts on identified cat trigeminal motoneurons and their correlation with medullary raphe nucleus stimulation J. Comp. Neurol. 384 1997 443 455
233. Y. Nakai S. Shioda H.J. Ochiai J. Kudo A. Hashimoto Ultrastructural relationship between monoamine- and TRH-containing axons in the rat median eminence, as revealed by combined radioautography and immunocytochemistry in the same tissue sections Cell Tissue Res. 230 1983 1 14
234. T. Naumann G.M. Peterson M. Frotscher Fine structure of rat septohippocampal neurons: II. A time course analysis following axotomy J. Comp. Neurol. 325 1992 219 242
235. S. Nedergaard J.P. Bolam S.A. Greenfield Facilitation of a dendritic calcium conductance by 5-hydroxytryptamine in the substantia nigra Nature 333 1988 174 177
236. B.W. Newton B.E. Maley R.W. Hamill Immunohistochemical demonstration of serotonin neurons in autonomic regions of the rat spinal cord Brain Res. 376 1986 155 163
237. N. Nishikawa G.J. Bennett M.A. Ruda G.W. Lu R. Dubner Immunocytochemical evidence for a serotoninergic innervation of dorsal column postsynaptic neurons in cat and monkey: light and electron microscopic observations Neuroscience 10 1983 1333 1340
238. Y. Nojyo Y. Sano Ultrastructure of the serotonergic nerve terminals in the suprachiasmatic and interpeduncular nuclei of rat brains Brain Res. 149 1978 482 488
239. F. Nothias B. Onteniente F. Roudier M. Peschanksi Immunocytochemical study of serotoninergic and noradrenergic innervation of the ventrobasal complex of the rat thalamus Neurosci. Lett. 95 1988 59 63
240. S. Oleskevich L. Descarries Quantified distribution of the serotonin innervation in adult rat hippocampus Neuroscience 34 1990 19 33
241. S. Oleskevich L. Descarries K.C. Watkins P. Séguéla A. Daszuta Ultrastructural features of the serotonin innervation in adult rat hippocampus. An immunocytochemical description in single and serial thin sections Neuroscience 42 1991 777 791
242. S.L. Palay V. Chan-Palay A guide to the synaptic analysis of the neuropil Cold Spring Harb. Symp. Quant. Biol. XL 1976 1 16
243. M. Palkovits M. Brownstein J.M. Saavedra Serotonin content of the brain stem nuclei in the rat Brain Res. 80 1974 237 249
244. G.C. Papadopoulos J.G. Parnavelas Distribution and synaptic organization of serotoninergic and noradrenergic axons in the lateral geniculate nucleus of the rat J. Comp. Neurol. 294 1990 345 355
245. G.G. Papadopoulos J.G. Parnavelas R. Buijs Monoaminergic fibers form conventional synapses in the cerebral cortex Neurosci. Lett. 76 1987 275 279
246. G.G. Papadopoulos J.G. Parnavelas R. Buijs Light and electron microscopic immunocytochemical analysis of the serotonin innervation of the rat visual cortex J. Neurocytol. 26 1987 883 892
247. M. Paré L. Descarries L. Wiklund Innervation and reinnervation of rat inferior olive by neurons containing serotonin and substance P: an immunohistochemical study after 5,6-dihydroxytryptamine lesioning J. Neurocytol. 16 1987 155 167
248. D. Paré D.R. Collins J.G. Pelletier Amygdala oscillations and the consolidation of emotional memories Trends Cogn. Sci. 6 2002 306 314
249. 3H]5-hydroxytryptamine Neuroscience 6 1981 115 138
250. J. Parizek R. Hassler I.J. Bak Light and electron microscopic radioautography of substantia nigra of rat after intraventricular administration of tritium labelled norepinephrine, dopamine, serotonin and the precursors Z. Zellforsch. 115 1971 137 148
251. J.G. Parnavelas H.C. Moises S.G. Speciale The monoaminergic innervation of the rat visual cortex Proc. R. Soc. Lond. B. 223 1985 319 329
252. T. Pasik P. Pasik Serotoninergic afferents in the monkey neostriatum Acta Biol. Acad. Sci. Hung. 33 1982 277 288
253. P. Pasik T. Pasik J. Pecci Saavedra Immunocytochemical localization of serotonin at the ultrastructural level J. Histochem. Cytochem. 30 1982 760 764
254. P. Pasik T. Pasik G.R. Holstein J. Pecci Saavedra Serotoninergic innervation of the monkey basal ganglia: an immunocytochemical light and electron microscopic study J.S. McKenzie R.E. Kenn L.N. Wilcock The Basal Ganglia: Structure and Function 1984 Plenum Press New York, NY 115 129
255. P. Pasik T. Pasik G.R. Holstein Serotonin-immunoreactivity in the monkey lateral geniculate nucleus Exp. Brain Res. 69 1988 662 666
256. C.D. Paspalas G.C. Papadopoulos Serotoninergic afferents preferentially innervate distinct subclasses of peptidergic interneurons in the rat visual cortex Brain Res. 891 2001 158 167
257. D.A. Pasquier M.J. Villar Specific serotonergic projections to the lateral geniculate body from the lateral groups of the raphe dorsalis Brain Res. 249 1982 142 146
258. J.P. Pecci-Saavedra T. Pasik P. Pasik Immunocytochemistry of serotoninergic neurons in the central nervous system of monkeys R. Caputto C. Ajmone Marsan Neural Transmission, Learning and Memory 1983 Raven Press New York, NY 81 96
259. J.P. Pecci-Saavedra A. Brusco S. Peressini D. Oliva A new case for a presynaptic role of dendrites: an immunocytochemical study of the n raphe dorsalis. Neurochem. Res. 11 1986 997 1009
260. G. Pelletier H.W.M. Steinbusch A.A. Verhofstad Immunoreactive substance P and serotonin present in the same dense-core vesicles Nature 293 1981 71 72
261. A. Peters S.L. Palay The morphology of synapses J. Neurocytol. 25 1996 687 700
262. G.M. Peterson T. Naumann M. Frotscher Identified septohippocampal neurons survive axotomy: a fine-structural analysis in the rat Neurosci. Lett. 138 1992 81 85
263. C.F. Phelix Z. Liposits W.K. Paull Monoamine innervation of bed nucleus of stria terminalis: an electron microscopic investigation Brain Res. Bull. 28 1992 949 965
264. V.M. Pickel D.M. Armstrong Ultrastructural localization of monoamines and peptides in rat area postrema Fed. Proc. 43 1984 2949 2951
265. V.M. Pickel J. Chan Ultrastructural localization of the serotonin transporter in limbic and motor compartments of the nucleus accumbens J. Neurosci. 19 1999 7356 7366
266. V.M. Pickel T.H. Joh D. Reis Monoamine synthesizing enzymes in central dopaminergic, noradrenergic and serotonergic neurons. Immunocytochemical localization by light and electron microscopy J. Histochem. Cytochem. 24 1976 792 806
267. V.M. Pickel T.H. Joh D. Reis A serotonergic innervation of noradrenergic neurons in nucleus locus coeruleus: demonstration by immunocytochemical localization of the transmitter specific enzymes tyrosine and tryptophan hydroxylase Brain Res. 131 1977 197 214
268. V.M. Pickel T.H. Joh J. Chan A. Beaudet Serotoninergic terminals: ultrastructure and synaptic interaction with catecholamine-containing neurons in the medial nuclei of the solitary tract J. Comp. Neurol. 225 1984 291 301
269. P.M. Pilowsky D. de Castro I. Llewellyn-Smith J. Lipski M.D. Voss Serotonin immunoreactive boutons make synapses with feline phrenic motoneurons J. Neurosci. 10 1990 1091 1098
270. P. Poulat L. Marlier N. Rajaofetra A. Privat 5-hydroxytryptamine, substance P and thyrotropin-releasing hormone synapses in the intermediolateral cell column of the rat thoracic spinal cord Neurosci. Lett. 136 1992 19 22
271. D.G. Rainnie Serotonergic modulation of neurotransmission in the rat basolateral amygdala J. Neurophysiol. 82 1999 69 85
272. N. Rajaofetra P. Poulat L. Marlier F. Sandillon M.J. Drian N. König F. Famose B. Verschuere D. Gouy M. Geffard A. Privat Transplantation of embryonic serotonin immunoreactive neurons into the transected spinal cord of adult monkey (Macaca fascicularis). Brain Res. 572 1992 329 334
273. R.N. Ranson R.M. Santer A.H.D. Watson The relationship between serotonin, dopamine beta hydroxylase and GABA immunoreactive inputs and spinal preganglionic neurones projecting to the major pelvic ganglion of Wistar rats Neuroscience 141 2006 1935 1949
274. R.W. Rhoades C.A. Bennett-Clarke R.D. Lane M.J. Leslie R.D. Mooney Increased serotoninergic innervation of the hamster's superior colliculus alters retinotectal projections J. Comp. Neurol. 334 1993 397 409
275. 1B serotonin receptors in adult rat brain J. Comp. Neurol. 417 2000 181 194
276. 3H]5-HT by supra-ependymal nerve terminals Brain Res. 134 1977 151 157
277. J.G. Richards H.P. Lorez J.P. Tranzer Indolealkylamine nerve terminals in cerebral ventricles: identification by electron microscopy and fluorescence histochemistry Brain Res. 57 1973 277 288
278. J.G. Richards H.P. Lorez V.E. Colombo R. Guggenheim D. Kiss Supraependymal nerve fibres in human brain: correlative transmission and scanning electron microscopical and fluorescence histochemical studies Neuroscience 5 1980 1489 1502
279. J.G. Richards H.P. Lorez V.E. Colombo R. Guggenheim D. Kiss J.Y. Wu Demonstration of supra-ependymal nerve fibres in human brain and their immunohistochemical identification in rat brain J. Physiol. (Paris) 77 1981 219 224
280. J.-L. Ridet Organisation ultrastructurale et plasticité des systèmes monoaminergiques dans la moelle épinière du rat. Thèse de doctorat 1994 Université de Montpellier II Montpellier 34
281. J.-L. Ridet N. Rajaofetra J.R. Teilhac M. Geffard A. Privat Evidence for non-synaptic serotonergic and noradrenergic innervation of the rat dorsal horn and possible involvement of neuron-glia interactions Neuroscience 52 1993 143 157
282. 3H]serotonin Brain Res. 184 1980 57 83
283. M.A. Ruda B. Allen S. Gobel Ultrastructure of descending serotoninergic axonal endings in layers I and II of the dorsal horn J. Physiol. (Paris) 77 1981 205 209
284. M.A. Ruda B. Allen S. Gobel Ultrastructural analysis of medial brain stem afferents to the superficial dorsal horn Brain Res. 205 1981 175 180
285. M.A. Ruda J. Coffield H.W.M. Steinbusch Immunocytochemical analysis of serotonergic axons in laminae I and II of the lumbar spinal cord of the cat J. Neurosci. 2 1982 1660 1671
286. A.F. Sadikot A. Parent The monoaminergic innervation of the amygdala in the squirrel monkey: an immunohistochemical study Neuroscience 36 1990 431 447
287. S. Saha K. Appenteng T.F.C. Batten Light and electron microscopical localisation of 5-HT immunoreactive boutons in the rat trigeminal motor nucleus Brain Res. 559 1991 145 148
288. H. Saïdi O. Bosler Serotonin reinnervation of the rat organum vasculosum laminae terminalis (OVLT) after 5,7-dihydroxytryptamine deafferentation Brain Res. 530 1990 151 155
289. Y. Sari M.C. Miquel M.J. Brisorgueil G. Ruiz E. Doucet M. Hamon D. Vergé Cellular and subcellular localization of 5-hydroxytryptamine1B receptors in the rat central nervous system: immunocytochemical, autoradiographic and lesion studies Neuroscience 88 1999 899 915
290. N. Schaffar A. Jean A. Calas Radioautographic study of serotoninergic axon terminals in the rat trigeminal motor nucleus Neurosci. Lett. 44 1984 31 36
291. A. Schmied D. Farin M. Amalric J.F. Dormont Changes in motor performance and rubral single unit activity in cats after microinjections of serotonin into the red nucleus area Brain Res. 567 1991 91 100
292. L. Ségu A. Calas The topographical distribution of serotoninergic terminals in the spinal cord of the cat: quantitative radioautographic studies Brain Res. 153 1978 449 464
293. L. Ségu J. Abdelkefi G. Dusticier J. Lanoir High-affinity serotonin binding sites: autoradiographic evidence for their location on retinal afferents in the rat superior colliculus Brain Res. 384 1986 205 217
294. P. Séguéla K.C. Watkins L. Descarries Ultrastructural relationships of serotonin axon terminals in the cerebral cortex of the adult rat J. Comp. Neurol. 289 1989 129 142
295. K.Z. Shen S.W. Johnson 5-HT inhibits synaptic transmission in rat subthalamic nucleus neurons in vitro Neuroscience 151 2008 1029 1033
296. J.F. Smiley P.S. Goldman-Rakic Serotonergic axons in monkey prefrontal cerebral cortex synapse predominantly on interneurons as demonstrated by serial section electron microscopy J. Comp. Neurol. 367 1996 431 443
297. J.F. Smiley M. Subramanian M.M. Mesulam Monoaminergic-cholinergic interactions in the primate basal forebrain Neuroscience 93 1999 817 829
298. J.-J. Soghomonian L. Descarries J. Lanoir Monoamine innervation of the oculomotor nucleus in the rat. A radioautographic study Neuroscience 17 1986 1147 1157
299. J.-J. Soghomonian G. Doucet L. Descarries Serotonin innervation in adult rat neostriatum. I. Quantified regional distribution Brain Res. 425 1987 85 100
300. J.-J. Soghomonian A. Beaudet L. Descarries Ultrastructural relationships of central serotonin neurons N.N. Osborne M. Hamon Neuronal Serotonin 1988 John Wiley & Sons Chichester 57 92
301. J.-J. Soghomonian L. Descarries K.C. Watkins Serotonin innervation in adult rat neostriatum. II. Ultrastructural features: a radioautographic and immunocytochemical study Brain Res. 481 1989 67 86
302. C. Sotelo A. Beaudet Influence of experimentally induced agranularity on the synaptogenesis of serotonin nerve terminals in rat cerebral cortex Proc. R. Soc. Lond. B 206 1979 133 138
303. I.M. Stanford M.A. Kantaria H.S. Chahal K.C. Loucif C.L. Wilson 5-Hydroxytryptamine induced excitation and inhibition in the subthalamic nucleus: action at 5-HT(2C), 5-HT(4) and 5-HT(1A) receptors Neuropharmacology 49 2005 1228 1234
304. H.W.M. Steinbusch Distribution of serotonin immunoreactivity in the central nervous system of the rat Cell bodies and terminals. Neuroscience 6 1981 557 618
305. H.V.M. Steinbusch Serotonin-immunoreactive neurons and their projections in the CNS A. Björklund T. Hökfelt M.J. Kuhar Handbook of Chemical Neuroanatomy. Vol. 3, Classical Transmitters and Transmitter Receptors in the CNS, Part II 1984 Elsevier Amsterdam 68 125
306. H.V.M. Steinbusch R. Nieuwenhuys Localization of serotonin-like immunoreactivity in the central nervous system and pituitary of the rat, with special references to the innervation of the hypothalamus Adv. Exp. Med. Biol. 133 1981 7 35
307. T.L. Steininger B.H. Wainer R.D. Blakely D.B. Rye Serotonergic raphe dorsalis projections to the cholinergic and noncholinergic neurons of the pedonculopontine tegmental region: a light and electron microscopic anterograde tracing and immunocytochemical study J. Comp. Neurol. 382 1997 302 322
308. M. Steriade R.W. McCarley Brain Control of Sleep and Wakefulness 2005 Kluwer Academic Press New York, NY
309. G.E. Stutzmann J.E. LeDoux GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: a mechanism for modulation of sensory inputs related to fear conditioning J. Neurosci. 19 1999 RC8
310. Q. Tai K.L. Palazzolo G. Goshgarian Synaptic plasticity of 5-hydroxytryptamine-immunoreactive terminals in the phrenic nucleus following spinal cord injury: a quantitative electron microscopic analysis J. Comp. Neurol. 386 1997 613 624
311. Y. Takeuchi Y. Sano Serotonin distribution in the circumventricular organs of the rat. An immunohistochemical study Anat. Embryol. (Berl.) 167 1983 311 319
312. Y. Takeuchi Y. Sano Immunohistochemical demonstration of serotonin-containing nerve fibers in the inferior olivary complex of the rat, cat and monkey Cell Tissue Res. 231 1983 17 28
313. Y. Takeuchi H. Kimura Y. Sano Immunohistochemical demonstration of serotonin-containing nerve fibers in the cerebellum Cell Tissue Res. 226 1982 1 12
314. Y. Takeuchi M. Kojima T. Matsuura Y. Sano Serotonergic innervation on the motoneurons in the mammalian brainstem. Light and electron microscopic immunohistochemistry Anat. Embryol. (Berl.) 167 1983 321 333
315. J.-H. Tao-Cheng F.C. Zhou Differential polarization of serotonin transporters in axons versus soma-dendrites: an immunogold electron microscopy study Neuroscience 94 1999 821 830
316. T. Tashiro T. Satoda R. Matsushima N. Mizuno Enkephalin-, substance P- and serotonin-like immunoreactive axonal varicosities in close apposition to perikarya of mesencephalic trigeminal nucleus neurons in the cat Brain Res. 494 1989 162 167
317. G. Tramu A. Pillez J. Leonardelli Serotonin axons of the ependyma and circumventricular organs in the forebrain of the guinea pig. An immunohistochemical study Cell Tissue Res. 228 1983 297 311
318. S. Trottier B. Evrard J.P. Vignal J.M. Scarabin P. Chauvel The serotonergic innervation of the cerebral cortex in man and its changes in focal cortical dysplasia Epilepsy Res. 25 1996 79 106
319. B. Ulfhake U. Arvidsson S. Cullheim T. Hökfelt E. Brodin A. Verhofstad T. Visser An ultrastructural study of 5-hydroxytryptamine-, thyrotropin-releasing hormone- and substance P-immunoreactive axonal boutons in the motor nucleus of spinal cord segments L7- S1 in the adult cat Neuroscience 23 1987 917 929
320. D. Umbriaco S. Garcia C. Beaulieu L. Descarries Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1) Hippocampus 5 1995 605 620
321. L.D. Van de Kar S.A. Lorens Differential serotonergic innervation of individual hypothalamic nuclei and other forebrain regions by the dorsal and median midbrain raphe nuclei Brain Res. 162 1979 45 54
322. E.J. Van Bockstaele V.M. Pickel Ultrastructure of serotonin-immunoreactive terminals in the core and shell of the rat nucleus accumbens: cellular substrates for interactions with catecholamine afferents J. Comp. Neurol. 334 1993 603 617
323. E.J. Van Bockstaele D.M. Cestari V.M. Pickel Synaptic structure and connectivity of serotonin terminals in the ventral tegmental area: potential sites for modulation of mesolimbic dopamine neurons Brain Res. 647 1994 307 322
324. E.J. Van Bockstaele J. Chan V.M. Pickel Pre- and postsynaptic sites for serotonin modulation of GABA-containing neurons in the shell region of the rat nucleus accumbens J. Comp. Neurol. 370 1996 116 128
325. M.G. Van Luijtelaar F.G. Wouterlood J.A. Tonnaer H.W.M. Steinbusch Ultrastructure of aberrant serotonin-immunoreactive fibers in the caudate putamen complex of the aged rat Synapse 8 1991 162 168
326. P.L. Vera V.R. Holets K.E. Miller Ultrastructural evidence of synaptic contacts between substance P-, enkephalin, and serotonin-immunoreactive terminals and retrogradely labeled sympathetic preganglionic neurons in the rat: a study using a double-peroxidase procedure Synapse 6 1990 221 229
327. R.P. Vertes A PHA-L analysis of ascending projections of the raphe dorsalis in the rat J. Comp. Neurol. 313 1991 643 668
328. R.P. Vertes B. Kocsis Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus Neuroscience 81 1997 893 926
329. R.P. Vertes G.F. Martin Radioautographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the raphe medianus in the rat J. Comp. Neurol. 275 1988 511 541
330. M.J. Villar M.L. Vitale T. Hökfelt A.A. Verhofstad Dorsal raphe serotoninergic branching neurons projecting both to the lateral geniculate body and superior colliculus: a combined retrograde tracing-immunohistochemical study in the rat J. Comp. Neurol. 277 1988 126 140
331. M.-J. Wallman M. Parent L. Descarries A. Parent Serotonin innervation of the subthalamic nucleus in monkey and human. Program No. 513.7 2007. Abstract Viewer/Itinerary Planner 2007 Society for Neuroscience Washington, DC Online
332. Q.-P. Wang J.-L. Guan S. Shioda Synaptic contacts between serotonergic and cholinergic neurons in the rat raphe dorsalis and laterodorsal tegmental nucleus Neuroscience 97 2000 553 563
333. R.Y. Wang G.K. Aghajanian Collateral inhibition of serotonergic neurones in the rat raphe dorsalis: pharmacological evidence Neuropharmacology 17 1978 819 825
334. R.Y. Wang G.K. Aghajanian Correlative firing patterns of serotonergic neurons in rat raphe dorsalis J. Neurosci. 2 1982 11 16
335. K.N. Westlund L.S. Sorkin D.G. Ferrington S.M. Carlton H.H. Willcockson W.D. Willis Serotoninergic and noradrenergic projections to the ventral posterolateral nucleus of the monkey thalamus J. Comp. Neurol. 295 1990 197 207
336. S.R. White R.S. Neuman Faciliatation of spinal motoneurone excitability by 5-hydroxytryptamine and noradrenaline Brain Res. 188 1980 119 127
337. L. Wiklund A. Björklund B. Sjölund The indolaminergic innervation of the inferior olive. 1. Convergence with the direct spinal afferents in the areas projecting to the cerebellar anterior lobe Brain Res. 131 1977 1 21
338. L. Wiklund L. Descarries K. Møllgärd Serotoninergic axon terminals in the rat dorsal accessory olive: normal ultrastructure and light microscopic demonstration of regeneration after 5,6-dihydroxytryptamine lesioning J. Neurocytol. 10 1981 1009 1027
339. J.O. Willoughby W.W. Blessing Origin of serotonin innervation of the arcuate and ventromedial hypothalamic region Brain Res. 418 1987 170 173
340. J.R. Wilson A.E. Hendrickson Serotonergic axons in the monkey's lateral geniculate nucleus Vis. Neurosci. 1 1988 125 133
341. Z. Xiang L. Wang S.T. Kitai Modulation of spontaneous firing in rat subthalamic neurons by 5-HT receptor subtypes J. Neurophysiol. 93 2005 1145 1157
342. H. Yamamoto M. Fujimiya Y. Shirai M. Nakashita M. Oyasu N. Saito Immunohistochemical localization of serotonin transporter in normal and colchicine treated rat brain Neurosci. Res. 32 1998 305 312
343. F.C. Zhou J.-H. Tao-Cheng L. Segu T. Patel Y. Wang Serotonin transporters are located on the axons beyond the synaptic junctions: anatomical and functional evidence Brain Res. 805 1998 241 254
344. C. Kohler The distribution of serotonin binding sites in the hippocampal region of the rat brain. An autoradiographic study Neuroscience 13 1984 667 680
345. A.R. Woodruff P. Sah Inhibition and synchronization of basal amygdala principal neuron spiking by parvalbumin-positive interneurons J. Neurophysiol. 98 2007 2956 2961