A split attractor design for rapidly writing a navigational goal

Recurrent attractor networks are widely thought to form the basis of working memory1–3, but how they can be rapidly switched on and off is unclear4–7. Here we investigate stability and switching in a recurrent circuit of the fly navigation centre8. h∆K and PFG neurons are recurrently connected in a ring structure and exhibit shared persistent bump activity that turns on with odour and terminates at the end of a goal-directed run. Using whole-cell recordings, we show that persistence in h∆K depends on recurrence, and that h∆K receives slow recurrent excitation and fast inhibition from its synaptic partners. Computational modelling reveals that these synaptic dynamics yield persistent attractor dynamics over a range of synaptic strengths. Next we examine the mechanisms of rapid switching. We find that whereas both populations show similar activity during runs, they become decoupled during turns and rest. We can reproduce these differential dynamics in our model by using inhibition to dynamically uncouple activity in h∆K from PFG. When h∆K is inhibited, PFG neurons follow their inputs from the compass system; when h∆K is disinhibited, recurrent interactions lock this input into place, forming a heading memory. Consistent with this model, we find that inhibitory inputs onto h∆K increase during turns and are suppressed during odour and goal-directed runs. Our work reveals how disinhibition can serve as a gate to rapidly write an ongoing measurement to a recurrent circuit. The recurrent h∆K–PFG neural circuit generates persistent heading memories through slow excitation, fast inhibition and a disinhibitory gate, where disinhibition controls the functional coupling of the network to rapidly transition between measurement and memory.