Based on comparative anatomical studies and electrophysiological
experiments, we have identified a conserved subset of neurons in the
lamina, medulla, and lobula of dipterous insects that are involved in
retinotopic visual motion direction selectivity. Working from the
photoreceptors inward, this neuronal subset includes lamina amacrine
(α) cells, lamina monopolar (L2) cells, the basket T-cell (T1 or
β), the transmedullary cell Tm1, and the T5 bushy T-cell. Two
GABA-immunoreactive neurons, the transmedullary cell Tm9 and a local
interneuron at the level of T5 dendrites, are also implicated in the
motion computation. We suggest that these neurons comprise the
small-field elementary motion detector circuits the outputs of which
are integrated by wide-field lobula plate tangential cells. We show
that a computational model based on the available data about these
neurons is consistent with existing models of biological elementary
motion detection, and present a comparable version of the
Hassenstein-Reichardt (HR) correlation model. Further, by using the
model to synthesize a generic tangential cell, we show that it can
account for the responses of lobula plate tangential cells to a wide
range of transient stimuli, including responses which cannot be
predicted using the HR model. This computational model of elementary
motion detection is the first which derives specifically from the
functional organization of a subset of retinotopic neurons supplying
the lobula plate. A key prediction of this model is that elementary
motion detector circuits respond quite differently to small-field
transient stimulation than do spatially integrated motion processing
neurons as observed in the lobula plate. In addition, this model
suggests that the retinotopic motion information provided to wide-field
motion-sensitive cells in the lobula is derived from a less refined
stage of processing than motion inputs to the lobula plate.