Decremental conduction of the visual signal in barnacle lateral eye

Abstract

1. There are problems associated with the notion that slow potentials alone are used to transmit information in the early stages of some visual systems. This idea and alternatives have been tested on the barnacle lateral ocellus, a simple eye with only three photoreceptors, each with its own axon about 1 cm long.2. All of the receptors have very similar properties including spectral sensitivity, and are also electrically coupled together. Impulses cannot be recorded from any of the cell bodies, all of which have been impaled as shown by dye marking.3. No impulses can be recorded externally from most of the ocellar nerve or intracellularly from the receptor axon terminals. Impulses driven by light, sometimes recorded in the final part of the nerve, are believed to originate in other axons.4. During illumination of the eye, current enters the receptor soma and leaves via the rest of the axon. This is consistent with the idea that the axon acts as a purely passive cable. The passive behaviour was also demonstrated in a comparison of the relative attenuation down the axon, of hyperpolarizations and depolarizations.5. Calculations based on the supposed electrical constants of the somas showed that the slow potential itself was unlikely to be the visual signal, since it would be enormously attenuated by passive spread down the long thin axons. To check this, the axon terminals in the supraoesophageal ganglion were penetrated and identified by electrical and dye-marking criteria. In fact, the slow potential was attenuated in the most favourable case only by a factor of about three, indicating an axon membrane resistance in the range of 10(5) Omega. cm(2).6. This resistance may be substantially higher than that of the soma surface membrane, corrected for increased surface area. The sheath around each axon probably does not influence the electrical properties, judged by its permeability to the small molecule of Procion Yellow.7. The minimal loss of voltage in the axon and the absence of regenerative activity implicate the slow potential itself as the visual signal. But there remains the alternative that light triggers some unknown transmission process, of which the slow potential is only an incidental by-product. If this were so, artificially imposed changes of membrane potential should not duplicate the action of light in promoting synaptic transmission. To test this, receptors were polarized by currents through the pipette whilst visually driven post-synaptic cells in the oesophageal connectives were being monitored. Currents could effectively substitute for lights to produce post-synaptic impulse trains of similar form and latency, confirming that the potential change produced by light is the normal visual signal.8. Only increases of receptor membrane potential stimulate the particular post-synaptic axons examined, which give ;off' responses to light. Transmission from the receptors is a voltage-dependent process which is most sensitive when a receptor is hyperpolarized from an already depolarized level.9. The discrimination of small visual signals from intrinsic axon noise is discussed, and should pose no problem in the case of the barnacle, where the smallest effective signal measured was about 0.3 mV in the soma. In other eyes where the problem may be more severe, electrical junctions between receptors could significantly improve the signal/noise ratio.