Transient uptake and storage of serotonin in developing thalamic neurons

Neuron

Volumn 17, Issue 5, 1996, Pages 823-835

  Lebrand, Cécile ^a   Cases, Olivier ^b   Adelbrecht, Christine ^a   Doye, Anne ^a   Alvarez, Chantal ^a   El Mestikawy, Salah ^a   Seif, Isabelle ^b   Gaspar, Patricia ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MONOAMINE; SEROTONIN;

ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTONIN UPTAKE; SOMATOSENSORY CORTEX; THALAMUS; VISUAL CORTEX;

EID: 0030292916     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80215-9     Document Type: Article

References (71)

1. Agmon, A., and O'Dowd, D.K. (1992). NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition. J. Neurophysiol. 68, 345-348.
2. Armstrong-James, M., Welker, E., and Callahan, C.A. (1993). The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex. J. Neurosci. 13, 2149-2160.
3. Bear, M.F., and Singer, W. (1986). Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172-176.
4. Bennett-Clarke, C.A., Chiaia, N.L., Crissman, R.S., and Rhoades, R.W. (1991). The source of the transient serotoninergic input to the developing visual and somatosensory cortices in rat. Neuroscience 43, 163-183.
5. Bennett-Clarke, C.A., Leslie, M.J., Chiaia, N.L., and Rhoades, R.W. (1993). Serotonin 1B receptors in the developing somatosensory and visual cortices are located on thalamocortical axons. Proc. Natl. Acad. Sci. USA 90, 153-157.
6. Bennett-Clarke, C.A., Hankin, M.H., Leslie, M.J., Chiaia, N.L., and Rhoades, R.W. (1994a). Patterning of the neocortical projections from the raphe nuclei in perinatal rats: investigation of potential organizational mechanisms. J. Comp. Neurol. 348, 277-290.
7. Bennett-Clarke, C.A., Leslie, M.J., Lane, R.D., and Rhoades, R.W. (1994b). Effect of serotonin depletion on vibrissa-related patterns of thalamic afferents in the rat's somatosensory cortex. J. Neurosci. 14, 7594-7607.
8. Bennett-Clarke, C.A., Lane, R.D., and Rhoades, R.W. (1995). Fenfluramine depletes serotonin from the developing cortex and alters thalamocortical organisation. Brain Res. 702, 255-260.
9. Berger, B., Trottier, S., Verney, C., Gaspar, P., and Alvarez, C. (1988). Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: a radioautographic study. J. Comp. Neurol. 273, 99-119.
10. Bina, K.G., Guzman, P., Broide, R.S., Leslie, F.M., Smith, M.A., and O'Dowd, D.K. (1995). Localization of α7 nicotinic receptor subunit mRNA and α-bungarotoxin binding sites in developing mouse somatosensory thalamocortical system. J. Comp. Neurol. 363, 321-332.
11. Blakely, R.D., Berson, H.E., Fremeau, R.T., Caron, M.G., Peek, M.M., Prince, H.K., and Bradley, C.C. (1991). Cloning and expression of a functional serotonin transporter from rat brain. Nature 354, 66-70.
12. Blue, M.E., and Johnston, M.V. (1995). The ontogeny of glutamate receptors in rat barrel field cortex. Dev. Brain Res. 84, 11-25.
13. Blue, M.E., Erzurumlu, R.S., and Jhaveri, S. (1991). A comparison of pattern formation by thalamocortical and serotonergic afferents in the rat barrel field cortex. Cereb. Cortex 1, 380-389.
14. Buznikov, G.A., and Shmukler, Y.B. (1981). Possible role of "prenervous" neurotransmitters in cellular interactions of early embryogenesis: a hypothesis. Neurochem. Res. 6, 55-68.
15. Cases, O., Seif, I., Grimsby, J., Gaspar, P., Chen, K., Pournin, S., Müller, U., Aguet, M., Babinet, C., Shih, J.C., and De Maeyer, E. (1995). Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268, 1763-1766.
16. Cases, O., Vitalis, T., Seif, I., De Maeyer, E., Sotelo, C., and Gaspar, P. (1996). Lack of barrels in the somatosensory cortex of monoamine oxidase A deficient mice: role of serotonin excess during the critical period. Neuron 16, 297-307.
17. Cohen, Z., Ehret, M., Maitre, M., and Hamel, E. (1995). Ultrastructural analysis of tryptophan hydroxylase immunoreactive nerve terminals in the rat cerebral cortex and hippocampus: their association with local blood vessels. Neuroscience 66, 555-569.
18. Consolazione, A., Milstein, C., Wright, B., and Cuello, A.C. (1981). Immunocytochemical detection of serotonin with monoclonal antibodies. J. Histochem. Cytochem. 29, 1425-1430.
19. Crair, M.C., and Malenka, R.C. (1995). A critical period for long-term potentiation at thalamocortical synapses. Nature 375, 325-328.
20. D'Amato, R.J., Blue, M.E., Largent, B.L., Lynch, D.R., Ledbetter, D.J., Molliver, M.E., and Snyder, S.H. (1987a). Ontogeny of the serotonergic projection to rat neocortex: transient expression of a dense innervation to primary sensory areas. Proc. Natl. Acad. Sci. USA 84, 4322-4326.
21. 3H]Imipramine. J. Pharmacol. Exp. Ther. 242, 364-371.
22. Darmon, M.C., Guibert, B., Leviel, V., Ehret, M., Maitre, M., and Mallet, J. (1988). Sequence of two mRNAS encoding active rat tryptophan hydroxylase. J. Neurochem. 51, 312-316.
23. 2-receptor: an up-date. In Cardiovascular Pharmacology of 5-Hydroxytryptamine, P.R. Saxena, D.I. Wallis, W. Wouters, and P. Sevan, eds. (Dordrecht, Netherlands: Kluwer Academic Publishers), pp. 445-457.
24. Dori, I., Dinopoulos, A., Blue, M.E., and Parnavelas, J.G. (1996). Regional differences in the ontogeny of the serotonergic projection to the cerebral cortex. Exp. Neurol. 138, 1-15.
25. Doucet, G., Descarries, L., Audet, M.A., Garcia, S., and Berger, B. (1988). Radioautographic method for quantitating regional monoamine innervations in the rat brain. Brain Res. 441, 233-259.
26. Dyck, R.H., and Cynader, M.S. (1993). Autoradiographic localization of serotonin receptor subtypes in cat visual cortex: transient regional, laminar, and columnar distributions during postnatal development. J. Neurosci. 13, 4316-4338.
27. Erickson, J.D., Eiden, L.E., and Hoffman, B.J. (1992). Expression cloning of a reserpine-sensitive vesicular monoamine transporter. Proc. Natl. Acad. Sci. USA 89, 10993-10997.
28. Faure, M.P., Nouel, D., and Beaudet, A. (1995). Axonal and dendritic transport of internalized neurotensin in rat mesostriatal dopaminergic neurons. Neuroscience 68, 519-529.
29. Fontaine, B., and Changeux, J.P. (1989). Localization of nicotinic acetylcholine receptor α-subunit transcripts during myogenesis and motor endplate development in the chick. J. Cell Biol. 108, 1025-1037.
30. Fox, K., and Zahs, K. (1994). Critical period control in sensory cortex. Curr. Opin. Neurobiol. 4, 112-119.
31. Fujimiya, M., Kimura, H., and Maeda, T. (1986). Postnatal development of serotonin nerve fibers in the somatosensory cortex of mice studied by immunohistochemistry. J. Comp. Neurol. 246, 191-201.
32. Fujita, M., Shimada, S., Maeno, H., Nishimura, T., and Tohyama, M. (1993). Cellular localization of serotonin transporter mRNA in the rat brain. Neurosci. Lett. 162, 59-62.
33. Fuller, R.W., Snoddy, H.D., and Roberston, D.W. (1988). Mechanisms of effects of d-fenfluramine on brain serotonin metabolism in rats: uptake inhibition versus release. Pharmacol. Biochem. Behav. 30, 715-721.
34. Gérard, A., Gérard, H., and Dollander, A. (1978). Capture et rétention de sérotonine tritiée par la chorde dorsale d'embryon de poulet. C.R. Acad. Sci. (Paris) 286, 891-894.
35. 6 receptor mRNA in the central nervous system of control or 5,7-dihydroxytryptamine-treated rats. Synapse 23, 164-173.
36. Gonzalez, A.M., Walther, D., Pazos, A., and Uhl, G.R. (1994). Synaptic vesicular monoamine transporter expression: distribution, and pharmacologic profile. Mol. Brain Res. 22, 219-226.
37. Gu, Q., and Singer, W. (1995). Involvement of serotonin in developmental plasticity of kitten visual cortex. Eur. J. Neurosci. 7, 1146-1153.
38. Henry, J.P., and Scherman, D. (1989). Radioligands of the vesicular transporter and their use as markers of monoamine storage vesicles. Biochem. Pharmacol. 38, 2395-2404.
39. Hoffman, B.J., Mezey, E., and Brownstein, M.J. (1991). Cloning of a serotonin transporter affected by antidepressants. Science 254, 579-580.
40. Jensen, K.F., and Killackey, H.P. (1987). Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. II. The altered morphology of thalamocortical afferents following neonatal infraorbital nerve cut. J. Neurosci. 7, 3544-3553.
41. Johnson, R.R., and Burkhalter, A. (1992). Evidence for excitatory amino acid neurotransmitters in the geniculo-cortical pathway and local projections within rat primary visual cortex. Exp. Brain Res. 89, 20-30.
42. Kasamatsu, T., Pettigrew, J.D., and Ary, M. (1979). Restoration of visual cortical plasticity by local microperfusion of norepinephrine. J. Comp. Neurol. 185, 163-182.
43. Kimelberg, H.K., and Katz, D.M. (1985). High-affinity uptake of serotonin into immunocytochemically identified astrocytes. Science 228, 889-891.
44. Kojima, T., Homma, S., Sako, H., Shimizu, I., Okada, A., and Okado, N. (1988). Developmental changes in density and distribution of serotonergic fibers in the chick spinal cord. J. Comp. Neurol. 267, 580-589.
45. Krejci, E., Gasnier, B., Botton, D., Isambert, M.F., Sagne, C., Gagnon, J., Massoulie, J., and Henry, J.P. (1993). Expression and regulation of the bovine vesicular monoamine transporter gene. FEBS Lett. 335, 27-32.
46. Kristt, D.A. (1979). Development of neocortical circuitry: quantitative ultrastructural analysis of putative monoaminergic synapses. Brain Res. 178, 69-88.
47. Kristt, D.A. (1989). Acetylcholinesterase in immature thalamic neurons: relation to afferentation, development, regulation and cellular distribution. Neuroscience 29, 27-43.
48. Lauder, J.M. (1993). Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci. 16, 233-239.
49. Lesch, K.P., Aulakh, C.S., Wolozin, B.L., Tolliver, T.J., Hill, J.L., and Murphy, D.L. (1993). Regional brain expression of serotonin transporter mRNA and its regulation by reuptake inhibiting antidepressants. Mol. Brain Res. 17, 31-35.
50. Liu, Y., Peter, D., Roghani, A., Schuldiner, S., Privé, G.G., Eisenberg, D., Brecha, N., and Edwards, R.H. (1992). A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter. Cell 70, 539-551.
51. Lombardo, A., Rabacchi, S.A., Cremisi, F., Pizzorusso, T., Cenni, M.C., Possenti, R., Barsacchi, G., and Maffei, L. (1995). A developmentally regulated nerve growth factor-induced gene, VGF, is expressed in geniculocortical afferents during synaptogenesis. Neuroscience 65, 997-1008.
52. Masana, Y., Wanaka, A., Kato, H., Asai, T., and Tohyama, M. (1993). Localization of trkB mRNA in postnatal brain development. J. Neurosci. Res. 35, 468-479.
53. Moiseiwitsch, J.R.D., and Lauder, J.M. (1995). Serotonin regulates mouse cranial neural crest migration. Proc. Natl. Acad. Sci. USA 92, 7182-7186.
54. Osterheld-Haas, M.C., and Hornung, J.P. (1996). Laminar development of the mouse barrel cortex: effects of neurotoxins against monoamines. Exp. Brain Res. 110, 183-195.
55. Osterheld-Haas, M.C., Van der Loos, H., and Hornung, J.P. (1994). Monoaminergic afferents to cortex modulate structural plasticity in the barrelfield of the mouse. Dev. Brain Res. 77, 189-202.
56. Ottersen, O.P., and Storm-Mathisen, J. (1984). Neurons containing or accumulating transmitter amino acids. In Handbook of Chemical Neuroanatomy, Volume 3: Classical Transmitters and Transmitter Receptors in the CNS, A. Björklund, T. Hökfelt, and M.J. Kuhar, eds. (Amsterdam: Elsevier), pp. 141-246.
57. Ovalle, S., Casanova, E., Garate, C., Llamazares, A.A., Chinchetru, M.A., and Calvo, P. (1995). Immunodetection of serotonin transporter from mouse brain. Neuroreport 6, 2353-2356.
58. Peter, D., Liu, Y., Sternin, C., de Giorgio, R., Brecha, N., and Edwards, R.H. (1995). Differential expression of two vesicular monoamine transporters. J. Neurosci. 15, 6179-6188.
59. Qian, Y., Melikian, H.E., Rye, D.B., Levey, A.I., and Blakely, R.D. (1995). Identification and characterization of antidepressant-sensitive serotonin transporter proteins using site-specific antibodies. J. Neurosci. 15, 1261-1274.
60. Rhoades, R.W., Bennett-Clarke, C.A., Chiaia, N.L., White, F.A., McDonald, G.J., Haring, J.H., and Jacquin, M.F. (1990). Development and lesion induced reorganization of the cortical representation of the rat's body surface as revealed by immunocytochemistry for serotonin. J. Comp. Neurol. 293, 190-207.
61. Rhoades, R.W., Bennett-Clarke, C.A., Shi, M-Y., and Mooney, R.D. (1994). Effects of 5-HT on thalamocortical synaptic transmission in the developing rat. J. Neurophysiol. 72, 2438-2450.
62. Rudnick, G., and Clark, J. (1993). From synapse to vesicle: the reuptake and storage of biogenic amine neurotransmitters. Biochem. Biophys. Acta 1144, 249-263.
63. Schlaggar, B.L., Fox, K., and O'Leary D.D.M. (1993). Postsynaptic control of plasticity in developing somatosensory cortex. Nature 364, 623-626.
64. 125I-RTI-55 autoradiography, in situ hybridization and immunocytochemistry. Soc. Neurosci., 344.9, 886.
65. Shuey, D.L., Sadler, T.W., and Lauder, J.M. (1992). Serotonin as a regulator of craniofacial morphogenesis: site specific malformations following exposure to serotonin uptake inhibitors. Teratology 46, 367-378.
66. Shuey, D.L., Sadler, T.W., Tamir, H., and Lauder, J.M. (1993). Serotonin and morphogenesis. Transient expression of serotonin uptake and binding protein during craniofacial morphogenesis in the mouse. Anat. Embryol. (Berl.) 187, 75-85.
67. Steinbusch, H.W.M. (1984). Serotonin-immunoreactive neurons and their projections in the CNS. In Handbook of Chemical Neuroanatomy, Volume 3. Classical Transmitters and Transmitter Receptors in the CNS, A. Björklund, T. Hökfelt, and M.J. Kuhar, eds. (Amsterdam: Elsevier), pp. 68-125.
68. Tramu, G., Pillez, A., and Leonardelli, J. (1983). Serotonin axons of the ependyma and circumventricular organs in the forebrain of the guinea pig. An immunohistochemical study. Cell Tiss. Res. 228, 297-312.
69. Van der Loos, H., Welker, E., Dörfl, J., and Hoogland, P.V. (1991). Brain maps: development, plasticity and distribution of signals beyond. In The Neocortex, Ontogeny and Phylogeny, B.L. Finlay, G. Innocenti, and H. Scheich, eds. (New York: Plenum Press), pp. 229-236.
70. Wallace, J.A. (1982). Monoamines in the early chick embryo: demonstration of serotonin synthesis and the regional distribution of serotonin-concentrating cells during morphogenesis. Am. J. Anat. 165, 261-276.
71. Wallace, J.A., and Lauder, J.M. (1992). Development of the serotonergic system in rat and chick embryos. In Handbook of Chemical Neuroanatomy, Volume 10: Ontogeny of Transmitters and Peptides in the CNS, A. Björklund, T. Hökfelt, and M. Tohyama, eds.(Amsterdam: Elsevier), pp. 619-645.