To generate an initial framework for this project we first developed a biologically constrained computational model of the CX (Stone et al., 2017). This circuit uses identified CX neurons to perform path integration, a navigation strategy used by many animals, including mammals. Importantly, whereas designed for path integration, the underlying computations performed by this circuit can drive any navigational decision. To illuminate the underlying biological circuits in detail, we developed a novel approach to extract connectomics information from large insects. This work first yielded the projectome of the bumblebee CX (Sayre et al., 2021) - to date the most detailed published account of the CX neural composition of any insect besides the fly Drosophila. While all core cell types were highly conserved, we found key differences between bees and flies, which, due to tight structure function links, support different computations (Pisokas et al, 2020). We also discovered neurons in the bee CX without counterpart in the fly, forming circuits suited to encode navigational goals. Synaptic level connectome analysis has since highlighting the conserved 400 million year old core of the CX decision making circuit and highlighted species-specific differences responsible to specific behavioral abilities (2 papers in prep.). To attach relevance to these anatomical data, we used electrophysiology to reveal the sensory pathways relaying optic flow signals to the CX path integrator (Honkanen et al, under review). We identified a neural network that reshapes simple motion signals from the visual periphery into responses encoding the bee’s movement through space. We also revealed that the CX in the migratory Bogong moth encodes the orientation of the Milky Way (Adden et al, in prep.) - distinctly different information than that encoded by corresponding bee neurons. This showed that despite the overall conservation of the CX, sensory inputs depend on a species’ ecology, a finding supported by our connectomics data.
The second part of our work aimed at illuminating goal encoding during path integration. Using a new behavioral paradigm, we demonstrated that bumblebees use path integration while walking over distances of less than two meters instead of hundreds of meters during flight and that their vector memories (goals) were highly resilient to disturbances (Patel et al., 2022). Importantly, the method can be expanded to study more complex forms of vector navigation, including potential cognitive maps. To make these behaviors and vector memories accessible to electrophysiology, we translated the paradigm from freely walking bees into a virtual reality setup, enabling multi-electrode recordings during behavior.
Third, on the output side of the CX, while connectomics data revealed that the computations underlying the initiation of steering commands are likely adapted to the movement strategies of a species (Sayre et al 2021), a model of the premotor command center downstream of the CX predicting a single steering pathway shared between many behaviors (Adden et al, 2022). Combining results from all stages of the project, we have constructed an overarching computational CX model that covers all processing steps from sensory input to motor output (Goulard et al., in prep.). This model provides the detailed computational framework that was the main goal of the project. Finally, besides generating new methods and results, we also created a transparent, open science tool to deposit, manage and share all data resulting from this project: the InsectBrainDatabase (www.insectbraindb.org; Heinze et al, 2021).
