The compound eyes of insects contain photoreceptors in small eyelets, ommatidia. The photoreceptors generally vary very little from ommatidium to ommatidium. However, in the large compound eyes of the cockroach (Periplaneta americana), previous studies have shown large differences in the optical structure between the ommatidia. The anatomy suggests pooling of 6 -20 photoreceptor signals into one second-order cell in the first synapse. Here, we show and characterize an unexpectedly large and seemingly random functional variability in the cockroach photoreceptors in terms of sensitivity, adaptation speed, angular sensitivity, and signal-to-noise ratio. We also investigate the implications of action potentials, triggered by the light-induced membrane depolarization in the photoreceptor axons. The combination of the functional features reported here is unique among the compound eyes. Recordings from the proximal parts of the thin and long photoreceptor axons or small and distant second-order neurons are not practical with the present methods. To alleviate this lack of data, we used computer simulations mimicking the functional variability, spike coding, and pooling of 12 photoreceptor signals, on the basis of our recordings from the photoreceptor somata and distal axons. The predicted responses of a simulated second-order cell follow surprisingly reliably the simulated light stimuli when compared with a simulation of functionally identical photoreceptors. We hypothesize that cockroach photoreceptors use action potential coding and a kind of population coding scheme for making sense of the inherently unreliable light signals at low luminance and for optimization of vision in its mainly dim living conditions.

Reliable vision in dim light depends on the efficient capture of photons. Moreover, visually guided behaviour requires reliable signals from the photoreceptors to generate appropriate motor reactions. Here, we show that at behavioural low-light threshold, cockroach photoreceptors respond to moving gratings with single-photon absorption events known as 'quantum bumps' at or below the rate of 0.1 s −1 . By performing behavioural experiments and intracellular recordings from photoreceptors under identical stimulus conditions, we demonstrate that continuous modulation of the photoreceptor membrane potential is not necessary to elicit visually guided behaviour. The results indicate that in cockroach motion detection, massive temporal and spatial pooling takes place throughout the eye under dim conditions, involving currently unknown neural processing algorithms. The extremely high night-vision capability of the cockroach visual system provides a roadmap for bio-mimetic imaging design.

Heimonen K, Immonen E-V, Frolov RV, Salmela I, Juusola M, Vähäsöyrinki M, Weckström M. Signal coding in cockroach photoreceptors is tuned to dim environments. J Neurophysiol 108: 2641-2652, 2012. First published August 29, 2012 doi:10.1152/jn.00588.2012.-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, darkadapted 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 ϳ20 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 Ͼ1,000 photons/s/photoreceptor. A signal-to-noise ratio (SNR) of the light responses was transiently higher at frequencies Ͻ5 Hz for ϳ5 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 ϳ100 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.vision; systems analysis; adaptation; temporal resolution; photons SENSORY SYSTEMS PROVIDE ANIMALS with necessary information for survival and reproduction. Like all senses of different species, visual systems are thought to have selectively adapted for functioning under their prevailing environmental conditions during their evolution and development

Night vision is ultimately about extracting information from a noisy visual input. Several species of nocturnal insects exhibit complex visually guided behaviour in conditions where most animals are practically blind. The compound eyes of nocturnal insects produce strong responses to single photons and process them into meaningful neural signals, which are amplified by specialized neuroanatomical structures. While a lot is known about the light responses and the anatomical structures that promote pooling of responses to increase sensitivity, there is still a dearth of knowledge on the physiology of night vision. Retinal photoreceptors form the first bottleneck for the transfer of visual information. In this review, we cover the basics of what is known about physiological adaptations of insect photoreceptors for low-light vision. We will also discuss major enigmas of some of the functional properties of nocturnal photoreceptors, and describe recent advances in methodologies that may help to solve them and broaden the field of insect vision research to new model animals.This article is part of the themed issue 'Vision in dim light'.

1. The voltage responses to light of dark-adapted cockroach photoreceptors were recorded from the somata in the retina and the axons below the two basement membranes. 2. One or more spike-like fast depolarizations superimposed on the graded receptor potential were recorded in photoreceptor axons identified by Lucifer yellow injections. These spikes are voltage dependent in as much as they could be elicited with depolarizing current pulses as well as with light stimuli. In photoreceptor somata only graded receptor potentials were recorded. 3. The physiological function of these axonal spikes may be to serve as an amplification mechanism that counteracts the unfavorable combination of photoreceptor geometry and electrical properties.