Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly

Abstract

In dipteran insects, the lobula plate neuropil provides a major efferent supply to the premotor descending neurons that control stabilized flight. The lobula plate itself is supplied by two major parallel retinotopic pathways from the medulla: small-field, magnocellular afferents that are implicated in achromatic motion processing and Y cells that connect the medulla with both the lobula plate and the lobula. A third pathway from the medulla involves transmedullary (Tm) neurons, which provide inputs to palisades of small-field neurons in the lobula. Although, in their passage to the brain, many output neurons from the lobula plate are separated physically from their counterparts in the lobula, there is an additional class of lobula complex output neurons. This group is composed of retinotopic lobula plate-lobula (LPL) and lobula-lobula plate (LLP) cells, each of which has dendrites in both the lobula and the lobula plate. The present account describes the anatomy and physiology of exemplars of LPL and LLP neurons, a wide-field tangential neuron that is intrinsic to the lobula complex, and representatives of the Tm- and Y-cell pathways. We demonstrate novel features of the lobula plate, which previously has been known as a motion-collating neuropil, and now also can be recognized as supporting direction- or nondirection-specific responses to local motion, encoding of contrast frequency, and processing of local structural features of the visual panorama.