Retinal horizontal cells of goldfish (Carassius auratus) display subtype-specific differences in spontaneous action potentials in situ.

Horizontal cells (HCs) are neurons of the outer retina, which provide inhibitory feedback onto photoreceptors and contribute to image processing. HCs in teleosts are classified into four subtypes (H1-H4), each having different roles: H1-H3 feed back onto different sets of cones, H4 feed back onto rods, and only H1 store and release the inhibitory neurotransmitter, γ-aminobutyric acid (GABA). Dissociated HCs exhibit spontaneous Ca2+ -based action potentials (APs), yet it is unclear if APs occur in situ, or if all subtypes exhibit APs. We measured intracellular Ca2+ and report APs in slice preparations of the goldfish retina. In HCs furthest from photoreceptors (i.e., H3/H4), APs were less frequent, with greater duration and area under the curve (a measure of Ca2+ flux). Next, we classified acutely dissociated HCs into subtypes by integrating the ratio of dendritic field size vs. soma size (rd/s ). H1 and H2 subtypes had low rd/s values (<8); H3/H4 had high rd/s (>12). To verify this model, H1s were identified by immunoreactivity for GABA and 95% of these cells had an rd/s < 4. In Ca2+ imaging experiments, as rd/s increased, AP duration and area under the curve increased, while frequency decreased. Our results demonstrate the presence of Ca2+ -based APs in the goldfish retina in situ and show that HC subtypes H1 through H4 exhibit progressively longer and less frequent spontaneous APs. These results suggest that APs may play an important role in inhibitory feedback, and may have implications for understanding the relative contributions of HC subtypes in the outer retina.