Neurotrophin-3 is required for appropriate establishment of thalamocortical connections

Neuron

Volumn 36, Issue 4, 2002, Pages 623-634

  Ma, Long ^a   Harada, Takayuki ^a   Harada, Chikako ^a   Romero, Mario ^a   Hebert, Jean M ^b   McConnell, Susan K ^b   Parada, Luis F ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTROPHIN; NEUROTROPHIN 3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN MATURATION; CONTROLLED STUDY; MOUSE; NEOCORTEX; NERVE FIBER; NERVE PROJECTION; NEUROTRANSMISSION; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE; THALAMOCORTICAL TRACT; THALAMUS; THALAMUS NUCLEUS; VERTEBRATE; VISUAL CORTEX; WHITE MATTER;

EID: 0037079079     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(02)01021-8     Document Type: Article

References (72)

1. Aldrich M.S., Alessi A.G., Beck R.W., Gilman S. Cortical blindness. etiology, diagnosis, and prognosis Ann. Neurol. 21:1987;149-158.
2. Allendoerfer K.L., Shatz C.J. The subplate, a transient neocortical structure. its role in the development of connections between thalamus and cortex Annu. Rev. Neurosci. 17:1994;185-218.
3. Allendoerfer K.L., Cabelli R.J., Escandon E., Kaplan D.R., Nikolics K., Shatz C.J. Regulation of neurotrophin receptors during the maturation of the mammalian visual system. J. Neurosci. 14:1994;1795-1811.
4. Angevine J.B. Jr. Time of neuron origin in the diencephalon of the mouse. An autoradiographic study. J. Comp. Neurol. 139:1970;129-187.
5. Antonini A., Fagiolini M., Stryker M.P. Anatomical correlates of functional plasticity in mouse visual cortex. J. Neurosci. 19:1999;4388-4406.
6. Auladell C., Perez-Sust P., Super H., Soriano E. The early development of thalamocortical and corticothalamic projections in the mouse. Anat. Embryol. (Berl.). 201:2000;169-179.
7. Bagri A., Marin O., Plump A.S., Mak J., Pleasure S.J., Rubenstein J.L., Tessier-Lavigne M. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron. 33:2002;233-248.
8. Baker-Nobles L., Rutherford A. Understanding cortical visual impairment in children. Am. J. Occup. Ther. 49:1995;899-903.
9. Bates B., Rios M., Trumpp A., Chen C., Fan G., Bishop J.M., Jaenisch R. Neurotrophin-3 is required for proper cerebellar development. Nat. Neurosci. 2:1999;115-117.
10. Bibel M., Barde Y.A. Neurotrophins. key regulators of cell fate and cell shape in the vertebrate nervous system Genes Dev. 14:2000;2919-2937.
11. Bicknese A.R., Sheppard A.M., O'Leary D.D., Pearlman A.L. Thalamocortical axons extend along a chondroitin sulfate proteoglycan- enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J. Neurosci. 14:1994;3500-3510.
12. Birch E.E., Bane M.C. Forced-choice preferential looking acuity of children with cortical visual impairment. Dev. Med. Child Neurol. 33:1991;722-729.
13. Braisted J.E., Tuttle R., O'Leary D.D. Thalamocortical axons are influenced by chemorepellent and chemoattractant activities localized to decision points along their path. Dev. Biol. 208:1999;430-440.
14. Braisted J.E., Catalano S.M., Stimac R., Kennedy T.E., Tessier-Lavigne M., Shatz C.J., O'Leary D.D. Netrin-1 promotes thalamic axon growth and is required for proper development of the thalamocortical projection. J. Neurosci. 20:2000;5792-5801.
15. Cabelli R.J., Hohn A., Shatz C.J. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science. 267:1995;1662-1666.
16. Cabelli R.J., Shelton D.L., Segal R.A., Shatz C.J. Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron. 19:1997;63-76.
17. Carpenter M.B. Core Text of Neuroanatomy. Third Edition:1985;Williams & Wilkins, Baltimore, MD.
18. Catalano S.M., Robertson R.T., Killackey H.P. Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. Proc. Natl. Acad. Sci. USA. 88:1991;2999-3003.
19. Chang G.Q., Hao Y., Wong F. Apoptosis. final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice Neuron. 11:1993;595-605.
20. Cohen-Cory S., Fraser S.E. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature. 378:1995;192-196.
21. DeFreitas M.F., McQuillen P.S., Shatz C.J. A novel p75NTR signaling pathway promotes survival, not death, of immunopurified neocortical subplate neurons. J. Neurosci. 21:2001;5121-5129.
22. Ernfors P., Lee K.F., Kucera J., Jaenisch R. Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell. 77:1994;503-512.
23. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates. 1997;The Academic Press, San Diego, CA.
24. Ghosh A., Shatz C.J. Involvement of subplate neurons in the formation of ocular dominance columns. Science. 255:1992;1441-1443.
25. Gordon J.A., Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 16:1996;3274-3286.
26. Grafstein B. Transneuronal transfer of radioactivity in the central nervous system. Science. 172:1971;177-179.
27. Hebert J.M., McConnell S.K. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 222:2000;296-306.
28. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 98:1999;739-755.
29. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
30. Katz L.C. What's critical for the critical period in visual cortex? Cell. 99:1999;673-676.
31. Kernie S.G., Liebl D.J., Parada L.F. BDNF regulates eating behavior and locomotor activity in mice. EMBO J. 19:2000;1290-1300.
32. Kokaia M., Asztely F., Olofsdotter K., Sindreu C.B., Kullmann D.M., Lindvall O. Endogenous neurotrophin-3 regulates short-term plasticity at lateral perforant path-granule cell synapses. J. Neurosci. 18:1998;8730-8739.
33. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA. 92:1995;8856-8860.
34. Kostovic I., Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 297:1990;441-470.
35. Lein E.S., Hohn A., Shatz C.J. Dynamic regulation of BDNF and NT-3 expression during visual system development. J. Comp. Neurol. 420:2000;1-18.
36. Liebl D.J., Tessarollo L., Palko M.E., Parada L.F. Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. J. Neurosci. 17:1997;9113-9121.
37. Lione L.A., Carter R.J., Hunt M.J., Bates G.P., Morton A.J., Dunnett S.B. Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation. J. Neurosci. 19:1999;10428-10437.
38. Lom B., Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J. Neurosci. 19:1999;9928-9938.
39. Lore R., Sawatski D. Performance of binocular and monocular infant rats on the visual cliff. J. Comp. Physiol. Psychol. 67:1969;177-181.
40. Ma L., Reis G., Parada L.F., Schuman E.M. Neuronal NT-3 is not required for synaptic transmission or long-term potentiation in area CA1 of the adult rat hippocampus. Learn. Mem. 6:1999;267-275.
41. Ma L., Merenmies J., Parada L.F. Molecular characterization of the TrkA/NGF receptor minimal enhancer reveals regulation by multiple cis elements to drive embryonic neuron expression. Development. 127:2000;3777-3788.
42. Maisonpierre P.C., Belluscio L., Friedman B., Alderson R.F., Wiegand S.J., Furth M.E., Lindsay R.M., Yancopoulos G.D. NT-3, BDNF, and NGF in the developing rat nervous system. parallel as well as reciprocal patterns of expression Neuron. 5:1990;501-509.
43. McAllister A.K., Lo D.C., Katz L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron. 15:1995;791-803.
44. McAllister A.K., Katz L.C., Lo D.C. Neurotrophin regulation of cortical dendritic growth requires activity. Neuron. 17:1996;1057-1064.
45. McAllister A.K., Katz L.C., Lo D.C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron. 18:1997;767-778.
46. McConnell S.K. Constructing the cerebral cortex. neurogenesis and fate determination Neuron. 15:1995;761-768.
47. McQuillen P.S., DeFreitas M.F., Zada G., Shatz C.J. A novel role for p75NTR in subplate growth cone complexity and visual thalamocortical innervation. J. Neurosci. 22:2002;3580-3593.
48. Metin C., Godement P. The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J. Neurosci. 16:1996;3219-3235.
49. Minichiello L., Klein R. TrkB and TrkC neurotrophin receptors cooperate in promoting survival of hippocampal and cerebellar granule neurons. Genes Dev. 10:1996;2849-2858.
50. Patapoutian A., Reichardt L.F. Trk receptors. mediators of neurotrophin action Curr. Opin. Neurobiol. 11:2001;272-280.
51. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron. 16:1996;1137-1145.
52. 3H]-proline containing material Brain Res. Bull. 12:1984;339-342.
53. Robertson R.T., Kaitz S.S. Thalamic connections with limbic cortex. I. Thalamocortical projections. J. Comp. Neurol. 195:1981;501-525.
54. Shatz C.J. How are specific connections formed between thalamus and cortex? Curr. Opin. Neurobiol. 2:1992;78-82.
55. Shibata H. Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J. Comp. Neurol. 330:1993;533-542.
56. Shibata H. Organization of projections of rat retrosplenial cortex to the anterior thalamic nuclei. Eur. J. Neurosci. 10:1998;3210-3219.
57. Shibata H. Organization of retrosplenial cortical projections to the laterodorsal thalamic nucleus in the rat. Neurosci. Res. 38:2000;303-311.
58. Snider W.D. Functions of the neurotrophins during nervous system development. what the knockouts are teaching us Cell. 77:1994;627-638.
59. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21:1999;70-71.
60. Sripanidkulchai K., Wyss J.M. Thalamic projections to retrosplenial cortex in the rat. J. Comp. Neurol. 254:1986;143-165.
61. Tessarollo L., Tsoulfas P., Martin-Zanca D., Gilbert D.J., Jenkins N.A., Copeland N.G., Parada L.F. trkC, a receptor for neurotrophin-3, is widely expressed in the developing nervous system and in non-neuronal tissues. Development. 118:1993;463-475.
62. Tessarollo L., Vogel K.S., Palko M.E., Reid S.W., Parada L.F. Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proc. Natl. Acad. Sci. USA. 91:1994;11844-11848.
63. Van Groen T., Wyss J.M. Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J. Comp. Neurol. 358:1995;584-604.
64. Vigers A.J., Baquet Z.C., Jones K.R. Expression of neurotrophin-3 in the mouse forebrain. insights from a targeted LacZ reporter J. Comp. Neurol. 416:2000;398-415.
65. Wilkinson G.A., Farinas I., Backus C., Yoshida C.K., Reichardt L.F. Neurotrophin-3 is a survival factor in vivo for early mouse trigeminal neurons. J. Neurosci. 16:1996;7661-7669.
66. Wong V.C. Cortical blindness in children. a study of etiology and prognosis Pediatr. Neurol. 7:1991;178-185.
67. Wong-Riley M.T. Cytochrome oxidase. an endogenous metabolic marker for neuronal activity Trends Neurosci. 12:1989;94-101.
68. Xu B., Zang K., Ruff N.L., Zhang Y.A., McConnell S.K., Stryker M.P., Reichardt L.F. Cortical degeneration in the absence of neurotrophin signaling. dendritic retraction and neuronal loss after removal of the receptor TrkB Neuron. 26:2000;233-245.
69. Yokoyama N., Romero M.I., Cowan C.A., Galvan P., Helmbacher F., Charnay P., Parada L.F., Henkemeyer M. Forward signaling mediated by ephrin-B3 prevents contralateral corticospinal axons from recrossing the spinal cord midline. Neuron. 29:2001;85-97.
70. Zhou X.F., Rush R.A. Localization of neurotrophin-3-like immunoreactivity in the rat central nervous system. Brain Res. 643:1994;162-172.
71. Zhu Y., Romero M.I., Ghosh P., Ye Z., Charnay P., Rushing E.J., Marth J.D., Parada L.F. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev. 15:2001;859-876.
72. Zhuo L., Theis M., Alvarez-Maya I., Brenner M., Willecke K., Messing A. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis. 31:2001;85-94.