Interneurons of the inner retina

Detailed studies of the neuronal interactions that occur at the terminal pedicle of cone photoreceptors have created a cohesive framework for understanding the complexity of visual processing in the outer retina and, in particular, the neuronal mechanisms that give rise to the parallel visual pathways mediated by the different types of bipolar cells (see Chapter 17, How Retinal Circuits Optimize the Transfer of Visual Information). By contrast, our understanding of how the visual signals are further processed in the inner retina has advanced comparatively little in the past decade, notwithstanding the detailed documentation of the neuronal diversity of both the amacrine and ganglion cells (see Chapter 26). In Ramón y Cajal's final paper addressing “the enigma of the amacrine cells,” he pointed out that the functions of most types of amacrine cells remained unknown almost 50 years after their discovery (Cajal, 1933). Although our present understanding of amacrine cell function is now informed by the knowledge that these cells are primarily inhibitory neurons and that they make and receive synapses on their dendrites (Dowling and Boycott, 1966), anyone who has looked down a microscope at Golgi-stained or dye-filled amacrine cells can appreciate how Cajal was bewildered by these cells.

Amacrine cells first came to prominence in the late 1880s. Although Müller (1851) had recognized that the cells at the vitread margin of the inner nuclear layer formed a distinct sublayer (spongiöse schicht), it was not until Tartuferi (1887) first applied the Golgi method to the retina that the detailed morphology of the spongioblasts was revealed. Shortly afterward, Cajal (1893) and Dogiel (1891) independently came to the conclusion that spongioblasts do not give rise to a classical axon, leading Cajal (1893) to name these inner retinal neurons amacrine cells, from the Greek a-makrós-inos meaning “without-long-fiber.” Cajal also recognized that some spongioblasts in the bird retina do give rise to a short intraretinal axon; these cells he called association spongioblasts or association amacrine cells, to distinguish them from amacrine cells proper. In keeping with Cajal's broad view, this review encompasses all retinal interneurons that receive their primary input in the inner retina, including the amacrine cells of the inner nuclear layer, the “displaced” amacrine cells of the ganglion cell layer, the association amacrine cells, and the interplexiform cells.