Parallel vector memories in the brain of a bee as foundation for flexible navigation.

Insects rely on path integration (vector-based navigation) and landmark guidance to perform sophisticated navigational feats, rivaling those seen in mammals. Bees in particular exhibit complex navigation behaviors including creating optimal routes and novel shortcuts between locations, an ability historically indicative of the presence of a cognitive map. A mammalian cognitive map has been widely accepted. However, in insects, the existence of a centralized cognitive map is highly contentious. Using a controlled laboratory assay that condenses foraging behaviors to short distances in walking bumblebees, we reveal that vectors learned during path integration can be transferred to long-term memory, that multiple such vectors can be stored in parallel, and that these vectors can be recalled at a familiar location and used for homeward navigation. These findings demonstrate that bees meet the two fundamental requirements of a vector-based analog of a decentralized cognitive map: Home vectors need to be stored in long-term memory and need to be recalled from remembered locations. Thus, our data demonstrate that bees possess the foundational elements for a vector-based map. By utilizing this relatively simple strategy for spatial organization, insects may achieve high-level navigation behaviors seen in vertebrates with the limited number of neurons in their brains, circumventing the computational requirements associated with the cognitive maps of mammals.

Vector navigation in walking bumblebees.

Path integration is a computational strategy that allows an animal to maintain an internal estimate of its position relative to a point of origin. Many species use path integration to navigate back to specific locations, typically their homes, after lengthy and convoluted excursions. Hymenopteran insects are impressive path integrators, directly returning to their hives after hundreds of meters of outward travel. Recent neurobiological insights have established hypotheses for how path integration vectors could be encoded in the brains of bees, but clear ways to test these hypotheses in the laboratory are currently unavailable. Here, we report that the bumblebee, Bombus terrestris, uses path integration while walking over short distances in an indoor arena. They estimate accurate vector distances after displacement and orient by artificial celestial cues. Walking bumblebees also exhibited systematic search patterns when home vectors failed to lead them accurately back to the nest, closely resembling searches performed by other species under natural conditions. We thus provide a robust experimental system to test navigation behavior in the laboratory that reflects most aspects of natural path integration. Importantly, we established this assay in an animal that is both readily available and resilient to invasive manipulations, as we demonstrate with the retention of the homing behavior post-anesthesia and surgery. In the future, our behavioral assay can therefore be combined with current electrophysiological techniques, opening a path toward directly probing the neural basis of the sophisticated vector navigation abilities of bees.

A projectome of the bumblebee central complex.

Insects have evolved diverse and remarkable strategies for navigating in various ecologies all over the world. Regardless of species, insects share the presence of a group of morphologically conserved neuropils known collectively as the central complex (CX). The CX is a navigational center, involved in sensory integration and coordinated motor activity. Despite the fact that our understanding of navigational behavior comes predominantly from ants and bees, most of what we know about the underlying neural circuitry of such behavior comes from work in fruit flies. Here, we aim to close this gap, by providing the first comprehensive map of all major columnar neurons and their projection patterns in the CX of a bee. We find numerous components of the circuit that appear to be highly conserved between the fly and the bee, but also highlight several key differences which are likely to have important functional ramifications.

Bumblebees forage widely for pollen and nectar from flowers, sometimes travelling kilometers away from their nest, but they can somehow always find their way home in a nearly straight line. These insects have been known to return to their nest from new locations almost 10 kilometers away. This homing ability is a complex neurological feat and requires the brain to combine several processes, including observing the external world, controlling bodily movements and drawing on memory. While the navigational behavior of bees has been well-studied, the neuronal circuitry behind it has not. Unfortunately, most of what is known about insects' brain activity comes from studies in species such as locusts or fruit flies. In these species, a region of the brain known as the central complex has been shown to have an essential role in homing behaviors. However, it is unknown how similar the central complex of bumblebees might be to fruit flies' or locusts', or how these differences may affect navigational abilities. Sayre et al. obtained images of thin slices of the bumblebee central complex using a technique called block-face electron microscopy, which produces high-resolution image volumes. These images were used to obtain a three-dimensional map of over 1300 neurons. This cellular atlas showed that key aspects of the central complex are nearly identical between flies and bumblebees, including the internal compass that monitors what direction the insect is travelling in. However, hundreds of millions of years of independent evolution have resulted in some differences. These were found in neurons possibly involved in forming memories of the directions and lengths of travelled paths, and in the circuits that use such vector memories to steer the insects towards their targets. Sayre et al. propose that these changes underlie bees' impressive ability to navigate. These results help explain how the structure of insects' brains can determine homing abilities. The insights gained could be used to develop efficient autonomous navigation systems, which are challenging to build and require a lot more processing power than offered by a small part of an insect brain.