Renewal of electrotonic synapses in teleost retinal horizontal cells

Abstract

In teleost retinas, the somata of same-type cone horizontal cells are electrically coupled via extensive gap junctions, as are the axon terminals of same-type cells. This coupling persists throughout the animal's life and is modulated by dopamine and conditions of light- vs. dark-adaptation. Gap junction particle density in goldfish horizontal cell somata has also been shown to change under these conditions, indicating that these junctions are dynamic. We have used electron microscopy to examine gap junctions in bass horizontal cells with a fixation method that facilitates detection of gap junctions. Annular gap junction profiles were observed in the somatic cytoplasm of all cone horizontal cell types in both light- and dark-adapted animals. Serial sections showed that most profiles represented gap junction vesicles free within the cytoplasm; the remainder represented vesicles still attached to extensive plasma membrane gap junctions by a thin cytoplasmic neck, suggestive of an intermediate stage in endocytosis. Observations of gap junction vesicles containing fragments of gap junctional membrane and/or fused with lysosomal bodies further supported this hypothesis. Because gap junctions persist between the horizontal cells, we propose that gap junction endocytosis and lysosomal degradation are balanced by addition of new junctions. While endocytosis has been widely demonstrated to serve in programmed removal of gap junctions (without subsequent replacement), from both nonneuronal cells and developing neurons, this study indicates that it can also function in the renewal of electrical synapses in the adult teleost retina, where gap junction elimination is not the goal.