RESUMEN
In dim light, scarcity of photons typically leads to poor vision. Nonetheless, many animals show visually guided behavior with dim environments. We investigated the signaling properties of photoreceptors of the dark active cockroach (Periplaneta americana) using intracellular and whole-cell patch-clamp recordings to determine whether they show selective functional adaptations to dark. Expectedly, dark-adapted photoreceptors generated large and slow responses to single photons. However, when light adapted, responses of both phototransduction and the nontransductive membrane to white noise (WN)-modulated stimuli remained slow with corner frequencies ~20 Hz. This promotes temporal integration of light inputs and maintains high sensitivity of vision. Adaptive changes in dynamics were limited to dim conditions. Characteristically, both step and frequency responses stayed effectively unchanged for intensities >1,000 photons/s/photoreceptor. A signal-to-noise ratio (SNR) of the light responses was transiently higher at frequencies <5 Hz for ~5 s after light onset but deteriorated to a lower value upon longer stimulation. Naturalistic light stimuli, as opposed to WN, evoked markedly larger responses with higher SNRs at low frequencies. This allowed realistic estimates of information transfer rates, which saturated at ~100 bits/s at low-light intensities. We found, therefore, selective adaptations beneficial for vision in dim environments in cockroach photoreceptors: large amplitude of single-photon responses, constant high level of temporal integration of light inputs, saturation of response properties at low intensities, and only transiently efficient encoding of light contrasts. The results also suggest that the sources of the large functional variability among different photoreceptors reside mostly in phototransduction processes and not in the properties of the nontransductive membrane.
Asunto(s)
Adaptación a la Oscuridad/fisiología , Células Fotorreceptoras de Invertebrados/fisiología , Potenciales de Acción , Animales , Sensibilidad de Contraste , Oscuridad , Periplaneta , FotonesRESUMEN
Shaker K(+)-channels are one of several voltage-activated K(+)-channels expressed in Drosophila photoreceptors. We have shown recently that Shaker channels act as selective amplifiers, attenuating some signals while boosting others. Loss of these channels reduces the photoreceptor information capacity (bits s(-1)) and induces compensatory changes in photoreceptors enabling them to minimize the impact of this loss upon coding natural-like stimuli. Energy as well as coding is also an important consideration in understanding the role of ion channels in neural processing. Here, we use a simple circuit model that incorporates the major ion channels, pumps and exchangers of the photoreceptors to derive experimentally based estimates of the metabolic cost of neural information in wild-type (WT) and Shaker mutant photoreceptors. We show that in WT photoreceptors, which contain Shaker K(+)-channels, each bit of information costs approximately half the number of ATP molecules than each bit in Shaker photoreceptors, in which lack of the Shaker K(+)-channels is compensated by increased leak conductance. Additionally, using a Hodgkin-Huxley-type model coupled to the circuit model we show that the amount of leak present in both WT and Shaker photoreceptors is optimized to both maximize the available voltage range and minimize the metabolic cost.