Reproductive State Modulates Retinal Sensitivity to Light in Female Túngara Frogs.

Caitlin E Leslie,Michael J Ryan,Hamilton E Farris,Robert F Rosencrans,William C Gordon,Nicolas G Bazan,Whitney Walkowski

doi:10.3389/fnbeh.2019.00293

Abstract

Visual cues are often a vital part of animal communication and courtship. While a plethora of studies have focused on the role that hormones play in acoustic communication of anurans, relatively few have explored hormonal modulation of vision in these animals. Much of what we do know comes from behavioral studies, which show that a frog’s hormonal state can significantly affect both its visual behavior and mating decisions. However, to fully understand how frogs use visual cues to make these mating decisions, we must first understand how their visual system processes these cues, and how hormones affect these processes. To do this, we performed electroretinograms (ERGs) to measure retinal sensitivity of túngara frogs (Physalaemus pustulosus), a neotropical species whose mating behavior includes previously described visual cues. To determine the effect of hormonal state on visual sensitivity, ERGs were recorded under scotopic and photopic conditions in frogs that were either non-reproductive or hormone-treated with human chorionic gonadotropin (hCG) prior to testing. Additionally, measurements of optical anatomy determined how túngara frog eye and retina morphology related to physiological sensitivity. As expected, we found that both sexes display higher visual sensitivity under scotopic conditions compared to photopic conditions. However, hormone injections significantly increased retinal sensitivity of females under scotopic conditions. These results support the hypothesis that hormonal modulation of neural mechanisms, such as those mediating visually guided reproductive behavior in this species, include modulation of the receptor organ: the retina. Thus, our data serve as a starting point for elucidating the mechanism of hormonal modulation of visual sensitivity.

Highlights

Visual cues, especially in the context of reproductive behavior, are important in many animal communication systems, subjecting the visual system to strong selection
We are aware of only one recent study making such direct measurements, showing mouthbrooding African cichlid females have a higher expression of sex steroids in retinal tissue as well as heightened retinal sensitivity (Butler et al, 2019)
Our goal is to address this gap by making direct electrophysiological measures of retinal sensitivity in a model anuran system

Summary

Introduction

Especially in the context of reproductive behavior, are important in many animal communication systems (for review, see Candolin, 2003), subjecting the visual system to strong selection. In order to modulate behavior, these visual traits must first be encoded by the retina and subjected to further central processing in the brain. We are aware of only one recent study making such direct measurements, showing mouthbrooding African cichlid females have a higher expression of sex steroids in retinal tissue as well as heightened retinal sensitivity (Butler et al, 2019). That study notwithstanding, compelling evidence for this phenomenon in other systems is largely indirect or lacking measures of sensitivity change in the sensory organ itself. Histological approaches have revealed steroid hormone receptors in the retinas of humans (Ogueta et al, 1999), goldfish (Tchoudakova et al, 1999), western mosquitofish, sailfin mollies (Friesen et al, 2017), and three-spined sticklebacks (Hoffmann et al, 2012).

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