Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: plasticity in the rod and degeneration in the cone system

Authors

  • Dana Specht,

    1. Department of Biology, Animal Physiology, University of Erlangen-Nuremberg, Staudtstrasse 5, 91058 Erlangen, Germany
    2. Max Planck Institute for Brain Research, Neuroanatomy, Frankfurt/Main, Germany
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    • *

      D.S., S.t.D. and J.A. contributed equally to this work.

  • Susanne Tom Dieck,

    1. Department of Biology, Animal Physiology, University of Erlangen-Nuremberg, Staudtstrasse 5, 91058 Erlangen, Germany
    2. Max Planck Institute for Brain Research, Neuroanatomy, Frankfurt/Main, Germany
    3. Leibniz Institute for Neurobiology, Magdeburg, Germany
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    • *

      D.S., S.t.D. and J.A. contributed equally to this work.

  • Josef Ammermüller,

    1. AG Neurobiology, University of Oldenburg, Oldenburg, Germany
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    • *

      D.S., S.t.D. and J.A. contributed equally to this work.

  • Hanna Regus-Leidig,

    1. Department of Biology, Animal Physiology, University of Erlangen-Nuremberg, Staudtstrasse 5, 91058 Erlangen, Germany
    2. Leibniz Institute for Neurobiology, Magdeburg, Germany
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  • Eckart Dieter Gundelfinger,

    1. Leibniz Institute for Neurobiology, Magdeburg, Germany
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  • Johann Helmut Brandstätter

    1. Department of Biology, Animal Physiology, University of Erlangen-Nuremberg, Staudtstrasse 5, 91058 Erlangen, Germany
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Dr Johann H. Brandstätter, as above.
E-mail: jbrandst@biologie.uni-erlangen.de

Abstract

Knowledge about the plastic and regenerative capacity of the retina is of key importance for therapeutic approaches to restore vision in patients who suffer from degenerative retinal diseases. In the retinae of mice, mutant for the presynaptic scaffolding protein Bassoon, signal transfer at photoreceptor ribbon synapses is disturbed due to impaired ribbon attachment to the active zone. In a long-term study we observed, with light and electron microscopic immunocytochemistry and electroretinographic recordings, two overlapping events in the Bassoon mutant retina, i.e. loss of photoreceptor synapses in the outer plexiform layer, and structural remodeling and formation of ectopic photoreceptor synapses in the outer nuclear layer, a region usually devoid of synapses. Formation of ectopic synaptic sites starts around the time when photoreceptor synaptogenesis is completed in wild-type mice and progresses throughout life. The result is a dense plexus of ectopic photoreceptor synapses with significantly altered but considerable synaptic transmission. Ectopic synapse formation is led by the sprouting of horizontal cells followed by the extension of rod bipolar cell neurites that fasciculate with and grow along the horizontal cell processes. Although only the rod photoreceptors and their postsynaptic partners show structural and functional remodeling, our study demonstrates the potential of the retina for long-lasting plastic changes.

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