Neuronal Circuits in Cephalopod Vision

Abstract

Cephalopods have a sophisticated visual system that is comparable in overall performance to many vertebrate visual systems. Although the eyes of cephalopods and vertebrates have strong similarities, their central processing systems seem anatomically very different. In this paper we investigate the mechanism used by cephalopods for analysing visual signals, with a view to comparing this with vertebrate systems. The cephalopod retina is comparatively simple containing only photoreceptors, supporting cells, and an efferent innervation. The retina is topographically mapped onto the optic lobe via a chiasma that inverts the visual map. Within the optic lobe most photoreceptor axons terminate in a complex ncuropil area, the outer plexiform zone. This zone receives connections from many different cell types and stains positively for most of the major neurotransmitters; this is undoubtedly an important processing area. Using 400 μm slices from the optic lobe, field potentials were recorded from this area in response to stimulation of the optic nerves; these showed a complex potential in the plexiform layers, indicating synaptic activity in this zone. This activity could be abolished by synaptic blocking agents. The spatial extent of this activity was revealed by an optical recording method, whereby the slice was stained with a voltage-sensitive dye and a fast video system was used to image the responses to electrical stimulation. This confirmed that the activity from the retinal photoreceptors excites follower cells in the plexiform zone, probably the small amacrine cells, and that this spreads along the margin of the zone to cover a distance of about 400 μm. The signal could not be followed further in transverse slices. These experiments provide evidence for the first steps in our understanding of visual processing in cephalopods and demonstrate the advantages of combining electrical and optical recordings in the analysis of complex neural processing.