Parallel spatial channels in the insect visual system

• Applicant: Dr. Anna Stöckl
• Subject Area: Cognitive, Systems and Behavioural Neurobiology ; Sensory and Behavioural Biology ; Molecular Biology and Physiology of Neurons and Glial Cells
• Term: from 2019 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 419991121

• Final Report Year: 2024

Final Report Abstract

Sensory systems process highly multidimensional information. To extract relevant features for specific tasks, they process the complex sensory input in parallel channels. The visual system acquires information about the natural world with a particularly high dimensionality. This makes it well suited to control a wide range of behaviours in humans and other animals. But the breadth of information also increases the need for sensory filtering and for categorizing visual signals at an early stage, to process the complex input with limited neural capacities. An important example for this are parallel spatial channels in the visual system. They can help resolve the general trade-off between spatial acuity and sensitivity in a task-specific manner. Behavioural and physiological evidence for this strategy can be found in primates, including humans. Their motion vision pathways sacrifice spatial resolution for high contrast sensitivity, while pattern detection pathways retain high spatial acuity, at the cost of contrast sensitivity. In insects, however, we do not know whether such parallel spatial filters exist. In this project, I planned to close this knowledge gap by investigating whether lamina monopolar cells form parallel spatial channels in insects, using the hummingbird hawkmoths as a model species. We began this project with a detailed characterisation of the morphology and neural connectivity of lamina monopolar cells of the hummingbird hawkmoth, and to our surprise found that previous characterisations were inaccurate. We therefore created a new classification of these cell types across different hawkmoth species, using serial block-face scanning electron microscopy, and established homology to the neuron types in fruit flies. This allowed us to extend the relevance of our findings to well-described neural circuits, particularly for wide-field motion processing underlying flight control via optic flow. We investigated the spatial tuning of translational optic-flow based flight responses in the hummingbird hawkmoth, as well as the allometric relationship between eye size, body size and spatial acuity. To our surprise, we found that flight guidance in our experimental paradigm was not limited by their spatial acuity, but by their temporal acuity. Investigating flight guidance in the hummingbird hawkmoth further, we found a novel flight control strategy, which helps the animals avoid flying under canopies. We found that this pathway operated in parallel with the “canonical” optic-flow-based flight control. The two pathways partitioned the visual field according to the prevalence of their respective input stimuli in natural visual habitats. Finally, we developed a computational model to describe visual information in natural scenes through eyes of range of animals, including hawkmoths. In summary, this project increased our understanding of insect vision, by providing new insights into early visual processing in hawkmoths, and establishing homology with other insects, particularly dipteran flies. Furthermore, it revealed new strategies for insect flight guidance, and provides a framework for linking insect visual processing to the information in natural visual scenes using computational modelling.

Publications

• Natural image statistics in the dorsal and ventral visual field match a switch in flight behaviour of a hawkmoth. Current Biology, 31(6), R280-R281.
  Bigge, Ronja; Pfefferle, Maximilian; Pfeiffer, Keram & Stöckl, Anna
  
• Spatial tuning of translational optic flow responses in hawkmoths of varying body size. J Comp Physiol A. 208:279-296. Source Data Repository
  Grittner, R., Baird, E. & Stöckl, A.
  
• Spatial tuning of translational optic flow responses in hawkmoths of varying body size. Journal of Comparative Physiology A, 208(2), 279-296.
  Grittner, Rebecca; Baird, Emily & Stöckl, Anna
  
• Allometric scaling of a superposition eye optimises sensitivity and acuity in large and small hawkmoths. Proc Biol Sci. B. 289:20220758. Source Data Repository
  Stöckl, A., Grittner, R., Taylor, G., Rau, C., Bodey, AJ, Kelber, A. & Baird, E.
  
• Allometric scaling of a superposition eye optimizes sensitivity and acuity in large and small hawkmoths. Proceedings of the Royal Society B: Biological Sciences, 289.
  Stöckl, Anna; Grittner, Rebecca; Taylor, Gavin; Rau, Christoph; Bodey, Andrew J.; Kelber, Almut & Baird, Emily
  
• Night skies through animals’ eyes—Quantifying night-time visual scenes and light pollution as viewed by animals. Frontiers in Cellular Neuroscience, 16.
  Stöckl, Anna Lisa & Foster, James Jonathan
  
• Source data: Night skies through animals’ eyes – quantifying night-time visual scenes and light pollution as viewed by animals.. figshare. Source Data Repository
  Stöckl, A. & Foster J.
  
• Integration of parallel pathways for flight control reflects prevalence and relevance of natural visual cues. Code Repository
  Bigge, R., Grittner, R. & Stöckl, A.
  
• Integration of parallel pathways for flight control in a hawkmoth reflects prevalence and relevance of natural visual cues. eLife Sciences Publications, Ltd.
  Bigge, Ronja; Grittner, Rebecca & Stöckl, Anna