Calcium dynamics and regulation in horizontal cells of the vertebrate retina: lessons from teleosts

Horizontal cells (HCs) are inhibitory interneurons of the vertebrate retina. Unlike typical neurons, HCs are chronically depolarized in the dark, leading to a constant influx of Ca²⁺. Therefore, mechanisms of Ca²⁺ homeostasis in HCs must differ from neurons elsewhere in the central nervous system, which undergo excitotoxicity when they are chronically depolarized or stressed with Ca²⁺. Horizontal cells are especially well characterized in teleost fish, and have been used to unlock mysteries of the vertebrate retina for over a century. More recently, mammalian models of the retina have been increasingly informative for HC physiology. We draw from both teleost and mammalian models in this review, using a comparative approach to examine what is known about Ca²⁺ pathways in vertebrate HCs. We begin with a survey of Ca²⁺-permeable ion channels, exchangers, and pumps, and summarize Ca²⁺ influx and efflux pathways, buffering, and intracellular stores. This includes evidence for Ca²⁺-permeable α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPARs) and N-methyl-D-aspartate receptors (NMDARs), and for voltage-gated Ca²⁺ channels. Special attention is given to interactions between ion channels, to differences between species, and in which subtypes of HCs these channels have been found. We then discuss a number of unresolved issues pertaining to Ca²⁺ dynamics in HCs, including: a potential role for Ca²⁺ in feedback to photoreceptors, the role for Ca²⁺-induced Ca²⁺ release, and the properties and functions of Ca²⁺-based action potentials. This review aims to highlight the unique Ca²⁺ dynamics in HCs, as these are inextricably tied to retinal function.

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