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• W2023874864 abstract "•Pan-neuronal imaging reveals distinct ON and OFF pathways in the fly medulla•Inputs to each pathway are not selective for light-on or light-off•However, downstream interneurons in each pathway are highly selective•Temporal filtering occurs between the input and output layers of the medulla 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 [1Hassenstein V.B. Reichardt W. Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus.Z. Naturforsch. B. 1956; 11: 513-524Google Scholar, 2Egelhaaf M. Borst A. Transient and steady-state response properties of movement detectors.J. Opt. Soc. Am. A. 1989; 6: 116-127Crossref PubMed Scopus (152) Google Scholar, 3Götz K.G. Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila [Optomoter studies of the visual system of several eye mutants of the fruit fly Drosophila].Kybernetik. 1964; 2: 77-92Crossref PubMed Scopus (318) Google Scholar], 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 [4Joesch M. Schnell B. Raghu S.V. Reiff D.F. Borst A. ON and OFF pathways in Drosophila motion vision.Nature. 2010; 468: 300-304Crossref PubMed Scopus (228) Google Scholar, 5Freifeld L. Clark D.A. Schnitzer M.J. Horowitz M.A. Clandinin T.R. GABAergic lateral interactions tune the early stages of visual processing in Drosophila.Neuron. 2013; 78: 1075-1089Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar, 6Joesch M. Weber F. Eichner H. Borst A. Functional specialization of parallel motion detection circuits in the fly.J. Neurosci. 2013; 33: 902-905Crossref PubMed Scopus (51) Google Scholar, 7Maisak M.S. Haag J. Ammer G. Serbe E. Meier M. Leonhardt A. Schilling T. Bahl A. Rubin G.M. Nern A. et al.A directional tuning map of Drosophila elementary motion detectors.Nature. 2013; 500: 212-216Crossref PubMed Scopus (221) Google Scholar]. However, related studies have reached disparate conclusions about where this selectivity emerges and whether it plays a major role in motion vision [8Clark D.A. Bursztyn L. Horowitz M.A. Schnitzer M.J. Clandinin T.R. Defining the computational structure of the motion detector in Drosophila.Neuron. 2011; 70: 1165-1177Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar, 9Egelhaaf M. Borst A. Are there separate ON and OFF channels in fly motion vision?.Vis. Neurosci. 1992; 8: 151-164Crossref PubMed Scopus (48) Google Scholar, 10Reiff D.F. Plett J. Mank M. Griesbeck O. Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila.Nat. Neurosci. 2010; 13: 973-978Crossref PubMed Scopus (80) Google Scholar, 11Rister J. Pauls D. Schnell B. Ting C.Y. Lee C.H. Sinakevitch I. Morante J. Strausfeld N.J. Ito K. Heisenberg M. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster.Neuron. 2007; 56: 155-170Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar, 12Silies M. Gohl D.M. Fisher Y.E. Freifeld L. Clark D.A. Clandinin T.R. Modular use of peripheral input channels tunes motion-detecting circuitry.Neuron. 2013; 79: 111-127Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar, 13Tuthill J.C. Nern A. Holtz S.L. Rubin G.M. Reiser M.B. Contributions of the 12 neuron classes in the fly lamina to motion vision.Neuron. 2013; 79: 128-140Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar]. 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) [14Bausenwein B. Dittrich A.P. Fischbach K.F. The optic lobe of Drosophila melanogaster. II. Sorting of retinotopic pathways in the medulla.Cell Tissue Res. 1992; 267: 17-28Crossref PubMed Scopus (107) Google Scholar, 15Takemura S.Y. Bharioke A. Lu Z. Nern A. Vitaladevuni S. Rivlin P.K. Katz W.T. Olbris D.J. Plaza S.M. Winston P. et al.A visual motion detection circuit suggested by Drosophila connectomics.Nature. 2013; 500: 175-181Crossref PubMed Scopus (446) Google Scholar]. 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. 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 [1Hassenstein V.B. Reichardt W. Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus.Z. Naturforsch. B. 1956; 11: 513-524Google Scholar, 2Egelhaaf M. Borst A. Transient and steady-state response properties of movement detectors.J. Opt. Soc. Am. A. 1989; 6: 116-127Crossref PubMed Scopus (152) Google Scholar, 3Götz K.G. Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila [Optomoter studies of the visual system of several eye mutants of the fruit fly Drosophila].Kybernetik. 1964; 2: 77-92Crossref PubMed Scopus (318) Google Scholar], 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 [4Joesch M. Schnell B. Raghu S.V. Reiff D.F. Borst A. ON and OFF pathways in Drosophila motion vision.Nature. 2010; 468: 300-304Crossref PubMed Scopus (228) Google Scholar, 5Freifeld L. Clark D.A. Schnitzer M.J. Horowitz M.A. Clandinin T.R. GABAergic lateral interactions tune the early stages of visual processing in Drosophila.Neuron. 2013; 78: 1075-1089Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar, 6Joesch M. Weber F. Eichner H. Borst A. Functional specialization of parallel motion detection circuits in the fly.J. Neurosci. 2013; 33: 902-905Crossref PubMed Scopus (51) Google Scholar, 7Maisak M.S. Haag J. Ammer G. Serbe E. Meier M. Leonhardt A. Schilling T. Bahl A. Rubin G.M. Nern A. et al.A directional tuning map of Drosophila elementary motion detectors.Nature. 2013; 500: 212-216Crossref PubMed Scopus (221) Google Scholar]. However, related studies have reached disparate conclusions about where this selectivity emerges and whether it plays a major role in motion vision [8Clark D.A. Bursztyn L. Horowitz M.A. Schnitzer M.J. Clandinin T.R. Defining the computational structure of the motion detector in Drosophila.Neuron. 2011; 70: 1165-1177Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar, 9Egelhaaf M. Borst A. Are there separate ON and OFF channels in fly motion vision?.Vis. Neurosci. 1992; 8: 151-164Crossref PubMed Scopus (48) Google Scholar, 10Reiff D.F. Plett J. Mank M. Griesbeck O. Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila.Nat. Neurosci. 2010; 13: 973-978Crossref PubMed Scopus (80) Google Scholar, 11Rister J. Pauls D. Schnell B. Ting C.Y. Lee C.H. Sinakevitch I. Morante J. Strausfeld N.J. Ito K. Heisenberg M. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster.Neuron. 2007; 56: 155-170Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar, 12Silies M. Gohl D.M. Fisher Y.E. Freifeld L. Clark D.A. Clandinin T.R. Modular use of peripheral input channels tunes motion-detecting circuitry.Neuron. 2013; 79: 111-127Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar, 13Tuthill J.C. Nern A. Holtz S.L. Rubin G.M. Reiser M.B. Contributions of the 12 neuron classes in the fly lamina to motion vision.Neuron. 2013; 79: 128-140Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar]. 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) [14Bausenwein B. Dittrich A.P. Fischbach K.F. The optic lobe of Drosophila melanogaster. II. Sorting of retinotopic pathways in the medulla.Cell Tissue Res. 1992; 267: 17-28Crossref PubMed Scopus (107) Google Scholar, 15Takemura S.Y. Bharioke A. Lu Z. Nern A. Vitaladevuni S. Rivlin P.K. Katz W.T. Olbris D.J. Plaza S.M. Winston P. et al.A visual motion detection circuit suggested by Drosophila connectomics.Nature. 2013; 500: 175-181Crossref PubMed Scopus (446) Google Scholar]. 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. We used two-photon imaging of a fluorescent calcium indicator to examine the activity of neurons within the fly visual system (Figure 1A). Flies have proven to be an excellent system for studying visual processing [1Hassenstein V.B. Reichardt W. Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus.Z. Naturforsch. B. 1956; 11: 513-524Google Scholar, 2Egelhaaf M. Borst A. Transient and steady-state response properties of movement detectors.J. Opt. Soc. Am. A. 1989; 6: 116-127Crossref PubMed Scopus (152) Google Scholar, 3Götz K.G. Optomotorische Untersuchung des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila [Optomoter studies of the visual system of several eye mutants of the fruit fly Drosophila].Kybernetik. 1964; 2: 77-92Crossref PubMed Scopus (318) Google Scholar, 16Järvilehto M. Zettler F. Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina.Z. Zellforsch. Mikrosk. Anat. 1973; 136: 291-306Crossref PubMed Scopus (62) Google Scholar, 17Laughlin S.B. Hardie R.C. Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly.J. Comp. Physiol. 1978; 128: 319-340Crossref Scopus (245) Google Scholar, 18Fischbach K.-F. Dittrich A. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure.Cell Tissue Res. 1989; 258: 441-475Crossref Scopus (553) Google Scholar], and broad conservation in the neuroanatomy of the visual system across a diversity of arthropods [19Osorio D. Bacon J.P. A good eye for arthropod evolution.Bioessays. 1994; 16: 419-424Crossref PubMed Scopus (50) Google Scholar, 20Strausfeld N.J. Nässel D.R. Neuroarchitecture of brain regions that subserve the compound eyes of Crustacea and Insects.in: Autrum H. Handbook of Sensory Physiology. Volume VII/6B. Springer-Verlag, New York1981Google Scholar, 21Berón de Astrada M. Tomsic D. Physiology and morphology of visual movement detector neurons in a crab (Decapoda: Brachyura).J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2002; 188: 539-551Crossref PubMed Scopus (41) Google Scholar] suggests that a deeper understanding of fly vision will produce widely generalizable conclusions. Beneath the fly retina, the visual system consists of four ganglia called the lamina, medulla, lobula, and lobula plate (Figure 1B). The lamina is the first layer of the visual system and contains the primary synaptic targets of the photoreceptors. Motion detection is presumed to occur within the medulla, because output neurons of the medulla show motion sensitivity [7Maisak M.S. Haag J. Ammer G. Serbe E. Meier M. Leonhardt A. Schilling T. Bahl A. Rubin G.M. Nern A. et al.A directional tuning map of Drosophila elementary motion detectors.Nature. 2013; 500: 212-216Crossref PubMed Scopus (221) Google Scholar]. We measured the calcium activity of the neurons that relay information from the lamina into the medulla, the lamina monopolar cells (LMCs; L1, L2, L3, and L4), and compared this to the cumulative activity of all neurons within each layer of the medulla neuropil. We made use of the GAL4/UAS system to express the genetically encoded calcium indicator GCaMP5G [22Akerboom J. Chen T.W. Wardill T.J. Tian L. Marvin J.S. Mutlu S. Calderón N.C. Esposti F. Borghuis B.G. Sun X.R. et al.Optimization of a GCaMP calcium indicator for neural activity imaging.J. Neurosci. 2012; 32: 13819-13840Crossref PubMed Scopus (860) Google Scholar] in either the LMCs L1–L4 or pan neuronally (details of the fly genotypes used are given in Table S1 available online, images of the driver lines are in Figure S1, and further details are in Supplemental Experimental Procedures). In vivo two-photon imaging of indicator fluorescence provided a relatively noninvasive measure of population-level neuronal activity in response to visual stimuli presented on a novel projector-based display (Figure 1A). The recorded calcium response to the appearance of a small black disc reveals three critical features of our results: (1) the responses are localized to a few medulla columns, which is consistent with the retinotopic organization of the medulla; (2) the layered structure of the medulla is readily discernible in these responses; and (3) light-on and light-off produce characteristic responses that vary between layers of the medulla (Figures 1C and 1D; Movie S1). To examine light-on and light-off responses within the medulla, we presented flies with a visual stimulus that consisted of a disc that alternated between bright and dark on an intermediate-intensity background (Figure 2A). A brief flickering protocol was first used to survey the medulla for a localized calcium response, which determined the imaging region used for subsequent experiments. In all layers of the medulla that contain LMC processes, the LMCs showed decreased activity in response to light increments and increased activity in response to light decrements (Figures 2B, 2C, and S2A). Although the calcium indicator was simultaneously expressed in LMCs L1–L4, the spatial separation of the LMC arborizations (Figure S1B) made it possible to assign the activity measured in each layer to specific cell types (Figure 2C; M1: L1; M2: L2+L4; M3: L3; M4: L4; and M5: L1). In all five layers, activity was dominated by a tonic decrease in response to light-on and a tonic increase in response to light-off. However, a phasic response to light decrements but not light increments was observed in layer M2 (likely from L2 given the absence of a similar response in M4), and modest but statistically significant differences in the magnitude of the response to light increments and decrements could be discerned in all layers, except in layer M5 (Figure S2A). These results are consistent with previous calcium imaging studies in which L1, L2, L3, and L4 were all found to show increased activity in response to light decrements and decreased activity in response to light increments, with slight-to-moderate selectivity depending on the specific stimulus conditions [5Freifeld L. Clark D.A. Schnitzer M.J. Horowitz M.A. Clandinin T.R. GABAergic lateral interactions tune the early stages of visual processing in Drosophila.Neuron. 2013; 78: 1075-1089Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar, 8Clark D.A. Bursztyn L. Horowitz M.A. Schnitzer M.J. Clandinin T.R. Defining the computational structure of the motion detector in Drosophila.Neuron. 2011; 70: 1165-1177Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar, 10Reiff D.F. Plett J. Mank M. Griesbeck O. Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila.Nat. Neurosci. 2010; 13: 973-978Crossref PubMed Scopus (80) Google Scholar, 12Silies M. Gohl D.M. Fisher Y.E. Freifeld L. Clark D.A. Clandinin T.R. Modular use of peripheral input channels tunes motion-detecting circuitry.Neuron. 2013; 79: 111-127Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar, 23Meier M. Serbe E. Maisak M.S. Haag J. Dickson B.J. Borst A. Neural Circuit Components of the Drosophila OFF Motion Vision Pathway.Curr. Biol. 2014; 24: 385-392Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar]. In a parallel set of experiments, we examined the summed response of all (or nearly all) medulla neurons to an identical stimulus using a pan-neuronal driver (R57C10) [24Jenett A. Rubin G.M. Ngo T.T. Shepherd D. Murphy C. Dionne H. Pfeiffer B.D. Cavallaro A. Hall D. Jeter J. et al.A GAL4-driver line resource for Drosophila neurobiology.Cell Rep. 2012; 2: 991-1001Abstract Full Text Full Text PDF PubMed Scopus (820) Google Scholar]. This driver was previously shown to drive expression in all known columnar medulla neuron types using stochastic single-cell labeling experiments [15Takemura S.Y. Bharioke A. Lu Z. Nern A. Vitaladevuni S. Rivlin P.K. Katz W.T. Olbris D.J. Plaza S.M. Winston P. et al.A visual motion detection circuit suggested by Drosophila connectomics.Nature. 2013; 500: 175-181Crossref PubMed Scopus (446) Google Scholar] (A.N., unpublished data), and double labeling with an antibody [25O’Neill E.M. Rebay I. Tjian R. Rubin G.M. The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway.Cell. 1994; 78: 137-147Abstract Full Text PDF PubMed Scopus (588) Google Scholar] for an established pan-neuronal marker [26Campos A.R. Rosen D.R. Robinow S.N. White K. Molecular analysis of the locus elav in Drosophila melanogaster: a gene whose embryonic expression is neural specific.EMBO J. 1987; 6: 425-431Crossref PubMed Scopus (92) Google Scholar] suggested that it is expressed in all columnar and tangential medulla neurons (Figure S1D). In contrast to the LMCs, the pan-neuronal activity displayed a complex spatiotemporal structure in response to the flickering disc stimulus (Figures 2B, 2C, and S2B). The pan-neuronal responses in most layers were strongly rectified, that is, the response to light-on did not resemble the inverse of the response to light-off. This rectification is indicative of nonlinear processing that would result in selectivity for either light-on or light-off signals. Increased activity in response to light increments was observed in layers M1, M6, M8/9, and M10. Increased activity in response to light decrements was observed in M1, M2, M3, and M8/9 (Figure S2B). For pan-neuronal images, layers M4/5 and M8/9 could not be readily distinguished based on either anatomy or activity and were treated as aggregates. In all layers, the magnitude of the response to light increments and decrements differed (Figure S2B). Finally, the LMC response was found to be significantly less rectified than the pan-neuronal response in each layer (Figure S2C). Although the pan-neuronal response represents the summed activity of many cell types, this alone cannot explain the rectification, because the linear sum of multiple unrectified responses remains unrectified. The activity of the LMCs is dominated by a tonic, unrectified response to light changes (Figures 2B and 2C, top), whereas the pan-neuronal activity shows substantial phasic, rectified responses to both light increments and decrements (Figures 2B and 2C, bottom). This difference, summarized in the statistical results of Figures S2A–S2C, strongly suggests that the rectification of medulla responses to light-on and light-off stimuli occurs downstream of the LMCs. The conclusion that the rectification occurs postsynaptic to the LMCs, and is not a difference between the intrinsic activity of L1 and L2, is supported by previous studies in which L1 and L2 were found to respond to both light increments and decrements [5Freifeld L. Clark D.A. Schnitzer M.J. Horowitz M.A. Clandinin T.R. GABAergic lateral interactions tune the early stages of visual processing in Drosophila.Neuron. 2013; 78: 1075-1089Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar, 8Clark D.A. Bursztyn L. Horowitz M.A. Schnitzer M.J. Clandinin T.R. Defining the computational structure of the motion detector in Drosophila.Neuron. 2011; 70: 1165-1177Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar] (but see [10Reiff D.F. Plett J. Mank M. Griesbeck O. Borst A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila.Nat. Neurosci. 2010; 13: 973-978Crossref PubMed Scopus (80) Google Scholar], which reaches a different conclusion). Can the complex spatiotemporal structure of the pan-neuronal response be decomposed into simpler, constituent responses, or is this complexity a necessary consequence of measuring the summed activity of a diverse neuronal population? To further explore this question, we performed a principal component analysis (PCA) of the responses to the flickering disc stimulus. The PCA was performed using individual pixels from both LMC and pan-neuronal data sets as variates and stimulus-synchronized time points as observations. Consequently, the obtained principal components utilized all available spatial (and temporal) information and simultaneously described both the LMC and pan-neuronal data sets. The first three principal components were found to capture a substantial fraction of the observed dynamics (Figure 2D; LMC, 60% and pan-neuronal, 61% of variance of each pixel at each time point across all animals). The first principal component captures a tonic, unrectified response to changes in light intensity; the second component describes a phasic, rectified response to light increments (an on response); and the third component corresponds to a phasic, rectified response to light decrements (an off response). Composing a prediction of the pan-neuronal response based on the extracted principal components produces a spatiotemporal pattern (Figure 2E) that qualitatively captures all of the features of the original averaged data set (Figure 2B). The spatial distribution of the signals in the second and third PCA components are strikingly similar to anatomical pathways that were suggested by a study of quantitative correlations in the neuronal arborization patterns of Golgi-impregnated medulla columnar neurons [14Bausenwein B. Dittrich A.P. Fischbach K.F. The optic lobe of Drosophila melanogaster. II. Sorting of retinotopic pathways in the medulla.Cell Tissue Res. 1992; 267: 17-28Crossref PubMed Scopus (107) Google Scholar]. We have reproduced the schematic view of these pathways from this classic study and compared them with our PCA results (Figures 2F and 2G). The signal energy in PC2 is very similar to the arborization density for members of the “L1 pathway,” whereas the signal energy in PC3 is well aligned with the arborization density for members of the “L2 pathway.” One confound to interpreting these responses as evidence of actual neuronal pathways is it assumes the stimulus we selected reflects generalizable phenomena. We have examined the response to moving edges of different polarities and have found that the temporal response is similar to the response observed for a flickering disc, suggesting that our primary stimulus is highly relevant for examining components of the motion detection circuitry (Figures S2D–S2I). The alignment of the spatial distribution of the observed responses with the classic neuroanatomical evidence suggests that the light-on response reflects activity in members of the “L1 pathway” and the light-off response reflects activity in members of the “L2 pathway.” This result agrees with previous studies that found that L1 and L2 blockade eliminates responses to light-on and light-off motion, respectively, in lobula plate tangential cells [4Joesch M. Schnell B. Raghu S.V. Reiff D.F. Borst A. ON and OFF pathways in Drosophila motion vision.Nature. 2010; 468: 300-304Crossref PubMed Scopus (228) Google Scholar, 6Joesch M. Weber F. Eichner H. Borst A. Functional specialization of parallel motion detection circuits in the fly.J. Neurosci. 2013; 33: 902-905Crossref PubMed Scopus (51) Google Scholar] and walking behavioral assays [8Clark D.A. Bursztyn L. Horowitz M.A. Schnitzer M.J. Clandinin T.R. Defining the computational structure of the motion detector in Drosophila.Neuron. 2011; 70: 1165-1177Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar, 12Silies M. Gohl D.M. Fisher Y.E. Freifeld L. Clark D.A. Clandinin T.R. Modular use of peripheral input channels tunes motion-detecting circuitry.Neuron. 2013; 79: 111-127Abstract Full Text Full Text PDF PubMed Scopus (89) Google Scholar]. This result is also in agreement with measurements of selectivity for light-on motion by T4 neurons and selectivity for light-off motion by T5 neurons [7Maisak M.S. Haag J. Ammer G. Serbe E. Meier M. Leonhardt A. Schilling T. Bahl A. Rubin G.M. Nern A. et al.A directional tuning map of Drosophila elementary motion detectors.Nature. 2013; 500: 212-216Crossref PubMed Scopus (221) Google Scholar], which have been implicated as the targets of the L1 and L2 pathways, respectively, based on connectivity [15Takemura S.Y. Bharioke A. Lu Z. Nern A. Vitaladevuni S. Rivlin P.K. Katz W.T. Olbris D.J. Plaza S.M. Winston P. et al.A visual motion detection circuit suggested by Drosophila connectomics.Nature. 2013; 500: 175-181Crossref PubMed Scopus (446) Google Scholar]. There is broad agreement that L1 and L2 are together required for motion detection [4Joesch M. Schnell B. Raghu S.V. Reiff D.F. Borst A. ON and OFF pathways in Drosophila motion vision.Nature. 2010; 468: 300-304Crossref PubMed Scopus (228) Google Scholar, 8Clark D.A. Bursztyn L. Horowitz M.A. Schnitzer M.J. Clandinin T.R. Defining the computational structure of the motion detector in Drosophila.Neuron. 2011; 70: 1165-1177Abstract Full Text Full Text PDF PubMed Scopus (184) Google Scholar, 11Rister J. Pauls D. Schnell B. Ting C.Y. Lee C.H. Sinakevitch I. Morante J. Strausfeld N.J. Ito K. Heisenberg M. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster.Neuron. 2007; 56: 155-170Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar, 13Tuthill J.C. Nern A. Holtz S.L. Rubin G.M. Reiser M.B. Contributions of the 12 neuron classes in the fly lamina to motion vision.Neuron. 2013; 79: 128-140Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar]; however, several behavioral studies identified other specific phenotypes upon inactivation. In one study, blocking L1 reduced the response to back-to-front motion, and blocking L2 reduced the response to front-to-back motion [11Rister J. Pauls D. Schnell B. Ting C.Y. Lee C.H. Sinakevitch I. Morante J. Strausfeld N.J. Ito K. Heisenberg M. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster.Neuron. 2007; 56: 155-170Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar]. In another study, separately blocking L1 or L2 had no effect on the response to either light-on or light-off moving edges [13Tuthill J.C. Nern A. Holtz S.L. Rubin G.M. Reiser M.B. Contributions of the 12 neuron classes in the fly lamina to motion vision.Neuron. 2013; 79: 128-140Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar]. Although anatomical evidence suggests that the L1 and L2 pathways are quite dissimilar, there are prominent interconnections between these pathways, notably through the feedforward neuron L5 and the feedback neurons C2 and C3 [15Takemura S.Y. Bharioke A. Lu Z. Nern A. Vitaladevuni S. Rivlin P.K. Katz W.T. Olbris D.J. Plaza S.M. Winston P. et al.A visual motion detection circuit suggested by Drosophila connectomics.Nature. 2013; 500: 175-181Crossref PubMed Scopus (446) Google Scholar]. Because of the presence of these interactions between the pathways, as well as clear evidence for at least one additional pathway (associated with the LMC L3 [15Takemura S.Y. Bharioke A. Lu Z. Nern A. Vitaladevuni S. Rivlin P.K. Katz W.T. Olbris D.J. Plaza S.M. Winston P. et al.A visual motion detection circuit suggested by Drosophila connectomics.Nature. 2013; 500: 175-181Crossref PubMed Scopus (446) Google Scholar]), there is no simple prediction for how complete L1 or L2 blockage would be expected to affect behavior. In contrast to these behavioral methods that can only provide an indirect measure of neuronal function, our imaging results directly c" @default.
• W2023874864 created "2016-06-24" @default.
• W2023874864 creator A5036110349 @default.
• W2023874864 creator A5046008896 @default.
• W2023874864 creator A5052264625 @default.
• W2023874864 date "2014-05-01" @default.
• W2023874864 modified "2023-10-12" @default.
• W2023874864 title "Direct Observation of ON and OFF Pathways in the Drosophila Visual System" @default.
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