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

Abstract

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.

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

“…Many LMCs responded to NS with a combination of graded potentials and spikes. To examine the functional relationship between the aspects of the stimulus and spikes, we calculated the spike-triggered average (STA) as described previously (Rusanen et al, 2017), by excising and averaging stimulus segments preceding the spike. To detect a spike, an algorithm combining template matching with simple voltage thresholding was used.…”

“…The second template had an amplitude of 22.7±7.5 mV and a half-width of 3.6±0.9 ms (n=75). These templates were then used to detect spikes (Rusanen et al, 2017). The minimal spike amplitude was determined as mean minus 2 s.d.…”

“…LED calibration was performed using a spectrometer (USB4000, Ocean Optics, Dunedin, FL, USA). Spectral sensitivities of LMCs were determined using a modified flash method as described previously (Rusanen et al, 2017). The isoquantal flash response series were usually recorded at least twice and the response amplitudes were averaged to improve accuracy.…”

“…Although LMCs are traditionally regarded as graded potentialsignaling neurons, it has been repeatedly shown that fast transient depolarizing events called spikes can be elicited (Järvilehto and Zettler, 1971;Zettler and Järvilehto, 1971;Hardie and Weckström, 1990;Rusanen et al, 2017). In the blowfly, spikes can be observed when a LMC is depolarized after light-induced hyperpolarization.…”

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].…”