Direct observation of ON and OFF pathways in the Drosophila visual system.
Visual motion perception is critical to many animal behaviors, and flies have emerged as a powerful model system for exploring this fundamental neural computation. Although numerous studies have suggested that fly motion vision is governed by a simple neural circuit [1-3], the implementation of this circuit has remained mysterious for decades. Connectomics and neurogenetics have produced a surge in recent progress, and several studies have shown selectivity for light increments (ON) or decrements (OFF) in key elements associated with this circuit [4-7]. However, related studies have reached disparate conclusions about where this selectivity emerges and whether it plays a major role in motion vision [8-13]. To address these questions, we examined activity in the neuropil thought to be responsible for visual motion detection, the medulla, of Drosophila melanogaster in response to a range of visual stimuli using two-photon calcium imaging. We confirmed that the input neurons of the medulla, the LMCs, are not responsible for light-on and light-off selectivity. We then examined the pan-neural response of medulla neurons and found prominent selectivity for light-on and light-off in layers of the medulla associated with two anatomically derived pathways (L1/L2 associated) [14, 15]. We next examined the activity of prominent interneurons within each pathway (Mi1 and Tm1) and found that these neurons have corresponding selectivity for light-on or light-off. These results provide direct evidence that motion is computed in parallel light-on and light-off pathways, demonstrate that this selectivity emerges in neurons immediately downstream of the LMCs, and specify where crucial elements of motion computation occur.
Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147-2408, USA.
James A
JA
Strother
Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147-2408, USA.
Aljoscha
A
Nern
Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147-2408, USA. Electronic address: reiserm@janelia.hhmi.org.
Michael B
MB
Reiser
D000818:Animals; D001522:Behavior, Animal; D002118:Calcium; D029721:Drosophila Proteins / Q000378:metabolism; D004331:Drosophila melanogaster / Q000502:physiology*; D034882:Lamins; D008954:Models, Biological; D009039:Motion Perception / Q000502:physiology; D009687:Nuclear Proteins / Q000378:metabolism; D010775:Photic Stimulation; D017956:Photoreceptor Cells, Invertebrate / Q000502:physiology*; D025341:Principal Component Analysis; D014335:Tropomyosin / Q000378:metabolism; D014785:Vision, Ocular / Q000502:physiology*; D014795:Visual Pathways / Q000502:physiology*
D029721:Drosophila Proteins; C440328:Lam protein, Drosophila; D034882:Lamins; D009687:Nuclear Proteins; C490776:Tm1 protein, Drosophila; D014335:Tropomyosin; D002118:Calcium