Non-linear amplification of graded voltage signals in the first-order visual interneurons of the butterflyPapilio xuthus

Abstract

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 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.

Chromatic information processing in the first optic ganglion of the butterfly Papilio xuthus

“…In our previous study, we reported that depolarizing offspikes could be recorded in some Papilio LMCs (Rusanen et al 2018). However, we found that the off-spike generation was an unstable trait, presumably related to the Naka-Rushton function: For typical LMCs, the exponential slope n is 1.02 and the stimulus intensity eliciting 50% V max (logK) is − 2.68; for slow LMC-like units n = 0.47 and logK = − 0.4; and for extracellular potential n = 0.54 and logK = − 1.01. k Latencies (i.e., time taken for the membrane potential to reach its peak) of hyperpolarizing ontransients under different light intensities for typical LMCs (N = 31), slow LMC-like units (N = 13), and extracellular potentials (N = 5).…”

Luminance Information Is Required for the Accurate Estimation of Contrast in Rapidly Changing Visual Contexts

“…Physiologically different LMC subtypes have been described in different species. For example, LMCs in bumblebees and butterflies exhibit sustained components [50,51], and motionsensitive neurons perform better than photoreceptor responses predict in the nocturnal hawkmoth [32,52]. Interestingly, presynaptic L2 and L3 calcium signals are highly reminiscent of sustained and transient calcium signals in bipolar cells of the vertebrate retina [53][54][55].…”

Immunolocalization suggests a role of the histamine‐gated chloride channel PxHCLB in spectral opponent processing in butterfly photoreceptors

“…Situation is similar in Papilio , where PxHCLA immunoreactivity is found in the medulla layers 2, 4, 5a, and 6–8 (Figure a,c). The layer 4 contains histamine‐containing lvf terminals (Hamanaka et al, ) as well as terminals of some LMCs (Ribi, ; Rusanen, Frolov, Weckström, Kinoshita, & Arikawa, ). Therefore, those PxHCLA‐positive cells may be LMCs.…”