Retinotopic Pathways Providing Motion- Selective Information to the Lobula From Peripheral Elementary Motion- Detecting Circuits JOHN K. DOUGLASS * AND NICHOLAS J. STRAUSFELD Division of Neurobiology, Arizona Research Laboratories, University of Arizona, Tucson, Arizona 85721 ABSTRACT Recordings from afferent channels from the medulla supplying deep neuropils of the fly’s optic lobes reveal different filter properties among the three classes of afferent neurons: transmedullary cells, T2 neurons, and Y cells. Whereas transmedullary cells respond to local flicker stimuli without discriminating these from directional or oriented motion, the T2 afferent neurons show clear motion orientation selectivity, which corresponds closely with a morphological bias in the orientation of their dendrites and could also be influenced by systems of local recurrent neurons in the medulla. A Y cell having a clearly defined terminal in the lobula, but having dendrite-like processes in the medulla and, possibly, the lobula plate, discriminates the direction of motion and its orientation. These results demonstrate unambiguously that the lobula receives information about motion and that the channels carrying it are distinct from those supplying wide-field motion-selective neurons in the lobula plate. Furthermore, recordings from a newly identified recurrent neuron linking the lobula back to the inner medulla demonstrate that the lobula discriminates nondirectional edge motion from flicker, thereby reflecting a property of this neuropil that is comparable with that of primary visual cortex in cats. The present findings support the proposal that elementary motion detecting circuits supply several parallel channels through the medulla, which seg- regate to, but are not shared by, the lobula and the lobula plate. The results are discussed in the context of other intracellular recordings from retinotopic neurons and with analogous findings from mammalian visual systems. J. Comp. Neurol. 457:326 –344, 2003. © 2003 Wiley-Liss, Inc. Indexing terms: insect vision; parallel pathways; motion processing; feedback; orientation selectivity; neural circuits Neuroanatomy and intracellular recordings have eluci- dated many features of neural circuitry underlying visual motion detection and processing by small-field retinotopic neurons in flies (Douglass and Strausfeld, 2001, and in press). Achromatic optomotor pathways begin with inputs from the R1– 6 photoreceptors to the pair of large lamina monopolar cells, L1 and L2, and various other lamina output neurons (Boschek, 1971). These afferent neurons terminate in the medulla, where they supply a system of retinotopic relays that supplies arrangements of direc- tional motion-sensitive neurons that eventually synapse onto wide-field tangential neurons of the lobula plate (Fig. 1A,C). Crucial players in this organization are the Tm1 small-field transmedullary cells that terminate at the den- drites of T5 direction-sensitive cells that extend from a superficial layer (the T5 layer) of a second deep visual neuropil, called the lobula (Fig. 1A). These retinotopically organized neurons together provide information about op- Grant sponsor: National Institutes of Health NCRR; Grant number: R01-RR08688; Grant sponsor: U.S. Navy; Grant number: N00014-97-1- 0970; Grant number: N68936-00-2-0002. *Correspondence to: John K. Douglass, Division of Neurobiology, Ari- zona Research Laboratories, 611 Gould-Simpson Bldg., University of Ari- zona, Tucson, AZ 85721. E-mail: jkd@neurobio.arizona.edu Received 29 May 2002; Revised 16 August 2002; Accepted 22 August 2002. DOI 10.1002/cne.10575 Published online the week of January 27, 2003 in Wiley InterScience (www.interscience.wiley.com). THE JOURNAL OF COMPARATIVE NEUROLOGY 457:326 –344 (2003) © 2003 WILEY-LISS, INC.