INTRODUCTION:Whirligig beetles (Coleoptera: Gyrinidae) are aquatic insects living on the water surface. They are equipped with four compound eyes, an upper pair viewing above the water surface and a lower submerged pair viewing beneath the water surface, but little is known about how their visual brain centers (optic lobes) are organized to serve such unusual eyes. We show here, for the first time, the peculiar optic lobe organization of the larval and adult whirligig beetle Dineutus sublineatus.RESULTS:The divided compound eyes of adult whirligig beetles supply optic lobes that are split into two halves, an upper half and lower half, comprising an upper and lower lamina, an upper and lower medulla and a bilobed partially split lobula. However, the lobula plate, a neuropil that in flies is known to be involved in mediating stabilized flight, exists only in conjunction with the lower lobe of the lobula. We show that, as in another group of predatory beetle larvae, in the whirligig beetle the aquatic larva precociously develops a lobula plate equipped with wide-field neurons. It is supplied by three larval laminas serving the three dorsal larval stemmata, which are adjacent to the developing upper compound eye.CONCLUSIONS:In adult whirligig beetles, dual optic neuropils serve the upper aerial eyes and the lower subaquatic eyes. The exception is the lobula plate. A lobula plate develops precociously in the larva where it is supplied by inputs from three larval stemmata that have a frontal-upper field of view, in which contrasting objects such as prey items trigger a body lunge and mandibular grasp. This precocious lobula plate is lost during pupal metamorphosis, whereas another lobula plate develops normally during metamorphosis and in the adult is associated with the lower eye. The different roles of the upper and lower lobula plates in supporting, respectively, larval predation and adult optokinetic balance are discussed. Precocious development of the upper lobula plate represents convergent evolution of an ambush hunting lifestyle, as exemplified by the terrestrial larvae of tiger beetles (Cicindelinae), in which activation of neurons in their precocious lobula plates, each serving two large larval stemmata, releases reflex body extension and mandibular grasp.

Flies are highly visually guided animals. In this thesis, I have used hoverflies as a model for studying motion vision. Flies process motion vision in three visual ganglia: the lamina, the medulla, and the lobula complex. In the posterior part of lobula complex, there are around 60 lobula plate tangential cells (LPTCs). Most of LPTCs have large receptive fields where the local direction sensitivity suggests that they function as matched filters to specific types of optic flow. LPTCs connect to descending or neck motor neurons that control wing and head movements, respectively. Therefore, in this thesis I have focused on the electrophysiological responses of LPTCs to gain understanding of visual behaviors in flies. The elementary motion detector (EMD) is a model that can explain the formation of local motion sensitivity. However, responses to higher order motion, where the direction of luminance change is uncorrelated with the direction of movement, cannot be predicted by classic EMDs. Nevertheless, behavior shows that flies can see and track bars with higher order motion cues. I showed (Paper I) that several LPTCs also respond to higher order motion. Many insects, including flies, release octopamine during flight. Therefore, adding octopamine receptor agonists can mimic physical activity. Our study (Paper II) investigated the effect of octopamine on three adaptation components. We found that the contrast gain reduction showed a frequency dependent increase after octopamine stimulation. Since the contrast gain is non-directional, it is likely presynaptic to the LPTC. We therefore believe that octopamine acts on the delay filter in the EMD. In the third paper we describe a novel LPTC. The centrifugal stationary inhibited flicker excited (cSIFE) is excited by flicker and inhibited by stationary patterns. Neither of these responses can be predicted by EMD models. Therefore, we provide a new type of motion detector that can explain cSIFE’s responses (Paper III). During bar tracking, self-generated optic flow may counteract the steering effect by inducing a contradictory optomotor response. Behavior shows that during bar fixation, flies ignore background optic flow. Our study (Paper IV) focus on the different receptive fields of two LPTCs, and relate these to the bar fixation behavior. In the neuron with a small and fronto-dorsal receptive field, we find a higher correlation with bar motion than with background motion. In contrast, the neuron with a larger receptive field shows a higher correlation with background motion.