How does the insect central complex use mushroom body output for steering?

Abstract

Research on central brain areas in Drosophila and other insects is revealing the highly conserved neural circuitries in the central complex that are responsible for course control using visual, ideothetic and compass cues [1,2], and in the mushroom bodies that hold long-term visual and olfactory memories [3,4]. Interactions between these areas are likely to be particularly important for navigation in which long-term memories determine an insect's course. Many ants, for example, use long-term visual memories for guidance along routes between their nest and food sites. But the interactions remain a puzzle: both because there are no known direct connections between mushroom body and central complex, and because the output from the mushroom body, where the route memories are probably stored [5], may simply signal whether a sensory input is attractive or aversive [4]. Extrapolating from a recent behavioural finding [6], we propose one way that the long-term memories in the mushroom body may be transformed into central complex steering commands. This answer, if correct, may reconcile two apparently conflicting ways of thinking about route following - suggesting how steering along a route can use a feedback controller based on a few prominent features [7], while the route memories themselves are holistic memories of the entire panorama [5]. It also suggests how visual navigation is related to (and possibly evolved from) visual targeting and olfactory-based guidance.