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Calbindin-D28k expression in spinal electromotoneurons of the weakly electric fish Apteronotus leptorhynchus during adult development and regeneration

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Abstract

Additive neurogenesis, the net increase in neuronal numbers by addition of new nerve cells to existing tissue, forms the basis for indeterminate spinal cord growth in brown ghost knifefish (Apteronotus leptorhynchus). Among the cells generated through the activity of adult neural stem cells are electromotoneurons, whose axons constitute the electric organ of this weakly electric fish. Electromotoneuron development is organized along a caudo-rostral gradient, with the youngest and smallest of these cells located near the caudal end of the spinal cord. Electromotoneurons start expressing calbindin-D28k when their somata have reached diameters of approximately 10 μm, and they continue expression after they have grown to a final size of about 50 μm. Calbindin-D28k expression is significantly increased in young neurons generated in response to injury. Immunohistochemical staining against caspase-3 revealed that electromotoneurons in both intact and regenerating spinal cord are significantly less likely to undergo apoptosis than the average spinal cord cell. We hypothesize that expression of calbindin-D28k protects electromotoneurons from cell death; and that the evolutionary development of such a neuroprotective mechanism has been driven by the indispensability of electromotoneurons in the fish’s electric behavior, and by the high size-dependent costs associated with their production or removal upon cell death.

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Acknowledgements

We thank Ruxandra F. Sîrbulescu for her suggestions on BrdU labeling of electromotoneurons, and two anonymous reviewers for their helpful comments on the manuscript. Funding for this investigation was provided by Northeastern University and National Science Foundation Grant no. 1538505. All animal experiments were approved by the Institutional Animal Care and Use Committee of Northeastern University. All efforts were made to reduce the number of animals used and to minimize suffering.

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Authors and Affiliations

  1. Laboratory of Neurobiology, Department of Biology, Northeastern University, 134 Mugar Life Sciences, 360 Huntington Avenue, Boston, MA, 02115, USA

    Antonia G. Vitalo & Günther K. H. Zupanc

  2. Healthcare Systems Engineering Institute, Department of Mechanical and Industrial Engineering, Northeastern University, Boston, MA, 02115, USA

    Iulian Ilieş

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  1. Antonia G. Vitalo
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  2. Iulian Ilieş
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  3. Günther K. H. Zupanc
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Correspondence to Günther K. H. Zupanc.

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Vitalo, A.G., Ilieş, I. & Zupanc, G.K.H. Calbindin-D28k expression in spinal electromotoneurons of the weakly electric fish Apteronotus leptorhynchus during adult development and regeneration. J Comp Physiol A 205, 595–608 (2019). https://doi.org/10.1007/s00359-019-01343-3

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