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Normal eye-specific patterning of retinal inputs to murine subcortical visual nuclei in the absence of brain-derived neurotrophic factor

Published online by Cambridge University Press:  05 April 2005

ALVIN W. LYCKMAN ,
GUOPING FAN ,
MARIBEL RIOS ,
RUDOLF JAENISCH  and
MRIGANKA SUR
ALVIN W. LYCKMAN
Affiliation:
The Picower Center for Learning and Memory and the Department of Brain and Cognitive Sciences, MIT, Cambridge
GUOPING FAN
Affiliation:
The Whitehead Institute for Biomedical Research, Cambridge Current address: UCLA School of Medicine, Department of Human Genetics, Los Angeles, CA 90095
MARIBEL RIOS
Affiliation:
The Whitehead Institute for Biomedical Research, Cambridge Current address: Tufts University School of Medicine, Department of Neuroscience, Boston, MA 02135
RUDOLF JAENISCH
Affiliation:
The Whitehead Institute for Biomedical Research, Cambridge
MRIGANKA SUR
Affiliation:
The Picower Center for Learning and Memory and the Department of Brain and Cognitive Sciences, MIT, Cambridge
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Abstract

Brain-derived neurotrophic factor (BDNF) is a preferred ligand for a member of the tropomyosin-related receptor family, trkB. Activation of trkB is implicated in various activity-independent as well as activity-dependent growth processes in many developing and mature neural systems. In the subcortical visual system, where electrical activity has been implicated in normal development, both differential survival, as well as remodeling of axonal arbors, have been suggested to contribute to eye-specific segregation of retinal ganglion cell inputs. Here, we tested whether BDNF is required for eye-specific segregation of visual inputs to the lateral geniculate nucleus and the superior colliculus, and two other major subcortical target fields in mice. We report that eye-specific patterning is normal in two mutants that lack BDNF expression during the segregation period: a germ-line knockout for BDNF, and a conditional mutant in which BDNF expression is absent or greatly reduced in the central nervous system. We conclude that the availability of BDNF is not necessary for eye-specific segregation in subcortical visual nuclei.

Keywords

Optic tractNeurotrophic factorSynaptic specificityPlasticityCompetition
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 1 , January 2005 , pp. 27 - 36
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Allendoerfer, K.L., Cabelli, R.J., Escandon, E., Kaplan, D.R., Nikolics, K., & Shatz, C.J. (1994). Regulation of neurotrophin receptors during the maturation of the mammalian visual system. Journal of Neuroscience 14 (3 Pt. 2), 1795–1811.Google Scholar
Atkinson, J., Panni, M.K., & Lund, R.D. (1999). Effects of neurotrophins on embryonic retinal outgrowth. Brain Research Developmental Brain Research 112 (2), 173–180.CrossRefGoogle Scholar
Bartoletti, A., Cancedda, L., Reid, S.W., Tessarollo, L., Porciatti, V., Pizzorusso, T., & Maffei, L. (2002). Heterozygous knock-out mice for brain-derived neurotrophic factor show a pathway-specific impairment of long-term potentiation but normal critical period for monocular deprivation. Journal of Neuroscience 22 (23), 10072–10077.Google Scholar
Bates, B., Rios, M., Trumpp, A., Chen, C., Fan, G., Bishop, J.M., & Jaenisch, R. (1999). Neurotrophin-3 is required for proper cerebellar development. Nature Neuroscience 2 (2), 115–117.CrossRefGoogle Scholar
Berardi, N. & Maffei, L. (1999). From visual experience to visual function: Roles of neurotrophins. Journal of Neurobiology 41 (1), 119–126.3.0.CO;2-N>CrossRefGoogle Scholar
Bonhoeffer, T. (1996). Neurotrophins and activity-dependent development of the neocortex. Current Opinion in Neurobiology 6 (1), 119–126.CrossRefGoogle Scholar
Bosco, A. & Linden, R. (1999). BDNF and NT-4 differentially modulate neurite outgrowth in developing retinal ganglion cells. Journal of Neuroscience Research 57 (6), 759–769.3.0.CO;2-Y>CrossRefGoogle Scholar
Cabelli, R.J., Hohn, A., & Shatz, C.J. (1995). Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267 (5204), 1662–1666.Google Scholar
Cabelli, R.J., Allendoerfer, K.L., Radeke, M.J., Welcher, A.A., Feinstein, S.C., & Shatz, C.J. (1996). Changing patterns of expression and subcellular localization of TrkB in the developing visual system. Journal of Neuroscience 16 (24), 7965–7980.Google Scholar
Cabelli, R.J., Shelton, D.L., Segal, R.A., & Shatz, C.J. (1997). Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19 (1), 63–76.Google Scholar
Caleo, M. & Maffei, L. (2002). Neurotrophins and plasticity in the visual cortex. Neuroscientist 8 (1), 52–61.CrossRefGoogle Scholar
Chalupa, L.M., Snider, C.J., & Kirby, M.A. (1996). Topographic organization in the retinocollicular pathway of the fetal cat demonstrated by retrograde labeling of ganglion cells. Journal of Comparative Neurology 368 (2), 295–303.3.0.CO;2-Z>CrossRefGoogle Scholar
Chapman, B. (2000). Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science 287 (5462), 2479–2482.Google Scholar
Colonnese, M.T. & Constantine-Paton, M. (2001). Chronic NMDA receptor blockade from birth increases the sprouting capacity of ipsilateral retinocollicular axons without disrupting their early segregation. Journal of Neuroscience 21 (5), 1557–1568.Google Scholar
Cook, P.M., Prusky, G., & Ramoa, A.S. (1999). The role of spontaneous retinal activity before eye opening in the maturation of form and function in the retinogeniculate pathway of the ferret. Visual Neuroscience 16 (3), 491–501.Google Scholar
Cork, R.J., Namkung, Y., Shin, H.S., & Mize, R.R. (2001). Development of the visual pathway is disrupted in mice with a targeted disruption of the calcium channel beta(3)-subunit gene. Journal of Comparative Neurology 440 (2), 177–191.CrossRefGoogle Scholar
Drager, U.C. (1985). Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse. Proceedings of the Royal Society B (London) 224 (1234), 57–77.CrossRefGoogle Scholar
Edwards, M.A., Schneider, G.E., & Caviness, V.S., Jr. (1986). Development of the crossed retinocollicular projection in the mouse. Journal of Comparative Neurology 248 (3), 410–421.CrossRefGoogle Scholar
Elliott, T. & Shadbolt, N.R. (1999). A neurotrophic model of the development of the retinogeniculocortical pathway induced by spontaneous retinal waves. Journal of Neuroscience 19 (18), 7951–7970.Google Scholar
Ellsworth, C.A., Lyckman, A.W., Feldheim, D.A., Flanagan, J.A., & Sur, M. (2005). Ephrin-A2 and -A5 influence patterning of normal retinal projections to the visual thalamus and novel projections to the auditory thalamus: Conserved mapping mechanisms in diverse targets. Journal of Comparative Neurology (in press).CrossRefGoogle Scholar
Ernfors, P. & Bramham, C.R. (2003). The coupling of a trkB tyrosine residue to LTP. Trends in Neuroscience 26 (4), 171–173.CrossRefGoogle Scholar
Ernfors, P., Lee, K.F., & Jaenisch, R. (1994). Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368 (6467), 147–150.Google Scholar
Erskine, L., Williams, S.E., Brose, K., Kidd, T., Rachel, R.A., Goodman, C.S., Tessier-Lavigne, M., & Mason, C.A. (2000). Retinal ganglion cell axon guidance in the mouse optic chiasm: Expression and function of robos and slits. Journal of Neuroscience 20 (13), 4975–4982.Google Scholar
Fan, G., Beard, C., Chen, R.Z., Csankovszki, G., Sun, Y., Siniaia, M., Biniszkiewicz, D., Bates, B., Lee, P.P., Kuhn, R., Trumpp, A., Poon, C., Wilson, C.B., & Jaenisch, R. (2001). DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. Journal of Neuroscience 21 (3), 788–797.Google Scholar
Fan, G., Egles, C., Sun, Y., Minichiello, L., Renger, J.J., Klein, R., Liu, G., & Jaenisch, R. (2000). Knocking the NT4 gene into the BDNF locus rescues BDNF deficient mice and reveals distinct NT4 and BDNF activities. Nature Neuroscience 3 (4), 350–357.Google Scholar
Feldheim, D.A., Vanderhaeghen, P., Hansen, M.J., Frisen, J., Lu, Q., Barbacid, M., & Flanagan, J.G. (1998). Topographic guidance labels in a sensory projection to the forebrain. Neuron 21 (6), 1303–1313.Google Scholar
Frost, D.O., Ma, Y.T., Hsieh, T., Forbes, M.E., & Johnson, J.E. (2001). Developmental changes in BDNF protein levels in the hamster retina and superior colliculus. Journal of Neurobiology 49 (3), 173–187.CrossRefGoogle Scholar
Galuske, R.A., Kim, D.S., Castren, E., Thoenen, H., & Singer, W. (1996). Brain-derived neurotrophic factor reversed experience-dependent synaptic modifications in kitten visual cortex. European Journal of Neuroscience 8 (7), 1554–1559.CrossRefGoogle Scholar
Godement, P., Saillour, P., & Imbert, M. (1980). The ipsilateral optic pathway to the dorsal lateral geniculate nucleus and superior colliculus in mice with prenatal or postnatal loss of one eye. Journal of Comparative Neurology 190 (4), 611–626.CrossRefGoogle Scholar
Godement, P., Salaun, J., & Imbert, M. (1984). Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. Journal of Comparative Neurology 230 (4), 552–575.CrossRefGoogle Scholar
Hanover, J.L., Huang, Z.J., Tonegawa, S., & Stryker, M.P. (1999). Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. Journal of Neuroscience 19 (22), RC40.Google Scholar
Hata, Y., Ohshima, 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. Journal of Neuroscience 20 (3), RC57.Google Scholar
Herrera, E., Brown, L., Aruga, J., Rachel, R.A., Dolen, G., Mikoshiba, K., Brown, S., & Mason, C.A. (2003). Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114 (5), 545–557.Google Scholar
Huang, Z.J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M.F., Maffei, L., & Tonegawa, S. (1999). BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98 (6), 739–755.Google Scholar
Huberman, A.D., Stellwagen, D., & Chapman, B. (2002). Decoupling eye-specific segregation from lamination in the lateral geniculate nucleus. Journal of Neuroscience 22 (21), 9419–9429.Google Scholar
Huberman, A.D., Wang, G.Y., Liets, L.C., Collins, O.A., Chapman, B., & Chalupa, L.M. (2003). Eye-specific retinogeniculate segregation independent of normal neuronal activity. Science 300, 994–998.CrossRefGoogle Scholar
Isenmann, S., Cellerino, A., Gravel, C., & Bahr, M. (1999). Excess target-derived brain-derived neurotrophic factor preserves the transient uncrossed retinal projection to the superior colliculus. Molecular and Cellular Neuroscience 14 (1), 52–65.CrossRefGoogle Scholar
Jhaveri, S., Erzurumlu, R.S., & Schneider, G.E. (1996). The optic tract in embryonic hamsters: fasciculation, defasciculation, and other rearrangements of retinal axons. Visual Neuroscience 13 (2), 359–374.CrossRefGoogle Scholar
Jiang, B., Akaneya, Y., Hata, Y., & Tsumoto, T. (2003). Long-term depression is not induced by low-frequency stimulation in rat visual cortex in vivo: A possible preventing role of endogenous brain-derived neurotrophic factor. Journal of Neuroscience 23 (9), 3761–3770.Google Scholar
Kernie, S.G., Liebl, D.J., & Parada, L.F. (2000). BDNF regulates eating behavior and locomotor activity in mice. EMBO Journal 19 (6), 1290–1300.Google Scholar
Klintsova, A.Y. & Greenough, W.T. (1999). Synaptic plasticity in cortical systems. Current Opinion in Neurobiology 9 (2), 203–208.CrossRefGoogle Scholar
Lein, E.S. & Shatz, C.J. (2000). Rapid regulation of brain-derived neurotrophic factor mRNA within eye-specific circuits during ocular dominance column formation. Journal of Neuroscience 20 (4), 1470–1483.Google Scholar
Lein, E.S., Hohn, A., & Shatz, C.J. (2000). Dynamic regulation of BDNF and NT-3 expression during visual system development. Journal of Comparative Neurology 420 (1), 1–18.Google Scholar
Lom, B. & Cohen-Cory, S. (1999). Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. Journal of Neuroscience 19 (22), 9928–9938.Google Scholar
Lu, B. (2003). BDNF and activity-dependent synaptic modulation. Learning and Memory 10 (2), 86–98.CrossRefGoogle Scholar
Lyckman, A.W., Jhaveri, S., Feldheim, D.A., Vanderhaeghen, P., Flanagan, J.G., & Sur, M. (2001). Enhanced plasticity of retinothalamic projections in an ephrin-A2/A5 double mutant. Journal of Neuroscience 21 (19), 7684–7690.Google Scholar
Maffei, L. (2002). Plasticity in the visual system: role of neurotrophins and electrical activity. Archives Italiennes de Biologie 140 (4), 341–346.Google Scholar
Messaoudi, E., Ying, S.W., Kanhema, T., Croll, S.D., & Bramham, C.R. (2002). Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. Journal of Neuroscience 22 (17), 7453–7461.Google Scholar
Meyer, R.L. (1982). Tetrodotoxin blocks the formation of ocular dominance columns in goldfish. Science 218 (4572), 589–591.Google Scholar
Minichiello, L., Calella, A.M., Medina, D.L., Bonhoeffer, T., Klein, R., & Korte, M. (2002). Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36 (1), 121–137.Google Scholar
Pak, W., Hindges, R., Pfaff, S.L., & O'Leary, D.D.M. (2002). Role for islet-2 in specifying subclasses of retinal ganglion cells and their midline axon pathfinding decisions. Society for Neuroscience Abstracts 28, 626–627.Google Scholar
Penn, A.A., Riquelme, P.A., Feller, M.B., & Shatz, C.J. (1998). Competition in retinogeniculate patterning driven by spontaneous activity. Science 279 (5359), 2108–2112.Google Scholar
Ravary, A., Muzerelle, A., Herve, D., Pascoli, V., Ba-Charvet, K.N., Girault, J.A., Welker, E., & Gaspar, P. (2003). Adenylate cyclase 1 as a key actor in the refinement of retinal projection maps. Journal of Neuroscience 23 (6), 2228–2238.Google Scholar
Reh, T.A. & Constantine-Paton, M. (1985). Eye-specific segregation requires neural activity in three-eyed Rana pipiens. Journal of Neuroscience 5 (5), 1132–1143.Google Scholar
Riddle, D.R., Lo, D.C., & Katz, L.C. (1995). NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature 378 (6553), 189–191.Google Scholar
Rios, M., Fan, G., Fekete, C., Kelly, J., Bates, B., Kuehn, R., Lechan, R.M., & Jaenisch, R. (2001). Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Molecular Endocrinology 15 (10), 1748–1757.CrossRefGoogle Scholar
Schmidt, J.T. & Tieman, S.B. (1985). Eye-specific segregation of optic afferents in mammals, fish, and frogs: The role of activity. Cellular and Molecular Neurobiology 5 (1–2), 5–34.CrossRefGoogle Scholar
Sengpiel, F. & Kind, P.C. (2002). The role of activity in development of the visual system. Current Biology 12 (23), R818–826.CrossRefGoogle Scholar
Shatz, C.J. & Stryker, M.P. (1988). Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242 (4875), 87–89.Google Scholar
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62 (2), 738–855.Google Scholar
Silver, M.A. & Stryker, M.P. (2001). TrkB-like immunoreactivity is present on geniculocortical afferents in layer IV of kitten primary visual cortex. Journal of Comparative Neurology 436 (4), 391–398.CrossRefGoogle Scholar
Smetters, D.K., Hahm, J., & Sur, M. (1994). An N-methyl-D-aspartate receptor antagonist does not prevent eye-specific segregation in the ferret retinogeniculate pathway. Brain Research 658 (1–2), 168–178.CrossRefGoogle Scholar
Sretavan, D.W. (1990). Specific routing of retinal ganglion cell axons at the mammalian optic chiasm during embryonic development. Journal of Neuroscience 10 (6), 1995–2007.Google Scholar
Sretavan, D.W. & Kruger, K. (1998). Randomized retinal ganglion cell axon routing at the optic chiasm of GAP-43-deficient mice: Association with midline recrossing and lack of normal ipsilateral axon turning. Journal of Neuroscience 18 (24), 10502–10513.Google Scholar
Thoenen, H. (2000). Neurotrophins and activity-dependent plasticity. Progress in Brain Research 128, 183–191.CrossRefGoogle Scholar
Thompson, I. & Holt, C. (1989). Effects of intraocular tetrodotoxin on the development of the retinocollicular pathway in the Syrian hamster. Journal of Comparative Neurology 282 (3), 371–388.CrossRefGoogle Scholar
Tropea, D., Caleo, M., & Maffei, L. (2003). Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. Journal of Neuroscience 23 (18), 7034–7044.Google Scholar
Tyler, W.J., Perrett, S.P., & Pozzo-Miller, L.D. (2002). The role of neurotrophins in neurotransmitter release. Neuroscientist 8 (6), 524–531.CrossRefGoogle Scholar
Upton, A.L., Ravary, A., Salichon, N., Moessner, R., Lesch, K.P., Hen, R., Seif, I., & Gaspar, P. (2002). Lack of 5-HT(1B) receptor and of serotonin transporter have different effects on the segregation of retinal axons in the lateral geniculate nucleus compared to the superior colliculus. Neuroscience 111 (3), 597–610.CrossRefGoogle Scholar
Upton, A.L., Salichon, N., Lebrand, C., Ravary, A., Blakely, R., Seif, I., & Gaspar, P. (1999). Excess of serotonin (5-HT) alters the segregation of ipsilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: Possible role of 5-HT uptake in retinal ganglion cells during development. Journal of Neuroscience 19 (16), 7007–7024.Google Scholar
Vecino, E., Garcia-Grespo, D., Garcia, M., Martinez-Millan, L., Sharma, S.C., & Carrascal, E. (2002). Rat retinal ganglion cells co-express brain derived neurotrophic factor (BDNF) and its receptor TrkB. Vision Research 42 (2), 151–157.CrossRefGoogle Scholar
Vercelli, A., Garbossa, D., Biasiol, S., Repici, M., & Jhaveri, S. (2000). NOS inhibition during postnatal development leads to increased ipsilateral retinocollicular and retinogeniculate projections in rats. European Journal of Neuroscience 12 (2), 473–490.CrossRefGoogle Scholar
von Bartheld, C.S. (1998). Neurotrophins in the developing and regenerating visual system. Histology and Histopathology 13 (2), 437–459.Google Scholar
Wahle, P., Di Cristo, G., Schwerdtfeger, G., Engelhardt, M., Berardi, N., & Maffei, L. (2003). Differential effects of cortical neurotrophic factors on development of lateral geniculate nucleus and superior colliculus neurons: Anterograde and retrograde actions. Development 130 (3), 611–622.Google Scholar
Williams, S.E., Mann, F., Erskine, L., Sakurai, T., Wei, S., Rossi, D.J., Gale, N.W., Holt, C.E., Mason, C.A., & Henkemeyer, M. (2003). Ephrin-B2 and EphB1 mediate retinal axon divergence at the optic chiasm. Neuron 39 (6), 919–935.Google Scholar
Wu, H.H., Cork, R.J., Huang, P.L., Shuman, D.L., & Mize, R.R. (2000). Refinement of the ipsilateral retinocollicular projection is disrupted in double endothelial and neuronal nitric oxide synthase gene knockout mice. Brain Research Developmental Brain Research 120 (1), 105–111.CrossRefGoogle Scholar
Zakharenko, S.S., Patterson, S.L., Dragatsis, I., Zeitlin, S.O., Siegelbaum, S.A., Kandel, E.R., & Morozov, A. (2003). Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1–CA3 synapses. Neuron 39(6), 975–990.CrossRefGoogle Scholar
Zhang, X. & Poo, M.M. (2002). Localized synaptic potentiation by BDNF requires local protein synthesis in the developing axon. Neuron 36 (4), 675–688.Google Scholar