Figures and data
Optic flow and directional responses partition the visual field for flight control in the hummingbird hawkmoth.
A Flight control in most insects is strongly based on optic flow, the apparent movement of the environment across the visual field, induced by the animals’ own movement. Ventrolateral translational optic flow supports straight flight, compared to featureless environments. Most insects keep the magnitude of translational optic flow constant across their eyes, by adjusting their speed and perpendicular distance to optic-flow inducing textures. In hawkmoths, optic-flow cues presented in the dorsal visual field induce directional responses, which align the hawkmoths’ flight with the main direction of the visual cue. Moreover, hawkmoths avoid any structures in the dorsal, but not the ventral, visual field, even if they generate only weak translational optic flow. B The distribution of optic flow and contrast cues was measured across different habitat types: open (no bushes or trees within 500m of the camera), semi-open (lateral vegetation but no closed canopy) and closed (entirely closed canopy). The left column shows an example image of each habitat type. Boxplots depict the mean magnitude of translational optic flow (left panel) and contrast edges (right panel) across habitat types, and for three different scenes within habitats in the dorsal, ventral and lateral segments of the visual field (see coloured inset). Statistical results from a linear mixed-effects model are abbreviated as * p < 0.05, ** p < 0.01, *** p < 0.001.
Optic-flow-based flight control and dorsal directional responses.
A Hawkmoth flight behaviour was tested in a 100 cm long, 30-by-30 cm diameter tunnel, which could present visual patterns on any face to generate translational optic flow and directional cues. B The hawkmoths’ flight paths (shown from the camera’s perspective) were digitized with a camera mounted below the tunnel. N gives the number of flights. The dark grey line highlights one representative path. C From the flight paths, we quantified the median position off the midline, the average frame-by-frame speed, the proportion of lateral movement (as the ratio of frame-by-frame movement perpendicular and parallel to the longitudinal axis of the tunnel), and the cross-index; the difference in lateral position in the first and last third of the tunnel. D-F Median position, average speed and proportion of lateral movement with grating patterns on either tunnel side. G Cross-index with a red stripe which changed its position in the central third of the tunnel, crossing from one tunnel side to the other. The last two conditions present a version of this stripe, which repeated at the same spatial frequency as the grating patterns. H Median position of flight tracks with gratings perpendicular (generating strong translational optic flow) and parallel (weak translational optic flow) to the tunnel’s longitudinal axis, covering one side of either the tunnel ceiling or floor. I Proportion of lateral movement with gratings of different spatial frequencies (repeating every 3 cm, 6 cm and 12 cm), mounted to the tunnel ceiling. Black letters in D-I show statistically significant differences in group medians (confidence level: 5%). The red letters in D represent statistically significant differences in group variance from pairwise Brown–Forsythe tests (significance level 5%). The white boxplots depict the median and 25% to 75% range, the whiskers represent the data exceeding the box by more than 1.5 interquartile ranges, and the violin plots indicate the distribution of the individual data points shown in black.
Cue conflict: lateral optic flow and dorsal directional cues.
A, B Flight tracks of hawkmoths presented with a lateral grating inducing translational optic flow, and a dorsal line which switched sides from the first to the last third of the tunnel (from the camera’s perspective below the tunnel). N represents the number of flights. The dark grey line highlights a single representative flight track. C-E Median position, cross-index and proportion of lateral movement with either grating patterns, the dorsal line stimulus, or a combination of both. Black letters in C-E show statistically significant differences in group medians (confidence level: 5%). The white boxplots depict the median and 25% to 75% range, the whiskers represent the data exceeding the box by more than 1.5 interquartile ranges and the violin plots indicate the distribution of the individual data points shown in black.
Cue conflict: lateral versus dorsal avoidance.
Flight tracks of hawkmoths presented with A a lateral and a dorsal grating pattern (the latter only spanning one half of the tunnel), and B a ventral and dorsal grating pattern, both shown from the camera’s perspective below the tunnel. N represents the number of flights. The dark grey line highlights a single representative flight track. C-F Median position, proportion of lateral movement and flight speed with either pattern in isolation and in combination. Black letters in C-E show statistically significant differences in group medians (confidence level: 5%). The white boxplots depict the median and 25% to 75% range, the whiskers represent the data exceeding the box by more than 1.5 interquartile ranges. The violin plots indicate the distribution of the individual data shown in black.
Magnitude of translational optic flow and contrast edges in the flight tunnel.
A Heatmaps of the magnitude of translational optic flow (middle row) and contrast edges (bottom row) in the different tunnel conditions (top row) used in conflict experiments. B Stacked bars present the average magnitude of translational optic flow (top panel) and contrast edges (bottom panel) in each of the four quadrants (ventral, left, right and dorsal) in the five tunnel conditions depicted in A. C The hierarchy of dorsal directional responses and translational optic flow-based control in the ventrolateral visual field resulting from the conflict experiments.
Optic flow based flight control and dorsal directional responses.
A Average speed of flight paths with a red stripe which changed its position in the central third of the tunnel, crossing from one tunnel side to the other. The last two conditions present a version of this stripe, which repeated at the same frequency as the grating patterns. B,E Average speed and proportion of lateral movement of flight paths with gratings perpendicular (generating strong translational optic flow) and parallel (weak translational optic flow) to the tunnel’s longitudinal axis, covering one side of either the tunnel ceiling or floor. C, F, I Proportion of lateral movement and average speed with gratings of different spatial frequencies (repeating every 3 cm, 6 cm and 12 cm), mounted on the tunnel floor or ceiling, respectively. D, G, H Area of hawkmoth silhouette in tunnel videos, as a measure of their flight height above the tunnel floor (the smaller the area, the higher the hawkmoths) with grating patterns on either tunnel side (D), gratings of various spatial frequencies mounted ventrally and dorsally (G) and gratings covering half the tunnel or the full tunnel ventrally and dorsally (H). Black letters show statistically significant differences in group medians (confidence level: 5%). The white boxplots depict the median and 25% to 75% range, the whiskers represent the data exceeding the box by more than 1.5 interquartile ranges and the violin plots indicate the distribution of the individual data points shown in black.
Cue conflict: lateral optic flow and dorsal directional cues.
A-C Median lateral position, cross-index and average speed of flight paths with a red stripe which changed its position in the central third of the tunnel, crossing from one tunnel side to the other, and a 50% contrast checkerboard pattern on both lateral tunnel sides, presented individually and in combination. Black letters show statistically significant differences in group medians (confidence level: 5%). The white boxplots depict the median and 25% to 75% range, the whiskers represent the data exceeding the box by more than 1.5 interquartile ranges and the violin plots indicate the distribution of the individual data points shown in black.
Cue conflict: lateral distance regulation versus dorsal avoidance.
A Average speed of flight paths with lateral gratings and dorsal gratings covering half the tunnel, presented individually and in combination. B Average area of hawkmoths as a readout for flight height (the smaller the area, the higher the hawkmoths in the tunnel) in videos with dorsal and ventral longitudinal and perpendicular gratings. Black letters show statistically significant differences in group medians (confidence level: 5%). The white boxplots depict the median and 25% to 75% range, the whiskers represent the data exceeding the box by more than 1.5 interquartile ranges and the violin plots indicate the distribution of the individual data points shown in black.
