A structured representation of odors in the fly mushroom body

The mushroom body (MB) is a third-order olfactory area in the insect brain required for adaptive olfactory behaviors, such as learning odor associations, and is loosely analogous to olfactory cortex in mammals. In the vinegar fly Drosophila melanogaster, the chemical selectivity of each of the ~2200 principal neurons of the MB, called Kenyon cells (KCs), is determined by the pooling of odor information from a small random subset of the ~50 channels of olfactory input. The random integration of olfactory inputs in KCs contrasts with connectivity rules in other third-order olfactory areas, such as the lateral horn, where feature selectivity is determined by the invariant integration of specific combinations of olfactory inputs. The distinct connectivity statistics in different third-order olfactory areas has led to the idea that odor representations in the MB are “unstructured” and individualized in every brain, and must acquire meaning through learning, whereas invariant, chemotopic representations in the lateral horn support innate behaviors. We present a method using genetically enabled, in vivo two-photon functional imaging to measure near complete population representations of odors in KCs. We find that the relationship among neural representations of odors in the MB is invariant across individual brains. Furthermore, we apply a simple computational model of MB odor responses to illustrate that sparse, random connectivity can result in invariant relationships among odor representations, the structure of which is at least partially dictated by the correlational structure of the peripheral olfactory code. However, the experimentally observed structure of MB representational space deviates significantly from the predictions of the model for some regions of odor space. We discuss possible reasons for this discrepancy and future experimental directions to distinguish among these possibilities.