Synaptic Organization of the Vertebrate Retina: General Principles and Species-Specific Variations

Abstract

One of the most striking features of the vertebrates is that their retinal structures are remarkably similar, as recognized by Ramon y Cajal over 100 years ago.1 All vertebrates have two types of photoreceptors, rods and cones, with a ubiquitous molecular cascade underlying phototransduction in the outer segments of both cell types.2,3 Five major types of second-/third-order retinal neurons are found in all vertebrate species: bipolar cells (BCs, including the hyperpolarizing and depolarizing BCs, HBCs, and DBCs), horizontal cells (HCs), amacrine cells (ACs), interplexiform cells (IPCs), and ganglion cells (GCs).4 The neuronal somas are located in three nuclear layers, and their axonal and dendritic processes form complex and orderly networks of chemical and electrical synapses in two (outer and inner) plexiform layers (OPL and IPL).1 During the past few decades, detailed studies on synaptic connectivity and functional pathways in the retina have been performed in many species, including fish, amphibians, reptiles, mammals, and humans. Results from these studies indicate that retinal synapses are organized in an intricate and orderly fashion, to efficiently process visual signals,4,5 and that synaptic pathways in the retina are arranged according to several general, cross-species principles.6,7 These principles dictate how retinal neurons are connected, synapses are formed, and various synaptic pathways are used to process different attributes of visual stimuli. Since not every type of retinal cell in every vertebrate is equally accessible for experimentation, identifying cross-species, general synaptic principles is important, not only to unravel how the first stages of the visual system operate, but also to facilitate our understanding of retinal function and dysfunction in less accessible animals, especially in humans. In this article, I shall discuss several general principles of synaptic organization in the vertebrate retina and their roles in visual information processing. Moreover, I will briefly mention several species-specific variations in retinal synaptic organization, but because of the space limitation, I will focus on the mammalian-specific AII amacrine cell (AIIAC) pathway.