To avoid the fierce competition for food, South African ball-rolling dung beetles carve a piece 4 of dung off a dung-pile, shape it into a ball and roll it away along a straight line path. For this 5 unidirectional exit from the busy dung pile, at night and day, the beetles use a wide repertoire 6 of celestial compass cues. This robust and relatively easily measurable orientation behavior has 7 made ball-rolling dung beetles an attractive model organism for the study of the neuroethology 8 behind insect orientation and sensory ecology. Although there is already some knowledge 9 emerging concerning how celestial cues are processed in the dung beetle brain, little is known 10 about its general neural layout. Mapping the neuropils of the dung beetle brain is thus a 11 prerequisite to understand the neuronal network that underlies celestial compass orientation. 12Here, we describe and compare the brains of a day-active and a night-active dung beetle species 13 based on immunostainings against synapsin and serotonin. We also provide 3D reconstructions 14 for all brain areas and many of the fiber bundles in the brain of the day-active dung beetle. 15Comparison of neuropil structures between the two dung beetle species revealed differences 16 that reflect adaptations to different light conditions. Altogether, our results provide a reference 17 framework for future studies on the neuroethology of insects in general and dung beetles in
In a microvillar photoreceptor, absorption of an incident photon initiates a phototransduction reaction that generates a depolarizing light-induced current (LIC) in the microvillus. Although in-depth knowledge about these processes in photoreceptors of the fruitfly Drosophila is available, not much is known about their nature in other insect species. Here, we present description of some basic properties of both elementary and macroscopic LICs and their Ca2+-dependence in the photoreceptors of a dark-active species, the cockroach Periplaneta americana. Cockroach photoreceptors respond to single photon absorptions by generating quantum bumps with about 5-fold larger amplitudes than in Drosophila. At the macroscopic current level, cockroach photoreceptors responded to light with variable sensitivity and current waveform. This variability could be partially attributed to differences in whole-cell capacitance. Transient LICs, both elementary and macroscopic, showed only moderate dependence on extracellular Ca2+. However, with long light pulses, response inactivation was largely abolished and the overall size of LICs increased when extracellular Ca2+ was omitted. Finally, by determining relative ionic permeabilities from reversals of LICs, we demonstrate that when compared to Drosophila, cockroach light-gated channels are only moderately Ca2+-selective.
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
Optimization of sensory processing during development can be studied by using photoreceptors of hemimetabolous insects (with incomplete metamorphosis) as a research model. We have addressed this topic in the stick insect Carausius morosus, where retinal growth after hatching is accompanied by a diurnal-to-nocturnal shift in behavior, by recording from photoreceptors of first instar nymphs and adult animals using the patch-clamp method. In the nymphs, ommatidia were smaller and photoreceptors were on average 15-fold less sensitive to light than in adults. The magnitude of A-type K ϩ current did not increase but the delayed rectifier doubled in adults compared with nymphs, the K ϩ current densities being greater in the nymphs. By contrast, the density of light-induced current did not increase, although its magnitude increased 8.6-fold, probably due to the growth of microvilli. Nymph photoreceptors performed poorly, demonstrating a peak information rate (IR) of 2.9 Ϯ 0.7 bits/s versus 34.1 Ϯ 5.0 bits/s in adults in response to white-noise stimulation. Strong correlations were found between photoreceptor capacitance (a proxy for cell size) and IR, and between light sensitivity and IR, with larger and more sensitive photoreceptors performing better. In adults, IR peaked at light intensities matching irradiation from the evening sky. Our results indicate that biophysical properties of photoreceptors at each age stage and visual behavior are interdependent and that developmental improvement in photoreceptor performance may facilitate the switch from the diurnal to the safer nocturnal lifestyle. This also has implications for how photoreceptors achieve optimal performance.
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