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Feature detection and orientation tuning in the Drosophila central complex

Abstract

Many animals, including insects, are known to use visual landmarks to orient in their environment. In Drosophila melanogaster, behavioural genetics studies have identified a higher brain structure called the central complex as being required for the fly’s innate responses to vertical visual features1 and its short- and long-term memory for visual patterns2,3,4. But whether and how neurons of the fly central complex represent visual features are unknown. Here we use two-photon calcium imaging in head-fixed walking and flying flies to probe visuomotor responses of ring neurons—a class of central complex neurons that have been implicated in landmark-driven spatial memory in walking flies2,3 and memory for visual patterns in tethered flying flies5. We show that dendrites of ring neurons are visually responsive and arranged retinotopically. Ring neuron receptive fields comprise both excitatory and inhibitory subfields, resembling those of simple cells in the mammalian primary visual cortex. Ring neurons show strong and, in some cases, direction-selective orientation tuning, with a notable preference for vertically oriented features similar to those that evoke innate responses in flies1,2. Visual responses were diminished during flight, but, in contrast with the hypothesized role of the central complex in the control of locomotion6, not modulated during walking. Taken together, these results indicate that ring neurons represent behaviourally relevant visual features in the fly’s environment, enabling downstream central complex circuits to produce appropriate motor commands6. More broadly, this study opens the door to mechanistic investigations of circuit computations underlying visually guided action selection in the Drosophila central complex.

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Figure 1: Drosophila ellipsoid body ring neurons arborize in visually responsive LTR microglomeruli which show a retinotopic organization.
Figure 2: Ring neurons are tuned to specific visual features and orientations.
Figure 3: Ring neuron LTR microglomeruli show stereotyped receptive field properties across flies.
Figure 4: Ring neuron visual responses are not significantly modulated during walking but diminished during flight.

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Acknowledgements

We thank A. Nern for sharing flies and technical advice; B. Pfeiffer and G. Rubin for providing pJFRC64, pJFRC118, and pJFRC119 flies; and R. Harris for building fly lines, sharing preliminary results, and providing critical feedback on the use of fly reagents. We thank K. Hibbard, D. Hall, J. Kao and the Janelia Fly Core for fly crosses and support; E. Chiappe for initial anatomy experiments; M. Reiser and J. Truman for sharing equipment; J. Liu for technical support; V. Iyer for ScanImage support; T. Adelman for helpful suggestions; and L. Looger and the Janelia GENIE team for GCaMP5 and GCaMP6. We are grateful to A. Leonardo, M. Reiser, E. Chiappe, J. Freeman, A. Karpova, S. Huston and members of Vivek’s laboratory for useful discussions and comments on the manuscript. This work was supported by the Howard Hughes Medical Institute.

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Authors and Affiliations

Authors

Contributions

Both authors designed the study and wrote the manuscript. J.S. carried out the experiments and data analysis.

Corresponding author

Correspondence to Vivek Jayaraman.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Pan-neuronal receptive fields for LTR microglomeruli.

a, Selected two-photon imaging frames showing calcium response in the LTR with pan-neuronal expression of GCaMP5. Highlighted in red are the microglomeruli that were selected for receptive field reconstruction. Scale bar, 5 μm. b, Schematic of visual stimulation used, receptive fields (two-trial averages) measured with left-and right-moving visual stimuli and their intersection labelled at full width at half maximum (FWHM) intensity (white ellipse) with the weighted centroid (white asterisk) of the distribution. c, Centre of each receptive field plotted against the centre of its corresponding microglomerulus. d, Correlation coefficient of data in d (r = 0.39, P = 0) and correlation coefficient of same data after randomly permuting the microglomeruli (n = 3,000 permutations, mean = (4.6 ± 0.076)×10–4). e, Principal component axes of receptive field centres (see Methods).

Extended Data Figure 2 Ring neurons make dendritic projections to LTR microglomeruli and send axonal arbors to the rings of the ellipsoid body.

a, A frame of a confocal stack of the LTR labelled with antibody staining against GFP using a pan-neuronal driver line, R57C10-LexA and antibody staining against red fluorescent protein (RFP) of EB1-GAL4. d, dorsal; m, medial. b, A section of a confocal stack of the LTR labelled with GFP using a pan-neuronal driver line R57C10-LexA and RFP labelling of c232-GAL4. c, Multicolour FLP-out labelling of c232-GAL4 (see Methods). d, Antibody staining of c232-GAL4 expressing the dendritic marker, DenMark (red) and an axonal label, synaptotagmin-tagged GFP (green). Entire cell is outlined with membrane-tagged HA (blue) (see Methods). Top panel is merge of all colours. e, Same as d for EB1-GAL4.

Extended Data Figure 3 Ring neurons respond with strong calcium transients to single stationary bright dots; receptive fields of ring neuron populations are spread non-uniformly across the largely ipsilateral visual field.

a, Overlay of all regions of interest of R4d microglomeruli recorded in a fly during visual stimulation over an average of all frames in a calcium video (940 frames), and selected frames of the calcium video showing responses of individual microglomeruli. Scale bar, 5 μm. b, An example of the single dot stimulus appearing at the specified azimuth and elevation for 1 s followed by a dark period of 1 s (coloured dot indicates both the stimulus and the subsequent off period) (top). ΔF/F for microglomerulus 3 in a responding to the stimulus (bottom). c, Excitatory receptive fields for all microglomeruli shown in a. d, Overlay of all regions of interest selected among R2 microglomeruli recorded during visual stimulation over an average of all frames (n = 940) in a calcium video, and selected frames of the calcium video showing responses of individual microglomeruli. Scale bar, 5 μm. e, Azimuth and elevation of the single bright dot presented for 1 s followed by a 1 s interval without stimulus (top). ΔF/F for microglomerulus 1 in d responding to the visual stimulus (bottom). f, Excitatory receptive fields for all microglomeruli shown in d. g, Overlapping receptive fields of R4d neurons. Ellipses have the same normalized second central moments as the receptive fields shown in c thresholded at 30% ΔF/F. Intensity scale indicates how many receptive fields overlap in a given region. h, Same as g for R2 neurons shown in f. i–k, Average receptive fields measured across all flies with single dot stimulation for R4d neurons (green, n = 8 flies, 159 receptive fields) (i), for R2 neurons (purple, n = 12 flies, 219 RFs) (j) and for both (overlay) (k). Recordings from the right lateral triangle were flipped to the contralateral side for averaging. Although a large fraction of R2 and R4d ring neurons we imaged were visually responsive, there were ring neurons that did not respond in our experiments. Such neurons may have receptive fields in areas of the fly’s visual field that we did not sample (for example, very lateral areas), be tuned to visual dimensions that we did not explore (such as colour or polarization or complex shapes), or be selectively responsive to other sensory modalities (such as mechanosensation or thermosensation).

Extended Data Figure 4 Ring neuron orientation preference and selectivity, direction selectivity and receptive field centre positions.

a, Correlation coefficients between predicted and measured responses for R2 neurons (histogram over all trials and receptive fields) (n = 6 flies). b, Same as a, for R4d neurons (n = 6 flies). c, Microglomeruli of R4d neurons coloured according to orientation preference and orientation selectivity (six-trial averages). d, Azimuth and elevation of the centre of the excitatory receptive fields of the neurons shown in c (two-trial averages, measured using moving bars as described in Extended Data Fig. 1 and Methods). e, Direction selectivity for neurons in c (six-trial averages). f, g, Microglomeruli shown in Fig. 2k, l labelled according to the azimuth and elevation of their excitatory receptive field centre (measured using moving stimuli as in Extended Data Fig. 1) (f) and their orientation selectivity (four-trial averages) (g). h–p, Distributions of preferred orientation, orientation selectivity and direction index for R2 (n = 10 flies), R4d (n = 12) and pan-neuronal (n = 11 flies) microglomeruli.

Extended Data Figure 5 Comparison of orientation tuning curves measured using dark-on-bright and bright-on-dark bars.

a, Orientation tuning curves (GCaMP6s) of three R4d microglomeruli measured using (top row) bright bars on a dark background (as in Fig. 2f) and dark bars on a bright background (exact contrast inversion of bright-bar stimulus). As suggested by excitatory–inhibitory structure of receptive fields (Fig. 2c, Extended Data Fig. 8), tuning curves measured with the two stimuli are qualitatively similar, but bright bars produce stronger responses (with our low-contrast, filtered LED array display, see Methods). b, Fitted tuning curves measured using dark and bright bars are highly correlated (mean = 0.648 ± 0.26, n = 7 flies).

Extended Data Figure 6 Stereotypy of excitatory receptive fields across flies in R4d neurons.

a, Excitatory receptive fields measured using single dot stimulation in one fly (fly1), and receptive fields recorded in other flies (n = 12) aligned by similarity. b, Cross-correlation coefficient between fly 1 and all other receptive fields in each column (mean = 0.74 ± 0.2).

Extended Data Figure 7 Stereotypy of excitatory receptive fields across flies in R2 neurons; summary of receptive field properties.

a, Same as Extended Data Fig. 6a, measured in R2 neurons in 8 flies. b, Cross-correlation coefficient between fly 1 and all other receptive fields in each column for R2 neurons shown in a (mean = 0.75 ± 0.12). c, Table showing characteristics of excitatory receptive fields for R4d and R2 ring neurons measured with single dot stimulation calculated at half maximum ΔF/F. The retinotopic correlation coefficients are significantly different from the control distributions, with P = 0.0283 for R4d (n = 8 flies, 159 receptive fields) and P = 0.0069 for R2 (n = 12 flies, 219 receptive fields).

Extended Data Figure 8 Stereotypy of white-noise-based receptive fields across flies in R2 neurons.

a, Receptive fields measured using white-noise stimulation in 6 flies aligned according to similarity. We used an average of 41 ± 13 trials (6 flies, number of trials: 38, 25, 39, 63, 35 and 47). Each trial consisted of presentation of 60 stimulus frames (see Methods). b, Receptive fields measured using white-noise stimulation in 7 flies aligned by similarity (subset of this data are shown in Fig. 3). We used an average of 33 ± 20 trials (7 flies, number of trials: 59, 61, 29, 21, 21, 14 and 26).

Extended Data Figure 9 Ring neuron visual responses in the LTR are diminished during flight but not walking.

a, Microglomeruli selected by visually assisted k-means clustering in R2 neurons, a subset of which are shown in Fig. 4b. b, Average over n = 24 trials of responses of R2 microglomeruli to a bright bar (15° × 90°) moving at 30° s−1 shown during a period when the fly is walking more than 50% of the time (blue) and less than 50% of the time (red) during rightward moving stimulation (envelopes show s.d.). c, d, Correlation coefficient (mean = 0.72 ± 0.25) between model (see Methods) and data for R2 microglomeruli recorded in n = 8 flies (c), and for R4d microglomeruli (n = 14 flies, mean 0.7 ± 0.25) that have unilateral receptive fields (d). e, Concatenation of seven epochs during walking behaviour with EB1-GAL4, UAS-GCaMP3 flies during stimulation with a left and right moving bar: data (blue) and model (red) fit (see Methods). f, Microglomeruli in R4d selected using visually assisted k-means clustering. g, Visual responses during flying and non-flying behaviour during stimulation with a bar moving from left to right (averaged over n = 14 trials for flying, n = 14 trials for non-flying), and during stimulation with a bar moving from right to left (n = 17 for flying and n = 11 trials for non-flying) for the fly shown in Fig. 4e (envelopes show s.d.). h, Correlation coefficient between model (see Methods) and data for R4d neurons with a linear dependence of the visual response on both wing angles (mean = 0.65 ± 0.27) recorded in n = 14 flies.

Extended Data Figure 10 Selection of microglomeruli using visually guided k-means clustering; walking and flight activity during behaving fly experiments.

a, Cross-correlation matrix between all pixels above threshold (see Methods for details). b, Cross-correlation matrix sorted according to clusters found by k-means clustering. c, Resulting regions of interest. d, Overlay of resulting regions of interest and selected frames of calcium video. Regions of interest that do not correspond to microglomeruli (based on comparison with the calcium video) are removed. e–g, Velocities measured: forward (e), side (f) and rotational (h) for all c232-GAL4, UAS-GCaMP3 flies recorded during walking behaviour. h, Percentage of walking for all EB1-GAL4 UAS-GCaMP3 flies recorded. i–k, Velocities forward (i), sidewise (j) and rotational (k). l, Percentage of walking for all EB1-GAL4, UAS-GCaMP3 flies recorded during walking behaviour. m, Number of 130 s epochs recorded for each c232-GAL4, UAS-GCaMP3 walking fly. n, Number of 130 s epochs recorded for each EB1-GAL4, UAS-GCaMP3 walking fly. o, Percentage of time flying during recording for all c232-GAL4, UAS-GCaMP3 flies recorded during flight behaviour. p, Number of 130 s epochs recorded for each c232-GAL4, UAS-GCaMP3 flying fly.

Supplementary information

C232 arborization in the central brain

GFP co-expressed under a pan-neuronal driver line, R57C10-LexA, together with a red fluorescent protein, RFP, under the control of c232-GAL4 (MOV 1317 kb)

C232 arborization in the LTr

Same sample as shown in video 1 imaged with larger zoom in the lateral triangle. (MOV 568 kb)

EB1 arborization in the central brain

Confocal stack of antibody staining of R57C10-LexA expressing GFP and EB1-GAL4 expressing RFP in the central brain. (MOV 2384 kb)

EB1 arborization in the LTr

Same sample as shown in video 3 imaged with larger zoom in the lateral triangle. (MOV 1196 kb)

Microglomeruli in the LTr respond to visual stimuli d

LTr imaged with GCaMP3 during visual stimulation with a left and right moving bar. The visual stimulus is shown at the same time as the LTr expressing GCaMP3 pan-neuronally. The size of the calcium movie frames is width = 26 mm, height = 26 mm. (MOV 4211 kb)

Visual responses in microglomeruli during walking behavior

A fly expressing GCaMP3 under the driver c232-GAL4 walking on an air supported ball is presented with a left and right moving bright bar. The panels show top left the calcium response in the lateral triangle, top right the stimulus that is presented to the fly, bottom left, the calcium response of selected glomeruli and, bottom right, the fly walking on the ball. (The size of the calcium movie frames is width = 28 µm, height = 26 µm.) (MOV 5455 kb)

Visual responses during flight behavior in c232

A fly expressing GCaMP3 under the driver c232-GAL4 performing flight behavior during the presentation of a bright bar. Note the increase in ΔF/F as the fly stops flying. (The size of the calcium movie frames is width = 26 µm, height = 22 µm.) (MOV 2732 kb)

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Seelig, J., Jayaraman, V. Feature detection and orientation tuning in the Drosophila central complex. Nature 503, 262–266 (2013). https://doi.org/10.1038/nature12601

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