Chemical neuroanatomy of the fly's movement detection pathway

Abstract

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. J. Comp. Neurol. 468:6–23, 2004.