Spatial tuning of translational optic flow responses in hawkmoths of varying body size

To safely navigate their environment, flying insects rely on visual cues, such as optic flow. Which cues insects can extract from their environment depends closely on the spatial and temporal response properties of their visual system. These in turn can vary between individuals that differ in body size. How optic flow-based flight control depends on the spatial structure of visual cues, and how this relationship scales with body size, has previously been investigated in insects with apposition compound eyes. Here, we characterised the visual flight control response limits and their relationship to body size in an insect with superposition compound eyes: the hummingbird hawkmoth Macroglossum stellatarum. We used the hawkmoths’ centring response in a flight tunnel as a readout for their reception of translational optic flow stimuli of different spatial frequencies. We show that their responses cut off at different spatial frequencies when translational optic flow was presented on either one, or both tunnel walls. Combined with differences in flight speed, this suggests that their flight control was primarily limited by their temporal rather than spatial resolution. We also observed strong individual differences in flight performance, but no correlation between the spatial response cutoffs and body or eye size.

Hawkmoth lamina monopolar cells act as dynamic spatial filters to optimize vision at different light levels

How neural form and function are connected is a central question of neuroscience. One prominent functional hypothesis, from the beginnings of neuroanatomical study, states that laterally extending dendrites of insect lamina monopolar cells (LMCs) spatially integrate visual information. We provide the first direct functional evidence for this hypothesis using intracellular recordings from type II LMCs in the hawkmoth Macroglossum stellatarum. We show that their spatial receptive fields broaden with decreasing light intensities, thus trading spatial resolution for higher sensitivity. These dynamic changes in LMC spatial properties can be explained by the density and lateral extent of their dendritic arborizations. Our results thus provide the first physiological evidence for a century-old hypothesis, directly correlating physiological response properties with distinctive dendritic morphology.

The roles of vision and antennal mechanoreception in hawkmoth flight control

Flying animals need continual sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here, we have investigated the visual-mechanosensory integration in the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston’s organs in their antennae to provide mechanosensory feedback on perturbations in body position. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Moreover, we did not observe compensatory interactions between antennal and visual feedback.

The roles of vision and antennal mechanoreception in hawkmoth flight control

Flying animals need constant sensory feedback about their body position and orientation for flight control. The visual system provides essential but slow feedback. In contrast, mechanosensory channels can provide feedback at much shorter timescales. How the contributions from these two senses are integrated remains an open question in most insect groups. In Diptera, fast mechanosensory feedback is provided by organs called halteres, and is crucial for the control of rapid flight manoeuvres, while vision controls manoeuvres in lower temporal frequency bands. Here we have investigated the visual-mechanosensory integration in an insect which lacks halteres: the hawkmoth Macroglossum stellatarum. They represent a large group of insects that use Johnston’s organs in their antennae to provide mechanosensory feedback on perturbations in body position. High-speed videos of freely-flying hawkmoths hovering at stationary or oscillating artificial flowers showed that positional fidelity during flight was reduced in flagella ablated animals, but was recovered after flagella re-attachment. Our experiments show that antennal mechanosensory feedback specifically mediates fast flight manoeuvres, but not slow ones. Differences in the latency of visual feedback (in different light intensities) affected all antennal conditions equally, suggesting there was no compensatory interaction between antennal and visual feedback under the tested conditions. These results establish the importance of antennal mechanosensors in providing rapid mechanosensory feedback for finer control of flight manoeuvres, acting in parallel to visual feedback.

Higher-order neural processing tunes motion neurons to visual ecology in three species of hawkmoths

To sample information optimally, sensory systems must adapt to the ecological demands of each animal species. These adaptations can occur peripherally, in the anatomical structures of sensory organs and their receptors; and centrally, as higher-order neural processing in the brain. While a rich body of investigations has focused on peripheral adaptations, our understanding is sparse when it comes to central mechanisms. We quantified how peripheral adaptations in the eyes, and central adaptations in the wide-field motion vision system, set the trade-off between resolution and sensitivity in three species of hawkmoths active at very different light levels: nocturnal Deilephila elpenor, crepuscular Manduca sexta , and diurnal Macroglossum stellatarum. Using optical measurements and physiological recordings from the photoreceptors and wide-field motion neurons in the lobula complex, we demonstrate that all three species use spatial and temporal summation to improve visual performance in dim light. The diurnal Macroglossum relies least on summation, but can only see at brighter intensities. Manduca, with large sensitive eyes, relies less on neural summation than the smaller eyed Deilephila , but both species attain similar visual performance at nocturnal light levels. Our results reveal how the visual systems of these three hawkmoth species are intimately matched to their visual ecologies.

Taubenschwänzchen, ein neuerdings häufiger Gast in unseren Gärten

Im warmen Sommer 2006 war das Taubenschwänzchen (Macroglossum stellatarum) häufig an verschiedenen Blüten zu beobachten. Es erinnert an einen Kolibri. Es wird ein Bild von einem Taubenschwänzchen, das an einer Folterpflanze (Araujia sericifera) gefangen war, gezeigt. Die Biologie des Taubenschwänzchens wird vorgestellt.