Interactions between TrkB Signaling and Serotonin Excess in the Developing Murine Somatosensory Cortex: A Role in Tangential and Radial Organization of Thalamocortical Axons

Journal of Neuroscience

Volumn 22, Issue 12, 2002, Pages 4987-5000

  Vitalis, Tania ^a,d   Cases, Olivier ^b   Gillies, Katy ^a   Hanoun, Naima ^b   Hamon, Michel ^b   Seif, Isabelle ^c   Gaspar, Patricia ^b   Kind, Peter ^a   Price, David J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c Faculté de Pharmacie   (France)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

BDNF; NT 4; Serotonin; Somatosensory cortex; Thalamocortical axons; TrkB signaling

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; MESSENGER RNA; NEUROTROPHIN; SEROTONIN; 5 HYDROXYINDOLEACETIC ACID; AMINE OXIDASE (FLAVIN CONTAINING); CYTOCHROME C OXIDASE; NERVE GROWTH FACTOR; NEUROTROPHIN 4;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXAMINATION; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; MOUSE; MUTATION; NERVE FIBER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; THALAMOCORTICAL TRACT; THALAMUS; VISUAL CORTEX; ANIMAL; BIOSYNTHESIS; BRAIN CORTEX; CELL DEATH; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; MOUSE MUTANT; ULTRASTRUCTURE;

ANIMALS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DEATH; CEREBRAL CORTEX; ELECTRON TRANSPORT COMPLEX IV; HYDROXYINDOLEACETIC ACID; KINETICS; MICE; MICE, KNOCKOUT; MONOAMINE OXIDASE; NERVE GROWTH FACTORS; RECEPTOR, TRKB; RNA, MESSENGER; SEROTONIN; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; THALAMUS;

EID: 0037096256     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-12-04987.2002     Document Type: Article

References (51)

1. Agmon A, Yang LT, O'Dowd DK, Jones EG (1993) Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex. J Neurosci 13:5365-5382.
2. Agmon A, Yang LT, Jones EG, O'Dowd DK (1995) Topographical precision in the thalamic projection to neonatal mouse barrel cortex. J Neurosci 15:549-561.
3. Alcantara S, Frisen J, del Rio JA, Soriano E, Barbacid M, Silos-Santiago I (1997) TrkB signaling is required for postnatal survival of CNS neurons and protects hippocampal and motor neurons from axotomy-induced cell death. J Neurosci 17:3623-3633.
4. Alsina B, Vu T, Cohen-Cory S (2001) Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat Neurosci 4:1093-1101.
5. Bagnard D, Betz H, Gotz M, Puschel AW, Boltz J (1996) Do semaphorins act as guidance molecules for afferent and efferent projections in the developing cerebral cortex? Soc Neurosci Abstr 22:1473.
6. Bagnard D, Chounlamountri N, Puschel AW, Bolz J (2001) Axonal surface molecules act in combination with semaphorin 3a during the establishment of corticothalamic projections. Cereb Cortex 11:278-285.
7. Bennett-Clarke CA, Leslie MJ, Lane RD, Rhoades RW (1994) Effects of serotonin depletion on vibrissa-related patterns of thalamic afferents in the rat's somatosensory cortex. J Neurosci 14:7594-7607.
8. Blue ME, Martin LJ, Brennan EM, Johnston MV (1997) Ontogeny of non-NMDA glutamate receptors in rat barrel field cortex. I. Metabotropic receptors. J Comp Neurol 386:16-28.
9. Bolz J, Novak N, Staiger V (1992) Formation of specific afferent connections in organotypic slice culture from rat visual cortex cocultured with lateral geniculate nucleus. J Neurosci 12:3054-3070.
10. Cabelli RJ, Hohn A, Shatz CJ (1995) Inhibition of ocular dominance column formation by infusion of NT4/5 or BDNF. Science 267:1662-1666.
11. Cabelli RJ, Shelton DL, Segal RA, Shatz CJ (1997) Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19:63-76.
12. Cases O, Seif I, Grimsby J, Gaspar P, Chen K, Pournin S, Muller U, Aguet M, Babinet C, Shih JC, De Maeyer E (1995) Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268:1763-1766.
13. Cases O, Vitalis T, Seif I, De Maeyer E, Sotelo C, Gaspar P (1996) Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period. Neuron 16:297-307.
14. Catalano SM, Robertson RT, Killackey HP (1996) Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J Comp Neurol 367:36-53.
15. Chavis P, Westbrook G (2001) Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411:317-321.
16. Cohen-Cory S (1999) BDNF modulates, but does not mediate, activity-dependent branching and remodeling of optic axon arbors in vivo. J Neurosci 19:9996-10003.
17. Cohen-Cory S, Fraser SE (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodeling in vivo. Nature 378:192-196.
18. Das KP, Chao SL, White LD, Haines WT, Harry GJ, Tilson HA, Barone Jr S (2001) Differential patterns of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNA and protein levels in developing regions of rat brain. Neuroscience 103:739-761.
19. Fontaine P, Changeux JP (1989) Localization of nicotinic acetylcholine receptor alpha-subunit transcripts during myogenesis and motor end-plate development in the chick. J Cell Biol 103:1025-1037.
20. Gates MA, Tai CC, Macklis JD (2000) Neocortical neurons lacking the protein-tyrosine kinase B receptor display abnormal differentiation and process elongation in vitro and in vivo. Neuroscience 98:437-447.
21. Hamon M, Fattaccini CM, Adrien J, Gallissot MC, Martin P, Gozlan H (1988) Alteration of central serotonin and dopamine turnover in rats treated with ipsapirone and other 5-hydroxytryptamine1A agonists with potential anxyolytic properties. J Pharmacol Exp Ther 246:745-752.
22. Hata Y, Oshshima M, Ichisaka S, Wakita M, Fukuda M, Tsumoto T (2000) Brain-derived neurotrophic factor expands ocular dominance columns in visual cortex in monocularly deprived and nondeprived kittens but does not in adult cats. J Neurosci 20:RC57(1-5).
23. Henderson TA, Mosconi TM, Foschini DR, Silos-Santiago I, Barbacid M, Jacquin MF (1995) Whisker-related patterning in the cerebral cortex of trkA, trkB, or trkC knock-out mice. Soc Neurosci Abstr 21:279.
24. Hsueh YP, Sheng M (1998) Eph receptors, ephrins, and PDZs gather in neuronal synapses. Neuron 21:1453-1463.
25. Itami C, Mizuno K, Kohno T, Nakamura S (2000) Brain-derived neurotrophic factor requirement for activity-dependent maturation of glutamatergic synapse in developing mouse somatosensory cortex. Brain Res 857:141-150.
26. Klein R, Smeyne RJ, Wurst W, Long LK, Auerbach BA, Joyner AL, Barbacid M (1993) Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75:113-122.
27. Lebrand C, Cases O, Aldebrecht A, Doye A, Alvarez C, El Mestikawy S, Seif I, Gaspar P (1996) Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 17:823-835.
28. Lebrand C, Cases O, Werhle R, Blakely RD, Edwards RH, Gaspar P (1998) Transient developmental expression of monoamine transporters in the rodent brain. J Comp Neurol 401:506-524.
29. Lieske V, Bennett-Clarke CA, Rhoades RW (1999) Effects of serotonin on neurite outgrowth from thalamic neurons in vitro. Neuroscience 90:967-974.
30. Lotto B, Upton L, Price DJ, Gaspar P (1999) Serotonin receptor activation enhances neurite outgrowth of thalamic neurones in rodents. Neurosci Lett 269:87-90.
31. Masana Y, Wanaka A, Kato H, Asai T, Tohyama M (1993) Localization of trkB mRNA in postnatal brain development. J Neurosci Res 35:468-479.
32. Molnar Z, Blakemore C (1995) How do thalamic axons find their way to the cortex? Trends Neurosci 9:389-396.
33. Molnar Z, Blakemore C (1999) Development of signals influencing the growth and termination of thalamocortical axons in organotypic culture. Exp Neurol 156:363-393.
34. Molnar Z, Adams R, Blakemore C (1998) Mechanisms underlying the establishment of thalamocortical connections in the rat. J Neurosci 18:5723-5745.
35. Munoz A, Liu XB, Jones EG (1999) Development of metabotropic glutamate receptors from trigeminal nuclei to barrel cortex in postnatal mouse. J Comp Neurol 409:549-566.
36. Noctor SC, Palmer SL, McLaughlin DF, Juliano SL (2001) Disruption of layers 3 and 4 during development results in altered thalamocortical projections in ferret somatosensory cortex. J Neurosci 21:3184-3195.
37. Obst-Pernberg K, Redies C (1999) Cadherins and synaptic specificity. J Neurosci Res 38:130-138.
38. Palmer SL, Noctor SC, Jablonska B, Juliano SL (2001) Laminar specific alterations of thalamocortical projections in organotypic cultures following layer 4 disruption in ferret somatosensory cortex. Eur J Neurosci 13:1559-1571.
39. Pollock GS, Vernon E, Forbes ME, Yan Q, Ma Y-T, Hsieh T, Robichon R, Frost DO, Johnson JE (2001) Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum. J Neurosci 21:3923-3931.
40. Rice FL, Van der Loos H (1977) Development of the barrels and barrel field in the somatosensory cortex of the mouse. J Comp Neurol 171:545-560.
41. Salichon N, Gaspar P, Upton L, Picaud S, Hanoun N, Hamon M, De Maeyer E, Murphy DL, Mossner R, Lesch KP, Hen R, Seif I (2001) Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase A and 5-HT transporter knock-out mice. J Neurosci 21:884-896.
42. Senft SL, Woolsey TA (1991) Growth of thalamic afferents into mouse barrel cortex. Cereb Cortex 1:308-335.
43. Sermasi E, Margotti E, Cattaneo A, Domenici L (2000) TrkB signalling controls LTP but not LTD expression in the developing rat visual cortex. Eur J Neurosci 12:1411-1419.
44. Singh TD, Mizuko K, Kohno T, Nakamura S (1997) BDNF and trkB mRNA expression in neurons of the neonatal mouse barrel field cortex: normal development and plasticity after cauterising facial vibrissae. Neurochem Res 7:791-797.
45. Skaliora I, Singer W, Betz H, Puschel AW (1998) Differential patterns of semaphorin expression in the developing rat brain. Eur J Neurosci 10:1215-1229.
46. Vanderhaeghen P, Lu Q, Prakash N, Frisen J, Walsh CA, Frostig RD, Flanagan JG (2000) A mapping label required for normal scale of body representation in the cortex. Nat Neurosci 3:358-365.
47. Vitalis T, Cases O, Callebert J, Launay JM, Price DJ, Seif I, Gaspar P (1998) Effects of monoamine oxidase A inhibition on barrel formation in the mouse somatosensory cortex. Determination of a sensitive developmental period. J Comp Neurol 393:169-184.
48. Wong-Riley MTT, Welt C (1980) Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc Natl Acad Sci USA 77:2333-2337.
49. Xu B, Zang K, Ruff NL, Zhang YA, McConnel SK, Stryker MP, Reichardt LF (2000) Cortical degeneration in the absence of neurotrophin signaling: dendritic retraction and neuronal loss after removal of the receptor TrkB. Neuron 26:233-245.
50. Yacoubian TA, Lo DC (2000) Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat Neurosci 3:342-349.
51. Zetterstrom TS, Pei Q, Madhav TR, Coppell AL, Lewis L, Grahame-Smith DG (1999) Manipulation of brain 5HT levels affect gene expression for BDNF in rat brain. Neuropharmacology 38:1063-1073.