Photocurrents have been recorded from the red spot of the isolated superfused pigeon retina. The technique used was to record photovoltage gradients and extracellular fluid resistivity in a direction parallel with the long axes of the receptors. 2. Cone and rod responses were identified, and experiments designed so that only the former were elicited. 3. In the outer portion of the receptor layer, the wave form of the cone photoresponse lacks the initial transient (the 'nose') seen in the portions of the receptor layer nearer the synapses. It is argued that this observation permits the use of a simple equivalent circuit for the generation of the extracellular photocurrent, to infer membrane properties from extracellular recordings. 4. When the superfusing Ringer is changed to one which has a very low calcium activity (2 X 10(-7)M) the first result is that photoresponses increase in magnitude (X 7.7) but the relationship between light intensity and response amplitude and the light intensity (sigma) required to produce a half maximal response remains unchanged. 5. This increase in photocurrent in low calcium also occurs if the superfusing fluid is cooled to 10 degrees. 6. After 2--3 min, the photoresponses in low calcium begin to decrease in amplitude, and the value of sigma is progressively reduced, tenfold in 10 min. 7. During this time, the wave form of the photocurrent alters, the rate of increase and decrease of the responses being slowed. 8. The relationship between peak photocurrent and duration of light flash is modified. 9. The response to a step of light is not well maintained in higher calcium, but is well maintained in low calcium. 10. In higher calcium, the current overshoots during recovery from a flash to below the previous dark level. This does not happen in low calcium. 11. In low calcium, a light adapting background illumination desensitizes the cones. All changes in wave form of the response can be accounted for in terms of the membrane non-linearities. The calculated time course of the change in concentration of the 'internal transmitter' is unaffected. The same is true of desensitization, in the dark, following exposure to intense illumination.
