Photoresponses of a sensitive extraretinal photoreceptor in Aplysia

1. The light-evoked membrane current, photo-current, of an extraretinal photo-receptor, the ventral photoresponsive neurone (v.p.n.), in the abdominal ganglion of Aplysia californica, was studied using the voltage clamp method. Flashes and steps of monochromatic light were used as stimuli. 2. Flashes of light 100 msec in duration elicit slowly developing outward currents which peak at 5--10 sec and then return to dark levels within 30--60 sec. 3. The peak of the action spectrum of v.p.n. is at 470 nm and is similar to the peak for R2, another photoresponsive extraretinal Aplysia neurone, and to the peak of absorption spectra of molluscan rhodopsins. V.p.n. also contains membrane-bound cytoplasmic pigmented granules similar to those found in R2, and these are thought to mediate the light response. 4. Photo-current is associated with an increase in membrane conductance. In normal sea water photo-current has a reversal potential at the K equilibrium potential, EK and the reversal potential has a Nernstian relationship with external K concentration. The current--voltage relationships for peak and steady-state photo-current are fitted by the same constant field equation; currents measured when voltage was changed in steps at peak photo-current also have a similar relationship with voltage. The results are similar when saturating or non-saturating light intensities were used. Thus it appears that the light-activated K+ conductance is neither time nor voltage dependent. 5. Minimally detectable responses occurred at flash photon densities of 10(12) photons cm-2 which is 10(-3) that for R2. This value is comparable to those reported for retinal photoreceptors of Pecten irradians, a scallop, and Salpa democratica, a pelagic tunicate, and is lower than values reported for extraretinal photoreceptors such as the pineal photoreceptors of Salmo gairdnerii irideus, the rainbow trout, and the caudal photoreceptor in the sixth abdominal ganglion of Procambarus clarkii, a crayfish. 6. V.p.n. has a linear amplitude response range for low intensities of light and a non-linear range that saturates at high intensities. In the accompanying paper the response wave form and its temperature dependence are interpreted according to a diffusion-based model.