Sublinear summation of responses in locust photoreceptors

Abstract

Summary. The response of a locust, Locusta miyratoria,photoreceptor to a simultaneous pair of dim flashes is smaller than the sum of the responses to the individual component flashes, even when the photon absorption sites are separated by a distance of 120 ~tm, which should prevent them from interacting biochemically. A similar depression is observed when a flash is paired with a depolarizing current instead of a second flash, irrespective of whether the flash response precedes or follows the current response. These results indicate that the sublinear summation is caused by the activation of a voltageactivated shunting conductance. This conductance is not blocked by low intracellular concentrations of tetraethylammonium chloride, and is therefore different from the conductance which causes the decrease of the receptor's step response from transient to steady-state.

The dynamic nonlinear behavior of fly photoreceptors evoked by a wide range of light intensities

“…In these terms, the behavior of a light-adapted photoreceptor is much simpler than a dark-adapted one, and the NLN model (with only second-order nonlinearity) fitted the responses quite well with a small residual mean square error. The output nonlinearity seems to be a simple compression, consistent with self-shunting of the membrane (Laughlin, 1981) enhanced by voltage-dependent mechanisms (Pece and French, 1992). Increased activation or deactivation of sion of the membrane potential range in light-adapted blowfly photoreceptors (Weckstrom et al, 1991).…”

“…Although the Hammerstein model gave a better fit to the data than a second-order Volterra system, there is significant evidence available for nonlinearities at the end of the phototransduction process. These include self-shunting of the light-induced conductance and voltage-activated conductances (Laughlin, 1981;Laughlin and Weckstrom, 1989;Weckstrom et al, 1991;Pece and French, 1992;Tsukahara, 1980). We therefore added a second static nonlinear component to the Hammerstein model to produce the nonlinear/ linear/nonlinear sandwich model (NLN model) shown in Fig.…”

“…Similar processes would also be expected to occur in lightadapted receptors, but the background light intensity of 106 ep/s means that the steps of light caused more limited changes in the numbers of photons being transduced, which might explain the more linear responses. It is difficult to explore this problem in isolation because nonlinear behavior occurs in photoreceptors transducing only two photons together, probably by membrane conductance changes (Dubs, 1981;Pece and French, 1992).…”

“…In insects, such gain control can occur with stimuli of only a few photons (Dubs, 1981; French and Kuster, 1985;Grzywacz and Hillman, 1985). Recently, one of these processes has been identified as voltage-activated ion channels that reduce the change in membrane potential by shunting the light-gated current (Laughlin and Weckstrom, 1989;Weckstrom et al, 1991;Hardie et al, 1991;Pece and French, 1992).…”

Static and Dynamic Adaptation of Insect Photoreceptor Responses to Naturalistic Stimuli

“…Although linear convolution with a filter function provided a close description to single flash responses and random fluctuations around a mean light intensity, insect photoreceptors clearly demonstrate nonlinear adaptation, even under asymptotically small signal conditions (Marmarelis and McCann, 1977; Laughlin and Hardie, 1978; Pece and French, 1992). Nonlinear analyses of flash responses and frequency responses suggested that the processes between light absorption and membrane conductance change included both an early gain reduction and a late saturation with light intensity (Weckström et al, 1988; Pece et al, 1990; French et al, 1993).…”