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Laboratory of Neurophysiology, National Institute of Neurological and Communicative Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20014, U.S.A.

1. Light responses were recorded from the photoreceptors of Hermissenda crassicornis. The response to a flash is a complex potential change involving an initial depolarization, a hyperpolarization, and a depolarizing tail. None of the phases of the response are due to synaptic interactions.

2. Polarization of the membrane by extrinsic current indicates that three separate conductance changes are associated with the response. The initial depolarization and hyperpolarization are accompanied by conductance increases and the tail with a conductance decrease. The initial depolarization has a positive reversal potential and the hyperpolarizing and tail phase have a reversal voltage more negative than resting potential.

3. The different processes that give rise to the conductance changes have similar spectral sensitivities but are affected unequally by light adaptation. Strong light adaptation reduced the depolarizing phases more than the hyperpolarizing phase, so that following an adapting stimulus the cell responded to illumination with a pure hyperpolarization (isolated hyperpolarization).

4. Removal of external Na⁺ ions greatly reduced the initial depolarization. In Na⁺-free sea water the cell responds to dim flashes with a slow depolarization (isolated tail) that involves a conductance decrease, and has the same reversal potential as the hyperpolarizing response recorded from light adapted cells.

5. The amplitude of the isolated hyperpolarization and tail varied inversely with the external K⁺ concentration.

6. It is concluded that in Hermissenda photoreceptors light initiates processes that result in three distinct permeability changes. Following a brief flash there is: a rapid and transient increase in Na⁺ permeability that is responsible for the initial depolarization, a less rapid increase in K⁺ permeability that is responsible for the hyperpolarizing phase, and a delayed decrease in K⁺ permeability that gives rise to the depolarizing tail.

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