Chemical Neuroanatomy of the Fly's Movement Detection Pathway

In Diptera, subsets of small retinotopic neurons provide a discrete channel from achromatic photoreceptors to large motion-sensitive neurons in the lobula complex. This pathway is distinguished by specific affinities of its neurons to antisera raised against glutamate, aspartate, γ-aminobutyric acid (GABA), choline acetyltransferase (ChAT), and a N-methyl-D-aspartate type 1 receptor protein (NMDAR1). Large type 2 monopolar cells (L2) and type 1 amacrine cells, which in the external plexiform layer are postsynaptic to the achromatic photoreceptors R1-R6, express glutamate immunoreactivity as do directionally selective motion-sensitive tangential neurons of the lobula plate. L2 monopolar cells ending in the medulla are accompanied by terminals of a second efferent neuron T1, the dendrites of which match NMDAR1-immunoreactive profiles in the lamina. L2 and T1 endings visit ChAT and GABA-immunoreactive relays (transmedullary neurons) that terminate from the medulla in a special layer of the lobula containing the dendrites of directionally selective retinotopic T5 cells. T5 cells supply directionally selective wide-field neurons in the lobula plate. The present results suggest a circuit in which initial motion detection relies on interactions among amacrines and T1, and the subsequent convergence of T1 and L2 at transmedullary cell dendrites. Convergence of ChAT-immunoreactive and GABA-immunoreactive transmedullary neurons at T5 dendrites in the lobula, and the presence there of local GABA-immunoreactive interneurons, are suggested to provide excitatory and inhibitory elements for the computation of motion direction. A comparable immunocytological organization of aspartate- and glutamate-immunoreactive neurons in honeybees and cockroaches further suggests that neural arrangements providing directional motion vision in flies may have early evolutionary origins.