Converting an allocentric goal into an egocentric steering signal

Abstract

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.

A neural circuit architecture for rapid behavioral flexibility in goal-directed navigation

“…Recent studies carried out in parallel to ours have highlighted the role of PFL3 neurons [84,85] and PFL2 neurons [85] in walking flies performing menotaxis [84,85]. Although it is not yet known how these neuron types function during learned behavior in flight, the experimental results in these studies are largely consistent with the model we propose.…”

A collicular map for touch-guided tongue control

“…In primates, sensorimotor cortical pathways mediate touch- and visually-guided reaching and grasping 2,43,46 , and SC has been implicated in visual, auditory, and somatosensory-guided orienting 20,45,49 . Yet spinalized frogs and Drosophila exhibit body position-dependent responses to stimuli 44,50,51 , showing that diverse circuit architectures can implement coordinate transformations important for sensory feedback-based aiming.…”

Monarch butterflies memorize the spatial location of a food source

“…In addition to the mushroom bodies, the central complex also plays a major role in spatial learning [86,87]. As the insect's internal compass, the central complex houses neurons encoding the current heading direction [58,[88][89][90], cells that control steering behaviour [79,91,92], and more recently described goal direction neurons [62,93]. Goal direction neurons may receive memorized information from the mushroom bodies.…”