A computational model for angular velocity integration in a locust heading circuit

Abstract

Accurate navigation often requires the maintenance of a robust internal estimate of heading relative to external surroundings. We propose a novel model for angular velocity integration to update the representation of heading in the central complex of the desert locust. In contrast to similar models proposed for the fruit fly, this circuit model uses a single 360{degrees} heading direction representation and is updated by neuromodulatory angular velocity inputs. Our computational model was implemented using steady-state firing rate neurons with dynamical synapses. The circuit connectivity was constrained by biological data and remaining degrees of freedom were optimised with a machine learning approach to yield physiologically plausible neuron activities. We demonstrate that the integration of heading and angular velocity in this circuit is robust to noise. The heading signal can be effectively used as input to an existing insect goal-directed steering circuit, adapted for outbound locomotion in a steady direction that resembles locust migration. Our study supports the possibility that similar computations for orientation may be implemented differently in the neural hardware of the fruit fly and the locust. Author summaryIn both fruit flies and locusts, a specific brain region has been observed to have an activity pattern that resembles a compass, with an activity peak moving across an array of neurons as the animal rotates through 360 degrees. However, some apparent differences in the properties of this pattern between the two species suggest there may be differences in how this internal compass is implemented. Here we focus on the locust brain, building a computational model that is based on observed neural connections and using machine learning to tune the system. Turning by the simulated locust provides modulatory input to the neural circuit that keeps activity in the array aligned to its heading direction. We simulate a migrating locust that tries to keep the same heading despite perturbances and show this circuit can steer it back on course. Our model differs from existing models of the fruit fly compass, showing how similar computations could have different implementations in different species. O_TBL View this table: org.highwire.dtl.DTLVardef@109a8b3org.highwire.dtl.DTLVardef@12298eborg.highwire.dtl.DTLVardef@65a654org.highwire.dtl.DTLVardef@18ae048org.highwire.dtl.DTLVardef@8ace20_HPS_FORMAT_FIGEXP M_TBL O_FLOATNOTable 1.C_FLOATNO O_TABLECAPTIONAbbreviations for neuron types and brain regions in the desert locust (Schistocerca gregaria) and homologues in the fruit fly (Drosophila melanogaster). C_TABLECAPTION C_TBL