Photoreceptors can be used as model systems for signal processing, involving input signals in the form of light-gated current, modulation of the resulting voltage signals by voltage-dependent channels, and output by synaptic transmission to interneurons . Nocturnal or crepuscular insects such as the cockroach have to cope with dim environments, where the reliability of visual information decreases due to the stochastic nature of photon arrival and relatively large transduction noise . We have for the first time characterized in detail the electrical membrane properties in photoreceptors of an insect adapted to dark, the cockroach Periplaneta americana.
Several anatomical and physiological strategies for improving dim light vision exist in the insect visual systems. Compound eye optics, photoreceptor properties and the later neural processes can be optimized for efficient light capture and signal transmission . At the photoreceptor level, common strategies used by nocturnal arthropods include temporal summation by the low-pass properties of phototransduction and the photo-insensitive membrane, large-amplitude single photon responses and a large rhabdomere that increases the photon catch [39, 40]. Spatial summation of signals from several photoreceptors in the 2nd order neurons of the Lamina can further improve vision under conditions where the number of photons is very small [41–43]. A conclusion that can be made from these studies is that, when only a small number of photons are absorbed by the photoreceptors, sufficient visual information is acquired through sacrificing either spatial or temporal resolution, or both. Our new results show how the voltage-dependent channels fit into this big picture in the cockroach photoreceptors. Both the experimental approach, patch-clamping of the photoreceptors in the isolated ommatidia, and the theoretical approach, mathematical modelling, are used to gain mechanistic understanding. Interestingly, our results show that the Kv channel composition in the cockroach photoreceptors does not follow the pattern found previously in the Diptera [10, 11].
As can be expected, temporal integration in the cockroach photoreceptors is clearly one of the main visual adaptations for life in the dark . It limits coding to the relatively slow visual signals compared to the fast-flying diurnal flies, whose photoreceptors respond to much higher stimulus frequencies [44, 45]. In cockroach photoreceptors low-pass filtering arises from the slow phototransduction (Figure 1C-D) and the electrical properties of the membrane (Figure 1E), manifested in the large whole-cell resistance and capacitance. The capacitance ensues from the rhabdomere’s large microvillar area that increases the photon capture efficiency of the cells . The high resistance in the dark and at rest combined with the large capacitance yields a slow time-constant: ca. 60 ms with typical membrane capacitance of 400 pF and resistance of 150 MΩ at -60 mV. This corresponds to a temporal low-pass filter with a cut-off frequency of ca. 3 Hz. For comparison, in dark-adapted photoreceptors of the diurnal blowfly Calliphora vicina, membrane resistance and time constant are 32 MΩ and 4 ms, resulting in a corner frequency of 25 Hz, which in light-adaptation is nearly tripled to 72 Hz . In cockroach photoreceptors the high input resistance near the resting potential amplifies single photon responses, enabling large amplitude voltage bumps.
During light responses the membrane gain and speed are strongly modulated by voltage-gated channels. The dark- and day-active Dipteran fly species possess varying Kv channel compositions dominated by either A-type or DR channels, respectively [10, 11]. This is considered to result from the optimization between the need for faster vision and the subsequent increase in the metabolic costs [2, 4]. Moreover, some insects that are active during both day and night demonstrate circadian changes in the Kv channels, with transient currents expressed at the night and sustained currents during the day [47, 48]. It was therefore surprising that the dominant Kv current in the nocturnal cockroach was the noninactivating KDR (Figure 2).
Our results show that the conductances activated with the depolarization are relatively specific for K+, and thus it is plausible that they are created by the Kv-channels (Figure 3). The voltage-activated currents could be separated into two components, the sustained non-inactivating KDR and the transient inactivating current KA (Figure 4. and the Appendix). Although both KDR and KA showed some of the typical characteristics of previously described insect Kv-channels, most importantly the voltage-dependence of activation and inactivation and the sensitivity to various Kv blockers (Figure 6; compare to channels in .), the molecular identities of the channels remain unknown. However, the insensitivity of KA to the Drosophila Shaker blocker αDTX suggests that KA is not coded by the Shaker gene. KDR was activated already at the -60 mV resting potential in dark, contributing almost 90% of total membrane conductance. Therefore KDR participates in shaping even the smallest light responses, the quantum bumps, and may be required to prevent or attenuate saturation with transient increases of light. Simulations showed that similarly to the sustained Kv currents in the photoreceptors of other species, KDR adjusts the speed and amplitude of the light-induced voltage responses [10, 11, 13].
The role of the transient Kv conductance, KA, is more difficult to assess. KA conductance at the dark resting potential was small (< 0.1 nS) and computer simulations demonstrated that KA had no significant role in prolonged light responses. Because of its rapid inactivation, even a 10-fold simulated increase in the KA conductance or various manipulations of voltage-dependent properties of KA had no significant effect on the light response (Figure 10). An increase in the KA current during the initial voltage transient was observed when the dark resting potential was set below the experimentally determined values. However, the physiological relevance of this finding is likely to be very small because the membrane voltage is rarely below the dark resting potential during the light stimuli. For high intensity light stimuli, the cation influx through the light-sensitive channels may induce exchanger and pump activity, which can lead to a brief hyperpolarization below the resting potential . It is possible that some of the cells in vivo could have more negative resting potentials where KA channels could be more effectively activated. However, no systematic variation of the resting potential was found during this work, neither has this been reported in earlier studies .
Besides the inter-species differences in Dipteran photoreceptor Kv channels , Kv channel expression can vary within the same species between photoreceptors with different functional and structural properties. In Drosophila, blue- and UV-sensitive photoreceptors with longer axons express larger transient Kv conductances than green-sensitive cells with short axons . The transient conductance (as opposed to the alternative sustained DR type) has been suggested to decrease the attenuation of the voltage signals during propagation to the 2nd order cells. Since cockroach photoreceptors have exceptionally long axons reaching over 1 mm , KA could serve a similar function.
Previous studies  and the data presented here (Figure 5A&C) indicate that a fraction of cockroach photoreceptors exhibit a particular strongly-adapting phenotype, characterized by higher KA conductance and smaller whole-cell capacitance than photoreceptors on average. In vivo intracellular recordings with sharp electrodes have earlier demonstrated the presence of action potential-like signals in the photoreceptor axons  and simulations of spiking hyper-adapting photoreceptors have shown that such combination efficiently encodes transient light intensity changes . Generally, A-type Kv conductances regulate several aspects in spiking neurons [32, 33, 52]. We therefore hypothesize that the KA conductance could be important in tuning the transient responses in a sub-population of photoreceptors, related to signalling with either transient graded potentials or spikes in the axons. However, good quality intracellular recordings from the thin axons, 0.5 - 1 μm in diameter are lacking at present.
The functional role of the hyperpolarization activated IR current (Figure 7) is enigmatic, because its activation range is well below physiological signalling range. It could be related to transient hyperpolarization of the membrane after strong light stimulation . Although a detailed study of its possible physiological function is beyond the scope of this paper, our results show that it is not carried by potassium and that substitution experiments are in accordance to its being a chloride conductance. These findings resemble a chloride current mediated by the CLC-2 channels , which have also been reported in the Drosophila photoreceptors .