Photoreceptors in the eye basically provide information about light intensities from which brains extract different kinds of visual cues (e.g. color, movement, pattern). How do the properties and response characteristic of visual interneurons differ from the periphery to the central brain? I intracellularly recorded from neurons in the second and third optic ganglia (medulla and lobula) and the central brain (protocerebrum) of bees (mainly bumblebees; Bombus impatiens) while presenting color and motion stimuli. Bees rely on such stimuli during flight and foraging and show sophisticated visual learning abilities. We found that neurons in the distal medulla are color specific while ones in the proximal medulla show complex, often antagonistic color responses. Neurons in the distal lobula (layers 1-4) mainly process motion information while the proximal lobula (layers 5 and 6) seems to combine color and motion responses. Anterior parts of the central brain receive complex input representing combinations of motion and color information characterized by specific temporal properties (e.g. temporal precision, 'novelty' information or entrainment). This kind of often sparsely coded information is also represented in the mushroom bodies, learning and memory centers in the insect brain. In contrast, posterior parts of the central brain receive mainly motion information and show more reliable responses yet less precise spike timing. While the former kind of information (temporally precise or novelty in anterior pathways) is suited to form stimulus associations relevant during foraging, the latter, more reliable information is thought to support fast optomotor flight control maneuvers and other less plastic behaviors.

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.

A key function of the nervous system is to sample data from the external world, generate internal signals, and transform them into meaningful information that can be used to trigger behaviour. In order to gain insight into the underlying mechanism for signal transformation, the visual system has been extensively studied: partly owing to the stimulus being reliably presentable, and the anatomy being well described. The Drosophila visual system is one such system, with the added advantage of genetic tractability. In this thesis, I studied the filtering property of visual neurons at two levels, biophysical and circuit levels. The first study looks at signal transformation at the biophysical level, at the input of the visual system, in photoreceptors. Voltage-gated potassium channels counteract the depolarization caused by opening of light sensitive channels, and the heterogeneous properties of their kinetics can fine-tune the photoreceptor’s frequency response to fulfill the animal’s ecological requirements. Shaker (Kv1) and Shab (Kv2) have been identified as fast and slow inactivating components of the photoreceptor’s outward currents, however a current with intermediate kinetics (IKf) has not been molecularly identified, but had been postulated to be Shal (Kv4). I focused on characterizing this current using whole-cell patch clamp in wild type and mutants, and using antibodies for Shal. My results from whole-cell patch clamp indicated that IKf in adult R1-6 cells are not Shal, from their voltage dependence and insensitivity to a Kv4 blocker. This calls for alternative molecular basis for IKf, which is likely to be a slow inactivating component of Shaker, or a combination of its many splice variants. The second study looks at signal transformation at the circuit level, at the output end, in the third optic neuropil, lobula. Visual projection neurons project from the lobula to the central brain, and have been proposed to carry behaviourally relevant visual features to higher brain regions. It was recently shown that optogenetic activation of individual visual projection neuron types could induce distinct behaviours such as takeoff and backward walking, linking these visual neurons to specific behavioural programs downstream. Using in vivo two-photon calcium imaging, I recorded visually evoked calcium responses from three of these cell types. Cell types that showed induced takeoff and backward walking preferentially responded to dark looming stimuli or fragmented expanding local features, suggesting their role in behaviours triggered by object approach. To explore how this visual information is transformed in the downstream circuit, we identified several candidate neurons that receive input from this cell type by anatomical overlap, and then validated their connections using optogenetic activation and calcium imaging. One downstream cell-type that projects bilaterally had very similar response properties to its upstream partner, whereas another cell-type that projects ipsilaterally seemed to filter out some information from its upstream partner. This is one of the first studies that functionally characterizes lobula visual projection neurons and their downstream partners in Drosophila, and their response properties agree with the general idea that visual information becomes increasingly selective as it is sent to higher brain regions.