Signal coding in cockroach photoreceptors is tuned to dim environments

Abstract

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.