Non-linear amplification of graded voltage signals in the first-order visual interneurons of the butterfly Papilio xuthus.

Lamina monopolar cells (LMCs) are the first-order visual interneurons of insects and crustacea, primarily involved in achromatic vision. Here, we investigated morphological and electrophysiological properties of LMCs in the butterfly Papilio xuthus Using intracellular recording coupled with dye injection, we found two types of LMCs. Cells with roundish terminals near the distal surface of the medulla demonstrating no or small depolarizing spikes were classified as L1/2. Cells with elongated terminals deep in the medulla that showed prominent spiking were classified as L3/4. The majority of LMCs of both types had broad spectral sensitivities, peaking between 480 and 570 nm. Depending on the experimental conditions, spikes varied from small to action potential-like events, with their amplitudes and rates decreasing as stimulus brightness increased. When the eye was stimulated with naturalistic contrast-modulated time series, spikes were reliably triggered by high-contrast components of the stimulus. Spike-triggered average functions showed that spikes emphasize rapid membrane depolarizations. Our results suggest that spikes are mediated by voltage-activated Na+ channels, which are mainly inactivated at rest. Strong local minima in the coherence functions of spiking LMCs indicate that the depolarizing conductance contributes to the amplification of graded responses even when detectable spikes are not evoked. We propose that the information transfer strategies of spiking LMCs change with light intensity. In dim light, both graded voltage signals and large spikes are used together without mutual interference, as a result of separate transmission bandwidths. In bright light, signals are non-linearly amplified by the depolarizing conductance in the absence of detectable spikes.

Characterization of the first-order visual interneurons in the visual system of the bumblebee (Bombus terrestris).

The bumblebee (Bombus terrestris) has become a common model animal in the study of various aspects of vision and visually guided behavior. Although the bumblebee visual system has been studied to some extent, little is known about the functional role of the first visual neuropil, the lamina. In this work, we provide an anatomical and electrophysiological description of the first-order visual interneurons, lamina monopolar cells (LMCs), of the bumblebee. Using intracellular recording coupled with dye injection, we found that bumblebee LMCs morphologically resemble those found in the honeybee, although only the LMC type L1 cells could be morphologically matched directly between the species. LMCs could also be classified on the basis of their light response properties as spiking or non-spiking. We also show that some bumblebee LMCs can produce spikes during responses to stimulation with naturalistic light contrasts, a property unusual for these neurons.

Frequency-selective transmission of graded signals in large monopolar neurons of blowfly Calliphora vicina compound eye.

The functional roles of voltage-gated K(+)(Kv) channels in visual system interneurons remain poorly studied. We have addressed this problem in the large monopolar cells (LMCs) of the blowfly Calliphora vicina, using intracellular recordings and mathematical modeling methods. Intracellular recordings were performed in two cellular compartments: the synaptic zone, which receives input from photoreceptors, and the axon, which provides graded potential output to the third-order visual neurons. Biophysical properties of Kv conductances in the physiological voltage range were examined in the dark with injections of current in the discontinuous current-clamp mode. Putative LMC types 1/2 and 3 (L1/2 and L3, respectively) had dissimilar Kv channelomes: L1/2 displayed a prominent inactivating Kv conductance in the axon, while L3 cells were characterized by a sustained delayed-rectifier Kv conductance. To study the propagation of voltage signals, the data were incorporated into the previously developed mathematical model. We demonstrate that the complex interaction between the passive membrane properties, Kv conductances, and the neuronal geometry leads to a resonance-like filtering of signals with peak frequencies of transmission near 15 and 40 Hz for L3 and L1/2, respectively. These results point to distinct physiological roles of different types of LMCs.