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Abstract Light intensity varies 1 million‐fold between night and day, driving the evolution of eye morphology and retinal physiology. Despite extensive research across taxa showing anatomical adaptations to light niches, surprisingly few empirical studies have quantified the relationship between such traits and the physiological sensitivity to light. In this study, we employ a comparative approach in frogs to determine the physiological sensitivity of eyes in two nocturnal (Rana pipiens,Hyla cinerea) and two diurnal species (Oophaga pumilio,Mantella viridis), examining whether differences in retinal thresholds can be explained by ocular and cellular anatomy. Scotopic electroretinogram (ERG) analysis of relative b‐wave amplitude reveals 10‐ to 100‐fold greater light sensitivity in nocturnal compared to diurnal frogs. Ocular and cellular optics (aperture, focal length, and rod outer segment dimensions) were assessed via the Land equation to quantify differences in optical sensitivity. Variance in retinal thresholds was overwhelmingly explained by Land equation solutions, which describe the optical sensitivity of single rods. Thus, at the b‐wave, stimulus‐response thresholds may be unaffected by photoreceptor convergence (which create larger, combined collecting areas). Follow‐up experiments were conducted using photopic ERGs, which reflect cone vision. Under these conditions, the relative difference in thresholds was reversed, such that diurnal species were more sensitive than nocturnal species. Thus, photopic data suggest that rod‐specific adaptations, not ocular anatomy (e.g., aperture and focal distance), drive scotopic thresholds differences. To the best of our knowledge, these data provide the first quantified relationship between optical and physiological sensitivity in vertebrates active in different light regimes.
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Neural Circuit Revision in Retinal Remodeling, A Pathoconnectomics Approach
Abstract The Aii glycinergic amacrine cell (Aii) plays a central role in bridging rod pathways with cone pathways, enabling an increased dynamic range of vision from scotopic to photopic ranges. The Aii integrates scotopic signals via chemical synapses from rod bipolar cells (RodBCs) onto the arboreal processes of Aii ACs, injecting signals into ON-cone bipolar cells (CBbs) via gap junctions with Aiis on the arboreal processes and the waist of the Aii ACs. The CBbs then carry this information to ON and OFF ganglion cell classes. In addition, the Aii is involved in the surround inhibition of OFF cone bipolar cells (CBas) through glycinergic chemical synapses from Aii ACs onto CBas. We have previously shown changes in RodBC connectivity as a consequence of rod photoreceptor degeneration in a pathoconnectome of early retinal degeneration: RPC1. Here, we evaluated the impact of rod photoreceptor degeneration on the connectivity of the Aii to determine the impacts of photoreceptor degeneration on the downstream network of the neural retina and its suitability for integrating therapeutic interventions as rod photoreceptors are lost. Previously, we reported that in early retinal degeneration, prior to photoreceptor cell loss, Rod BCs make pathological gap junctions with Aiis. Here, we further characterize this altered connectivity and additional shifts in both the excitatory drive and gap junctional coupling of Aiis in retinal degeneration, along with discussion of the broader impact of altered connectivity networks. New findings reported here demonstrate that Aiis make additional gap junctions with CBas increasing the number of BC classes that make pathological gap junctional connectivity with Aiis in degenerating retina. In this study, we also report that the Aii, a tertiary retinal neuron alters their synaptic contacts early in photoreceptor degeneration, indicating that rewiring occurs in more distant members of the retinal network earlier in degeneration than was previously predicted. This rewiring impacts retinal processing, presumably acuity, and ultimately its ability to support therapeutics designed to restore image-forming vision. Finally, these Aii alterations may be the cellular network level finding that explains one of the first clinical complaints from human patients with retinal degenerative disease, an inability to adapt back and forth from photopic to scotopic conditions.
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- PAR ID:
- 10521672
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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- https://doi.org/10.1101/2024.02.14.580149
