Goal-directed navigation is thought to rely on the activity of head-direction cells, but how this activity guides moment-to-moment action remains poorly understood. Here we characterize how heading neurons in the Drosophila central complex guide moment-to-moment actions. We establish an innate, heading-neuron dependent, tethered navigational behavior where walking flies maintain a straight trajectory along a specific angular bearing for hundreds of body lengths. While flies perform this task, we use chemogenetics to transiently rotate their neural heading estimate and observe that the flies slow down and turn in a direction that aims to return the heading estimate to the angle it occupied prior to stimulation. These results support a working model in which the fly brain quantitatively compares an internal estimate of current heading with an internal goal heading and uses the sign and magnitude of the difference to determine which way to turn, how hard to turn, and how fast to walk forward.

Highlights d Ant odorant receptors show unique early expression and localization in pupae d Sensory neuron innervation is necessary for proper antennal lobe development d Sensory neuron ablation reveals latent antennal lobe structure in ants, but not flies d Insects with complex olfactory systems may employ a different developmental logic

One Sentence Summary:Flies compare an internal heading estimate with an internal goal angle to guide navigation. Abstract:While navigating their environment, many animals track their angular heading via the activity of heading-sensitive neurons. How internal heading estimates are used to guide navigational behavior, however, remains largely unclear in any species. We found that normal synaptic output from heading neurons in Drosophila is required for flies to stably maintain their trajectory along an arbitrary direction while navigating a simple virtual environment. We further found that if the heading estimate carried by these neurons is experimentally redirected by focal stimulation, the fly typically turns so as to rotate this internal heading estimate back towards the initial angle, while also slowing down until this correction has been made. These experiments argue that flies compare an internal heading estimate with an internal goal angle to guide navigational decisions, highlighting an important computation underlying how a spatial variable in the brain is translated into navigational action.. CC-BY-NC 4.0 International license It is made available under a was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint (which . http://dx.doi.org/10.1101/315796 doi: bioRxiv preprint first posted online May. 7, 2018; 3 Main Text:Many animals, from insects to mammals, keep track of their two-dimensional position (1, 2) and angular heading (3, 4) as they navigate through an environment. Neurons that track heading were first discovered in rodents (5), and more recently in insects (6, 7), including Drosophila (8). Whereas emphasis has been placed on understanding how the physiological properties of heading neurons are built (8)(9)(10)(11)(12)(13)(14), recent experiments have also begun to explore how animals use internal heading signals to guide navigational behavior (15). For example, destabilizing a rat's head-direction system induces longer, more circuitous routes to a home position (16), suggesting that head direction cell activity is generally important for oriented navigation. Furthermore, electrophysiological recordings in flying bats have revealed not only neurons that track the bat's head direction, but also neurons that track its goal direction--i.e., the angle of a known landing platform relative to the bat (17)--suggesting that a neural comparison between heading-and goal-direction guides the bat's navigational behavior. However, whether such a neural comparison takes place and how the output of any such comparison is translated into navigational action remains poorly understood in any species. Here, we describe a behavioral task in which Drosophila maintain a consistent walking direction for minutes in a simple virtual environment. We further provide correlational and perturbational evidence that flies accomplish this task by turning so as to maintain a neural heading estimate at an internal goal angle, w...

Neuronal signals relevant for spatial navigation have been described in many species[1-12], however, a circuit-level understanding of how such signals interact to guide behaviour is lacking. Here we characterize a neuronal circuit in theDrosophilacentral complex that compares internally generated estimates of the fly's heading and goal angles--both encoded in world-centred, or allocentric, coordinates--to generate a body-centred, or egocentric, steering signal. Past work has argued that the activity of EPG cells, or "compass neurons"[2], represents the fly's moment-to-moment angular orientation, or heading angle, during navigation[13]. An animal's moment-to-moment heading angle, however, is not always aligned with its goal angle, i.e., the allocentric direction in which it wishes to progress forward. We describe a second set of neurons in theDrosophilabrain, FC2 cells[14], with activity that correlates with the fly's goal angle. Furthermore, focal optogenetic activation of FC2 neurons induces flies to orient along experimenter-defined directions as they walk forward. EPG and FC2 cells connect monosynaptically to a third neuronal class, PFL3 cells[14,15]. We found that individual PFL3 cells show conjunctive, spike-rate tuning to both heading and goal angles during goal-directed navigation. Informed by the anatomy and physiology of these three cell classes, we develop a formal model for how this circuit can compare allocentric heading- and goal-angles to build an egocentric steering signal in the PFL3 output terminals. Quantitative analyses and optogenetic manipulations of PFL3 activity support the model. The biological circuit described here reveals how two, population-level, allocentric signals are compared in the brain to produce an egocentric output signal appropriate for the motor system.