Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task-a celestial-cue-based visual compass and an optic-flow-based visual odometer-but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light-based compass neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy, we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically identified neurons suggested for each processing step. The resulting model circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e., a ground velocity that is not precisely aligned with body orientation) typical of bee flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings-suggesting a more basic function for central complex connectivity, from which path integration may have evolved.

Oriented behaviour is present in almost all animals, indicating that it is an ancient feature that has emerged from animal brains hundreds of millions of years ago. Although many complex navigation strategies have been described, each strategy can be broken down into a series of elementary navigational decisions. In each moment in time an animal has to compare its current heading with its desired direction and compensate for any mismatch by producing a steering response either to the right or to the left. Different from reflex driven movements, target directed navigation is not only initiated in response to sensory input, but also takes into account previous experience and motivational state. Once a series of elementary decisions are chained together to form one of many coherent navigation strategies, the animal can pursue a navigational target, e.g. a food source, a nest entrance, or a constant flight direction during migrations. Insects show a great variety of complex navigation behaviours and, owing to their small brains, the pursuit of the neural circuits controlling navigation has made substantial progress over the last years. A brain region as ancient as insects themselves, called the central complex, has emerged as the likely navigation centre of the brain. Research across many species has shown that the central complex contains the circuitry that might comprise the neural substrate of elementary navigational decisions. While this region is also involved in a wide range of other functions, we hypothesise in this review that its role in mediating the animal’s next move during target directed behaviour is its ancestral function, around which other functions have been layered over the course of evolution.

The nocturnal Bogong moth (Agrotis infusa) is an iconic and well-known Australian insect that is also a remarkable nocturnal navigator. Like the Monarch butterflies of North America, Bogong moths make a yearly migration over enormous distances, from southern Queensland, western and northwestern New South Wales (NSW) and western Victoria, to the alpine regions of NSW and Victoria. After emerging from their pupae in early spring, adult Bogong moths embark on a long nocturnal journey towards the Australian Alps, a journey that can take many days or even weeks and cover over 1000 km. Once in the Alps (from the end of September), Bogong moths seek out the shelter of selected and isolated high ridge-top caves and rock crevices (typically at elevations above 1800 m). In hundreds of thousands, moths line the interior walls of these cool alpine caves where they “hibernate” over the summer months (referred to as “estivation”). Towards the end of the summer (February and March), the same individuals that arrived months earlier leave the caves and begin their long return trip to their breeding grounds. Once there, moths mate, lay eggs and die. The moths that hatch in the following spring then repeat the migratory cycle afresh. Despite having had no previous experience of the migratory route, these moths find their way to the Alps and locate their estivation caves that are dotted along the high alpine ridges of southeastern Australia. How naïve moths manage this remarkable migratory feat still remains a mystery, although there are many potential sensory cues along the migratory route that moths might rely on during their journey, including visual, olfactory, mechanical and magnetic cues. Here we review our current knowledge of the Bogong moth, including its natural history, its ecology, its cultural importance to the Australian Aborigines and what we understand about the sensory basis of its long-distance nocturnal migration. From this analysis it becomes clear that the Bogong moth represents a new and very promising model organism for understanding the sensory basis of nocturnal migration in insects.

The lateral accessory lobes (LALs), paired structures that are homologous among all insect species, have been well studied for their role in pheromone tracking in silkmoths and phonotaxis in crickets, where their outputs have been shown to correlate with observed motor activity. Further studies have shown more generally that the LALs are crucial both for an insect's ability to steer correctly and for organising the outputs of the descending pathways towards the motor centres. In this context, we propose a framework by which the LALs may be generally involved in generating steering commands across a variety of insects and behaviours. Across different behaviours, we see that the LAL is involved in generating two kinds of steering: (1) search behaviours and (2) targeted steering driven by direct sensory information. Search behaviours are generated when the current behaviourally relevant cues are not available, and a well-described LAL subnetwork produces activity which increases sampling of the environment. We propose that, when behaviourally relevant cues are available, the LALs may integrate orientation information from several sensory modalities, thus leading to a collective output for steering driven by those cues. These steering commands are then sent to the motor centres, and an additional efference copy is sent back to the orientation-computing areas. In summary, we have taken known aspects of the neurophysiology and function of the insect LALs and generated a speculative framework that suggests how LALs might be involved in steering control for a variety of complex real-world behaviours in insects.

Every year, millions of Australian Bogong moths (Agrotis infusa) complete an astonishing journey: In Spring, they migrate over 1,000 km from their breeding grounds to the alpine regions of the Snowy Mountains, where they endure the hot summer in the cool climate of alpine caves. In autumn, the moths return to their breeding grounds, where they mate, lay eggs and die. These moths can use visual cues in combination with the geomagnetic field to guide their flight, but how these cues are processed and integrated into the brain to drive migratory behavior is unknown. To generate an access point for functional studies, we provide a detailed description of the Bogong moth's brain.Based on immunohistochemical stainings against synapsin and serotonin (5HT), we describe the overall layout as well as the fine structure of all major neuropils, including the regions that have previously been implicated in compass-based navigation. The resulting average brain atlas consists of 3D reconstructions of 25 separate neuropils, comprising the most detailed account of a moth brain to date. Our results show that the Bogong moth brain follows the typical lepidopteran ground pattern, with no major specializations that can be attributed to their spectacular migratory lifestyle. These findings suggest that migratory behavior does not require widespread modifications of brain structure, but might be achievable via small adjustments of neural circuitry in key brain areas. Locating these subtle changes will be a challenging task for the future, for which our study provides an essential anatomical framework. K E Y W O R D S central complex, insect brain, Lepidoptera, mushroom body, noctuid 1 | INTRODUCTION One of the central questions in neuroscience is how animal behaviors result from neural computations. From the sensory input that elicits abehavior to the motor circuits that execute it-the neural processing is complex and, as yet, we only understand small pieces of this multi-level puzzle. To delve deeper into this question, we need an animal model that shows a robust behavior and whose brain is accessible enough to