Regional specializations in the eye of Aplysia, a neuronal circadian oscillator

The eye of the opisthobranch mollusc, Aplysia californica, contains a neuronal circadian oscillator system as well as a photoreceptor system. The retina contains five classes of receptors, several of which are described for the first time in this paper, and two types of neurons. The most conspicuous photoreceptor has long microvilli and is densely packed with small vesicles. The other four receptor types bear both microvilli and cilia and lack densely packed vesicles. Because of their small size, these four receptors occupy only a small fraction of the retinal area, but numerically they account for about half of the receptors. There are marked differences between the dorsal and ventral portions of the eye of Aplysia. The optic nerve head and associated bundles of axons within the retina form a boundary between two anatomically distinct regions of the eye. The microvillous photoreceptor and one of the receptors bearing both microvilli and cilia are found throughout the eye. The other three receptor types are restricted to the region ventral to the optic nerve head. One type of neuron, which has been shown in other studies to produce compound action potentials whose frequency varies with a circadian rhythm, is also found only ventral to the optic nerve head and associated axon bundles. There are also marked regional variations in cellular dimensions. The rhabdom originating from the microvillous photoreceptors is thickest in the dorsal and central retina, and the cross-sectional areas of these photoreceptors are largest dorsally. The pigmented layer is also much thicker in the dorsal retina. No other molluscan eye has been reported to have as many receptor types as Aplysia, nor has restriction of a receptor or neuronal type to a limited area been described. Regional variations in cellular dimensions have been reported previously primarily in the advanced cephalopod eyes. The significance of these unusual features is discussed in relation to both the visual properties of the eye and the circadian oscillator it contains.