Cone Bipolar Cells in the Retina of the MicrobatCarollia perspicillata

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Abstract

We studied the retinal cone bipolar cells of Carollia perspicillata, a microchiropteran bat of the phyllostomid family. Microchiroptera are strongly nocturnal, with small eyes and rod-dominated retinae. However, they also possess a significant cone population (2–4%) comprising two spectral types, which are hence the basis for daylight and color vision. We used antibodies against the calcium-binding protein recoverin and the carbohydrate epitope 15 (CD15) as reliable markers for certain cone bipolar cells. Dye injections of recoverin- or CD15-prelabeled cone bipolar cells in vertical slices revealed the morphology of the axon terminal system of individual bipolar cells. Seven distinct cone bipolar cell types were identified. They differed in the morphology and stratification level of their axon terminal system in the inner plexiform layer and in immunoreactivity for recoverin and/or CD15. Additional immunocytochemical markers were used to assess the functional ON/OFF subdivision of the inner plexiform layer. In line with the extended thickness of the ON sublayer of the inner plexiform layer in the microbat retina, more ON than OFF cone bipolar cell types were found, namely, four versus three. Most likely, in the bats' predominantly dark environment, ON signals have greater importance for contrast perception. We conclude that the microbat retina conforms to the general mammalian blueprint, in which light signals of intensities above rod sensitivity are detected by cones and transmitted to various types of ON and OFF cone bipolar cells. J. Comp. Neurol. 523:963–981, 2015. © 2014 Wiley Periodicals, Inc.

Using intracellular DiI injections and immunolabeling, seven cone bipolar cell types are identified in the retina of a microchiropteran bat. In contrast to the traditional view, the strongly nocturnal microbats have recently been shown to possess some retinal prerequisites for cone-based vision in addition to rod-based vision. The presence of several cone bipolar cell types strengthens the conclusion that the microbat retina largely conforms to the general mammalian pattern of complex cone pathways. The figure shows dye-injected cone bipolar cell type 1 (CB1) and summary diagram of bipolar cell types in the retina of the microbat Carollia perspicillata. Seven cone bipolar cell types and one rod bipolar cell type (RB) could be distinguished by immunohistochemical prelabeling and intracellular injection of DiI.

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