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The Journal of Neuroscience, May 10, 2006, 26(19):5248-5255; doi:10.1523/JNEUROSCI.4483-05.2006

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Development/Plasticity/Repair
Synaptic Plasticity in CNGA3^–/– Mice: Cone Bipolar Cells React on the Missing Cone Input and Form Ectopic Synapses with Rods

Silke Haverkamp,¹ Stylianos Michalakis,² Ellen Claes,¹ Mathias W. Seeliger,³ Peter Humphries,⁴ Martin Biel,² and Andreas Feigenspan⁵

¹Department of Neuroanatomy, Max-Planck-Institute for Brain Research, D-60528 Frankfurt/Main, Germany, ²Department Pharmazie–Zentrum für Pharmaforschung, Ludwig Maximilians Universität, D-81377 Munich, Germany, ³Retinal Diagnostics Research Group, Department of Ophthalmology II, Eberhard-Karls University, D-72076 Tuebingen, Germany, ⁴Department of Genetics, Trinity College, Dublin 2, United Kingdom, and ⁵Department of Neurobiology, University of Oldenburg, D-26111 Oldenburg, Germany

Correspondence should be addressed to Silke Haverkamp, Max-Planck-Institute for Brain Research, Deutschordenstrasse 46, D-60528 Frankfurt/Main, Germany. Email: Haverkamp{at}mpih-frankfurt.mpg.de

In the mammalian retina, rods and cones connect to distinct sets of bipolar cells. Rods are presynaptic to a single type of rod bipolar cell, whereas cones connect to different types of cone bipolar cells. Synaptic rewiring between cone photoreceptor terminals and rod bipolar cell dendrites has been described as a general result of photoreceptor degeneration. To investigate whether cone bipolar cells also show synaptic plasticity in the absence of cone input, we studied the connectivity of cone bipolar cell dendrites in CNGA3^–/– mice, a model with specific loss of cone photoreceptor function. Dendritic connections of ON and OFF cone bipolar cells were visualized using specific cell markers or by intracellular injection with fluorescent dyes. The results show that cone bipolar cells in CNGA3^–/– mice form ectopic synapses with rods. In contrast, cone bipolar cells do not form ectopic synapses with rods in CNGA3^–/–Rho^–/– mice, in which both types of photoreceptors are nonfunctional. In analogy with these results, we found that input-deprived rod bipolar cells form ectopic synapses with functional cones in Rho^–/– mice but not with inoperable cones in the CNGA3^–/–Rho^–/– mouse. Our data indicate that the formation of ectopic bipolar cell synapses in the outer plexiform layer requires a functional presynaptic photoreceptor.

Key words: retina; cones; rods; bipolar cells; dendritic plasticity; ectopic synaptogenesis

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Received Oct. 19, 2005; revised March 31, 2006; accepted April 1, 2006.

Correspondence should be addressed to Silke Haverkamp, Max-Planck-Institute for Brain Research, Deutschordenstrasse 46, D-60528 Frankfurt/Main, Germany. Email: Haverkamp{at}mpih-frankfurt.mpg.de

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