Expression of trkB and trkC mRNAs by adult midbrain dopamine neurons: A double-label in situ hybridization study

Journal of Comparative Neurology

Volumn 403, Issue 3, 1999, Pages 295-308

  Numan, Suzanne ^a,b   Seroogy, Kim B ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Coexistence; Neurotrophin receptors; Parkinson's disease; Tyrosine hydroxylase; Ventral mesencephalon

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NEUROTROPHIN 3; NEUROTROPHIN 4; NEUROTROPHIN RECEPTOR;

ANIMAL TISSUE; ARTICLE; DOPAMINERGIC NERVE CELL; FEMALE; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RNA PROBE;

ANIMALS; DOPAMINE; FEMALE; IN SITU HYBRIDIZATION; MALE; MESENCEPHALON; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; RECEPTOR, TRKC; RECEPTORS, NERVE GROWTH FACTOR; RNA, MESSENGER; SUBSTANTIA NIGRA; TRANSCRIPTION, GENETIC; TYROSINE 3-MONOOXYGENASE;

EID: 0033579839     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990118)403:3<295::AID-CNE2>3.0.CO;2-L     Document Type: Article

References (104)

1. Acheson A, Conover JC, Fandl JP, Dechiara TM, Russell M, Thadani A, Squinto SP, Yancopoulos GD, Lindsay RM. 1995 A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374:450-453.
2. Agid Y. 1991 Parkinsons disease: Pathophysiology. Lancet 337:1321-1327.
3. Albers KM, Perrone TN, Goodness TP, Jones ME, Green MA, Davis BM. 1996. Cutaneous overexpression of NT-3 increases sensory and sympathetic neuron number and enhances touch dome and hair follicle innervation. J Cell Biol 134:487-497.
4. Alexi T, Hefti F. 1996. Neurotrophin-4/5 selectively protects nigral calbindin-containing neurons in rats with medial forebrain bundle transections. Neuroscience 72:911-921.
5. Alexi T, Venero JL, Hefti F. 1997. Protective effects of neurotrophin-4/5 and transforming growth factor-alpha on striatal neuronal phenotypic degeneration after excitotoxic lesioning with quinolinic acid. Neuroscience 78:73-86.
6. Altar CA, Boylan CB, Jackson C, Hershenson S, Miller J, Wiegand SJ, Lindsay RM, Hyman C. 1992. Brain-derived neurotrophic factor augments rotational behavior and nigrostriatal dopamine turnover in vivo. Proc Natl Acad Sci USA 89:11347-11351.
7. Altar CA, Boylan CB, Fritsche M, Jackson C, Hyman C, Lindsay RM. 1994a. The neurotrophins NT-4/5 and BDNF augment serotonin, dopamine and GABAergic systems during behaviorally effective infusions to the substantia nigra. Exp Neurol 130:31-40.
8. 125I]NT-3. Eur J Neurosci 6:1389-1405.
9. Altar CA, Cai N, Bliven T, Juhasz M, Conner JM, Acheson AL, Lindsay RM, Wiegand SJ. 1997. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389:856-860.
10. Anderson KD, Alderson RF, Altar CA, DiStefano PS, Corcoran TL, Lindsay RM, Wiegand SJ. 1995. Differential distribution of exogenous BDNF, NGF, and NT-3 in the brain corresponds to the relative abundance and distribution of high-affinity and low-affinity neurotrophin receptors. J Comp Neurol 357:296-317.
11. Arborgast LA, Voogt JL. 1991. Hyperprolactinemia increases and hypoprolactinemia decreases tyrosine hydroxylase messenger ribonucleic acid levels in the arcuate nucleus, but not the substantia nigra. Endocrinology 128:997-1005.
12. Ardelt AA, Flaris N, Roth KA. 1994. Neurotrophin-4 selectively promotes survival of striatal neurons in organotypic slice culture. Brain Res 647:340-344.
13. Arenas E, Åkerud P, Wong V, Boylan C, Persson H, Lindsay RM, Altar CA. 1996. Effects of BDNF and NT-4/5 on striatonigral neuropeptides or nigral GABA neurons in vivo. Eur J Neurosci 8:1707-1717.
14. Barbacid M. 1994. The trk family of neurotrophin receptors. J Neurobiol 25:1386-1403.
15. Berg-von der Emde K, Dees WL, Hiney JK, Hill DF, Dissen GA, Costa ME, Moholt-Siebert M, Ojeda SR. 1995. Neurotrophins and the neuroendocrine brain: Different neurotrophins sustain anatomically and functionally segregated subsets of hypothalamic dopaminergic neurons. J Neurosci 15:4223-4237.
16. Berninger B, Marty S, Zafra F, Berzaghi MP, Thoenen H, Lindholm D. 1995. GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121:2327-2335.
17. Cabelli RJ, Allendoerfer KL, Radeke MJ, Welcher AA, Feinstein SC, Shatz CL. 1996. Changing patterns of expression and subcellular localization of TrkB in the developing visual system. J Neurosci 16:7965-7980.
18. Canossa M, Griesbeck O, Benedikt B, Campana G, Kolbeck R, Thoenen H. 1997. Neurotrophin release by neurotrophins: Implications for activity-dependent neuronal plasticity. Proc Natl Acad Sci USA 94:13279-13286.
19. Cellerino A, Maffei L, Domenici L. 1996. The distribution of brain-derived neurotrophic factor and its receptor trkB in parvalbumen-containing neurons of the rat visual cortex. Eur J Neurosci 8:1190-1197.
20. Collazo D, Takahashi H, McKay RD. 1992. Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9:643-656.
21. Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S. 1997 Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: Evidence for anterograde axonal transport. J Neurosci 17:2295-2313.
22. Cragg SJ, Greenfield SA. 1997. Differential autoreceptor control of somatodendritic and axon terminal dopamine release in substantia nigra, ventral tegmental area, and striatum. J Neurosci 17:5738-5746.
23. Croll SD, Wiegand SJ, Anderson KD, Lindsay RM, Nawa H. 1994. Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF. Eur J Neurosci 6:1343-1353.
24. Dahlström A, Fuxe K. 1964. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol Scand (Suppl.) 62:1-55.
25. Dixon JE, McKinnon D. 1994. Expression of the trk gene family of neurotrophin receptors in prevertebral sympathetic ganglia. Dev Brain Res 77:177-182.
26. Ebendal T. 1992. Function and evolution in the NGF family and its receptors. J Neurosci Res 32:461-470.
27. Ernfors P, Wetmore C, Olson L, Persson H. 1990. Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5:511-526.
28. Ernfors P, Van De Water T, Loring J, Jaenisch R. 1995. Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14:1153-1164.
29. Escalpez M, Tillakaratne NJK, Kaufman DL, Tobin AJ, Houser CR. 1994. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14:1834-1855.
30. Fallon JH, Loughlin SE. 1995. Substantia nigra. In G. Paxinos (ed): The Rat Nervous System. 2nd ed. San Diego: Academic Press, Inc., pp. 215-237.
31. Frim DM, Uhler TA, Galpern WR, Beal MK, Breakefield XO, Isacson O. 1994. Implanted fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevent 1-methyl-4-phenylpyridinium toxicity to dopaminergic neurons in the rat. Proc Natl Acad Sci USA 91:5104-5108.
32. Fryer RH, Kaplan DP, Feinstein SC, Radeke MJ, Grayson DR, Kromer LF. 1996. Developmental and mature expression of full-length and truncated TrkB receptors in the rat forebrain. J Comp Neurol 374:21-40.
33. Gall CM, Gold SJ, Isackson PJ, Seroogy KB. 1992. Brain-derived neurotrophic factor and neurotrophin-3 mRNAs are expressed in ventral midbrain regions containing dopaminergic neurons. Mol Cell Neurosci 3:56-63.
34. Gerfen CR, Baimbridge KG, Miller JJ. 1985. The neostriatal mosaic: Compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci USA 82:8780-8784.
35. German DC, Manaye KF. 1993. Midbrain dopaminergic neurons (nuclei A8, A9 and A10): three-dimensional reconstruction in the rat. J Comp Neurol 331:297-309.
36. Goodman LJ, Valverde J, Lim F, Geschwind MD, Federhoff HJ, Geller AI, Hefti F. 1996. Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons. Mol Cell Neurosci 7:222-238.
37. Grima B, Lamouroux A, Blanot K, Biguet NF, Mallet (1985). Complete coding sequence of rat tyrosine hydroxylase mRNA. Proc Natl Acad Sci USA 82:617-621.
38. Hagg T. 1998. Neurotrophins prevent death and differentially affect tyrosine hydroxylase of adult rat nigrostriatal neurons in vivo. Exp Neurol 149:183-192.
39. Haque NSK, Hlavin M-L, Fawcett JW, Dunnett SB. 1996. The neurotrophin NT4/5, but not NT3, enhances the efficacy of nigral grafts in a rat model of Parkinson's disease. Brain Res 712:45-52.
40. Hyman C, Hofer M, Barde Y-A, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM. 1991. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350:230-232.
41. Hyman C, Juhasz M, Jackson C, Wright P, Ip NY, Lindsay RM. 1994. Overlapping and distinct actions of the neurotrophins BDNF, NT-3 and NT-4/5 on cultured dopaminergic and GABAergic neurons of the ventral mesencephalon. J Neurosci 14:335-347.
42. Ip NY, Li Y, Yancopoulos GD, Lindsay RM. 1993a. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J Neurosci 13:3394-3405.
43. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD. 1993b. Similarities and differences in the way neurotrophins interact with trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
44. Jones KR, Fariñas I, Backus C, Reichardt LF. 1994. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999.
45. Kalivas PW. 1993. Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Rev 18:75-113.
46. Kim HG, Wang T, Olafsson P, Lu B. 1994. Neurotrophin-3 potentiates neuronal activity and inhibits γ-aminobutyratergic synaptic transmission in cortical neurons. Proc Natl Acad Sci USA 91:12341-12345.
47. - toxicity and oxidative stress in neonatal animals. Brain Res 713:178-185.
48. Klein R, Conway D, Parada LF, Barbacid M. 1990. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61:647-656.
49. Knüsel B, Winslow JW, Rosenthal A, Burton LE, Seid DP, Nikolics K, Hefti F. 1991. Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin 3. Proc Natl Acad Sci USA 88:961-965.
50. Korsching S. 1993. The neurotrophic factor concept: A reexamination. J. Neurosci 13:2739-2748.
51. Lamballe F, Klein R, Barbacid M. 1991. trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66:967-979.
52. Lärkfors L, Lindsay RM, Alderson RF. 1996. Characterization of the responses of Purkinje cells to neurotrophin treatment. J Neurochem 66:1362-1873.
53. Levivier M, Przedborski S, Bencsics C, Kang UJ. 1995. Intrastriatal implantation of fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevents degeneration of dopaminergic neurons in a rat model of Parkinson's disease. J Neurosci 15:7810-7820.
54. 28K and calretinin. Neuroscience 75:523-533.
55. Lindholm D, Carroll P, Tzimagiorgis G, Thoenen H. 1996. Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT-3 and NT-4. Eur J Neurosci 8:1452-1460.
56. Lindsay RM, Altar CA, Cedarbaum JM, Hyman C, Wiegand SJ. 1993. The therapeutic potential of neurotrophic factors in the treatment of Parkinson's disease. Exp Neurol 124:103-118.
57. Lindvall O, Björklund A. 1983. Dopamine-and norepinephrine-containing neuron systems: Their anatomy in the rat brain. In P.C. Emson (ed): Chemical Neuroanatomy. New York: Raven Press, pp. 229-255.
58. Maisonpierre PC, Belluscio L, Friedman B, Alderson RF, Wiegand SJ, Furth ME, Lindsay RM, Yancopoulos GD. 1990. NT-3, BDNF, and NGF in the developing rat nervous system: Parallel as well as reciprocal patterns of expression. Neuron 5:501-509.
59. Martin-Iverson MT, Altar CA. 1996. Spontaneous behaviors of rats are differentially affected by substantia nigra infusions of brain-derived neurotrophic factor and neurotrophin-3. Eur J Neurosci 8:1696-1706.
60. Martin-Iverson MT, Todd KG, Altar CA. 1994. Brain-derived neurotrophic factor and neurotrophin-3 activate striatal dopamine and serotonin metabolism and related behaviors: Interactions with amphetamine. J Neurosci 14:1262-1270.
61. Marty S, Berninger B, Carroll P, Thoenen H. 1996. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16:565-570.
62. Marty S, Berzaghi MP, Berninger B. 1997. Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci 20:198-202.
63. McAllister AK, Katz LC, Lo DC. 1997. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 18:767-778.
64. McRitchie DA, Hardman CD, Halliday GM. 1996. Cytoarchitectural distribution of calcium binding proteins in midbrain dopaminergic regions of rats and humans. J Comp Neurol 364:121-150.
65. Merlio J-P, Ernfors P, Jaber M, Persson H. 1992. Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience 51:515-532.
66. Middlemas DS, Lindberg RA, Hunter T. 1991. trkB, a neural receptor protein-tyrosine kinase: Evidence for a full-length and two truncated receptors. Mol Cell Biol 11:143-153.
67. Mizuno K, Carnahan J, Nawa H. 1994. Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons. Dev Biol 165:243-256.
68. Mount TJ, Dreyfus CF, Black IB. 1994. Neurotrophin-3 selectively increases cultured Purkinje cell survival. NeuroReport 5:2497-2500.
69. Mufson EJ, Kroin JS, Sobreviela T, Burke MA, Kordower JH, Penn RD, Miller JA. 1994. Intrastriatal infusions of brain-derived neurotrophic factor: Retrograde transport and colocalization with dopamine containing substantia nigra neurons in rat. Exp Neurol 129: 15-26.
70. Nawa H, Bessho Y, Carnahan J, Nakanishi S, Mizuno K. 1993. Regulation of neuropeptide expression in cultured cerebral cortical neurons by brain-derived neurotrophic factor. J Neurochem 60:772-775.
71. Nawa H, Pelleymounter MA, Carnahan J. 1994. Intraventricular administration of BDNF increases neuropeptide expression in newborn rat brain. J Neurosci 14:3751-3765.
72. Numan S, Seroogy KB. 1996. Expression of trkB and trkC mRNAs by dopaminergic neurons of the adult rat ventral midbrain. Soc Neurosci Abstr 22:1004.
73. Numan S, Seroogy KB. 1997. Increased expression of trkB mRNA in rat caudate-putamen following 6-OHDA lesions of the nigrostriatal pathway. Eur J Neurosci 9:101-107.
74. Pappas IS, Parnavelas JG. 1997. Neurotrophins and basic fibroblast growth factor induce the differentiation of calbindin-containing neurons in the cerebral cortex. Exp Neurol 144:302-314.
75. Phillips HS, Hains JM, Laramee GR, Rosenthal A, Winslow JW. 1990. Widespread expression of BDNF but not NT-3 by target areas of basal forebrain cholinerigic neurons. Science 250:290-294.
76. Robinson M, Buj-Bello A, Davies AM. 1996. Paracrine interactions of BDNF involving NGF-dependent embryonic sensory neurons. Mol Cell Neurosci 7:143-151.
77. Rogers JH. 1992. Immunohistochemical markers in the rat brain: Colocalization of calretinin and calbindin-D28k with tyrosine hydroxylase. Brain Res 587:203-210.
78. Sauer H, Campbell K, Wiegand SJ, Lindsay RM, Björklund A. 1994. Brain-derived neurotrophic factor enhances striatal neuropeptide expression in both the intact and the dopamine-depleted rat striatum. NeuroReport 5:609-612.
79. Sauer H, Wong V, Björklund A. 1995. Brain-derived neurotrophic factor and neurotrophin 4/5 modify neurotransmitter-related gene expression in the 6-hydroxydopamine-lesioned rat striatum. Neuroscience 65:927-933.
80. Schmidt-Kastner R, Wetmore C, Olson L. 1996. Comparative study of brain-derived neurotrophic factor messenger RNA and protein at the cellular levels suggests multiple roles in the hippocampus, striatum and cortex. Neuroscience 74:161-183.
81. / mice reveals a role for neurotrophins in CNS patterning. Neuron 19:269-281.
82. Seroogy KB, CM Gall. 1993. Expression of neurotrophins by midbrain dopaminergic neurons. Exp Neurol 124:119-128.
83. Seroogy KB, Herman JP. 1997. In situ hybridization approaches to the study of the nervous system. In A.J. Turner and H.S. Bachelard (eds): Neurochemistry: A Practical Approach, 2nd ed. Oxford: Oxford University Press, pp. 121-150.
84. Seroogy K, Ceccatelli S, Schalung M, Hökfelt T, Frey P, Walsh J, Dockray G, Brown J, Buchan A, Goldstein M. 1988. A subpopulation of dopaminergic neurons in rat ventral mesencephalon contains both neurotensin and cholecystokinin. Brain Res 455:88-98.
85. Seroogy KB, Dangaran K, Lim S, Haycock J, Fallon JH. 1989. Ventral mesencephalic neurons containing both cholecystokinin-and tyrosine hydroxylase-like immunoreactivities project to forebrain regions. J Comp Neurol 279:397-414.
86. Seroogy KB, Lundgren KH, Tran TMB, Guthrie KM, Isackson PJ, Gall CM. 1994. Dopaminergic neurons in rat ventral midbrain express brain-derived neurotrophic factor and neurotrophin-3 mRNAs. J Comp Neurol 342:321-334.
87. Shen R-Y, Altar CA, Chiodo LA. 1994. Brain-derived neurotrophic factor increases the electrical activity of pars compacta dopamine neurons in vivo. Proc Natl Acad Sci USA 91:8920-8924.
88. Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J, Burton LE, Stanton BR, Kaplan DR, Hunter T, Nikolics K, Parada LF. 1991 The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895-903.
89. Spenger C, Hyman C, Studer L, Egli M, Evtouchenko L, Jackson C, Dahl-Jørgensen A, Lindsay RM, Seiler RW. 1995. Effects of BDNF on dopaminergic, serotonergic, and GABAergic neurons in cultures of human fetal ventral mesencephalon. Exp Neurol 133:50-63.
90. Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Radziejewski C, Glass DJ, Masiakowski P, Furth ME, Valenzuela DM, DiStefano PS, Yancopoulos GD. 1991. trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65:885-893.
91. Sternini C, Su D, Arakawa J, Giorgio RD, Rickman DW, Davis BM, Albers KM, Brecha NC. 1996. Cellular localization of pan-trk immunoreactivity and trkC mRNA in the enteric nervous system. J Comp Neurol 368:597-607.
92. Studer L, Spenger C, Seiler RW, Altar CA, Lindsay RM, Hyman C. 1995. Comparison of the effects of the neurotrophins on the morphological structure of dopaminergic neurons in cultures of rat substantia nigra. Eur J Neurosci 7:223-233.
93. Tongiorgi E, Righi M, Cattaneo A. 1997. Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17:9492-9505.
94. Tsoulfas P, Stephens RM, Kaplan DR, Parada LF. 1996. TrkC isoforms with inserts in the kinase domain show impaired signaling responses. J Biol Chem 271:5691-5697.
95. Valenzuela DM, Maisonpierre PC, Glass DJ, Rojas E, Nuñez L, Kong Y, Gies DR, Stitt TN, Ip NY, Yancopoulos, GD. 1993. Alternative forms of rat trkC with different functional capabilities. Neuron 10:963-974.
96. Venero JL, Beck KD, Hefti F. 1994. 6-Hydroxydopamine lesions reduce BDNF mBNA levels in adult rat brain substantia nigra. NeuroReport 5:429-432.
97. Ventimiglia R, Mather P, Jones BE, Lindsay RM. 1995. The neurotrophins BDNF, NT-3 and NT-4/5 promote survival and morphological and biochemical differentiation of striatal neurons in vitro. Eur J Neurosci 7:213-222.
98. Vicario-Abejon C, Johe KK, Hazel TG, Collazo D, McKay RD. 1995. Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15:105-114.
99. Volpe BT, Wildmann J, Altar CA. 1998. Brain-derived neurotrophic factor prevents the loss of nigral neurons induced by excitotoxic striatal-pallidal lesions. Neuroscience 83:741-748.
100. Widmer HR, Hefti F. 1994a. Stimulation of GABAergic neuron differentiation by NT-4/5 in cultures of rat cerebral cortex. Dev Brain Res 80:279-284.
101. Widmer HR, Hefti F. 1994b. Neurotrophin-4/5 promotes survival and differentiation of rat striatal neurons developing in culture. Eur J Neurosci 6:1669-1679.
102. Yan Q, Radeke MJ, Matheson CR, Talvenheimo J, Welcher AA, Feinstein SC. 1997a. Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J Comp Neurol 378:135-157.
103. Yan Q, Rosenfeld RD, Matheson CR, Hawkins N., Lopez OT, Bennett L, Welcher AA. 1997b. Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 78:431-448.
104. Zhou J, Bradford H, Stern GM. 1994. The response of human and rat fetal ventral mesencephalon in culture to the brain-derived neurotrophic factor treatment. Brain Res 656:147-156.