Disinhibition of a recurrent attractor gates a persistent goal signal for navigation

Recurrent attractor networks are widely thought to form the basis of working memory1-3, but how stable attractor activity can be rapidly switched on and off is unclear4-7. Here we investigate how stability and rapid switching can be combined in a discrete recurrent circuit of the fly navigation center8. h{Delta}K and PFG neurons are recurrently connected in a ring structure. Using in vivo imaging, we find that these two populations exhibit shared persistent bump activity that turns on with odor and terminates at the end of a goal-directed upwind run. Using whole-cell recordings, we show that persistence in h{Delta}K depends on recurrent signalling, and that h{Delta}K receives slow recurrent excitation and fast inhibition from its synaptic partners. Computational modeling reveals that this combination of slow excitation with fast inhibition yields persistent attractor dynamics over a range of excitation and inhibition strengths. Next we examine the mechanisms that allow this activity bump to be rapidly turned on and off. We find that while both populations show positionally stable bump activity during goal-directed runs, during turns and rest the PFG bump tracks heading while h{Delta}K is supressed. We can reproduce these differential dynamics in our model by using inhibition to dynamically uncouple activity in h{Delta}K from PFG. When h{Delta}K is inhibited, PFG neurons follow their inputs from the compass system; when h{Delta}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{Delta}K increase during turns and are suppressed during odor input and goal-directed upwind runs. Our work reveals how disinhibition can serve as a gate to rapidly write an ongoing measurement to a recurrent memory circuit.