Purpose
Vision in all mammals occurs through “duplex” retinae containing both rod and cone photoreceptors, the signals from which are processed through cone-and/or rod-specific retinal interneuron pathways. Recent investigations, however, have determined that several cetacean families possess mutations in their single cone opsin gene likely resulting in a condition unique among mammals known as rod monochromacy. Natural and artificial loss-of-function mutations in mammalian opsin genes are reported to cause massive photoreceptor loss and large-scale remodeling of the retina. Here we investigated the cellular organization of the bowhead whale (Balaena mysticetus) retina to determine how this unprecedented functional loss of an entire mammalian photoreceptor class affects light signaling pathways in the retina.
Methods
Sequencing was performed for cDNA derived from cone opsin mRNA in balaenid whales. Light microscopy, transmission electron microscopy and anti-opsin immunofluorescence were used to characterize retinal architecture and to determine the photoreceptor types in B. mysticetus. In addition, bipolar cell immunofluorescence was used to identify bipolar cell types in the retina.
Results
Genetic analyses indicate the severe truncation of the single cone opsin mRNA in the B. mysticetus retina, indicating loss of cone cell function, but maintenance of a non-photosensitive, opsin-expressing cone-like cell in the retina. Immunofluorescence, histological and ultrastructural analyses indicate the complete loss of LWS cone outer segments in the balaenid whale retina, suggesting the total loss of cone-based photoreception, but maintenance of cone soma and cone bipolar cells.
Conclusions
These findings show for the first time a rod-monochromatic mammalian retina, and suggest that despite the loss of cone-mediated photoreception, the associated cone signaling machinery may be functionally maintained for multi-channel rod-based signaling in balaenid whales.
Keywords: 693 retinal connections, networks, circuitry •
604 mutations •
648 photoreceptors