Integration of parallel pathways for flight control in a hawkmoth reflects prevalence and relevance of natural visual cues

An animal’s behaviour is rarely guided just by one neural pathway or sensory modality. More often, parallel input from multiple sensory modalities supports various control systems at any given time: an insect might be following an odour plume, for example, while guiding its flight safely using visual and mechanosensory cues (Duistermars and Frye, 2008; Vickers and Baker, 1994). Even within the same modality, multiple pathways might act in parallel to shape the same behavioural output (Fox and Frye, 2014; Frighetto and Frye, 2023; Nassi and Callaway, 2009). How these parallel pathways are integrated, particularly when their individual outputs are in conflict, is key to understanding the complex natural behaviour of animals (Doudlah et al., 2022). This question can be particularly well investigated in a context where the same visual stimuli evoke different responses in different parts of the visual field. Such visual field partitioning is widespread among animals and likely shaped by the frequency at which these stimuli occur in the natural habitats of the animals (Baden et al., 2013; Hornstein et al., 2000; Turner et al., 2019; Alexander et al., 2022).

Insect flight control is a behaviour that strongly depends on visual information sampled across a wide receptive field. It utilises translational optic flow, the perceived relative motion of the environment generated by the animals’ own motion (Koenderink, 1986), to regulate the distance to the surrounding environment, and the flight speed across a wide range of insects (Baird et al., 2005; Baird et al., 2010; David, 1982; Fry et al., 2009; Portelli et al., 2011; Willis and Card, 1990; Dyhr and Higgins, 2010; Kennedy and Marsh, 1974; Kern et al., 2012; Kirchner and Srinivasan, 1989; Kuenen and Baker, 1982; Portelli et al., 2010; Grittner et al., 2022; Stöckl et al., 2019). This regulation is thought to be achieved by keeping the perceived rate of translational optic flow at a constant level across both eyes and over time (Portelli et al., 2011; Franceschini et al., 2007). In consequence, when insects encounter features that change contrast in the direction of travel, and thus generate translational optic flow, such as an array of trees or a vertically patterned wall in a flight tunnel, they slow down and keep a greater distance. Thereby, they reduce the perceived magnitude of translational optic flow (Collett, 2002; Egelhaaf, 2023; Srinivasan et al., 1999). Optic flow cues are also used to guide flight straightness, particularly when presented in the ventral visual field (Bigge et al., 2021; Linander et al., 2017). It is thought that insects measure optic flow across their entire visual field and respond to the area with the highest magnitude of translational optic flow within (Portelli et al., 2011; Linander et al., 2015). While this assumption has rarely been tested with dorsal optic flow cues, in honeybees and fruit flies, dorsal optic flow responses similar to the ventrolateral ones have been described (Portelli et al., 2011; Mazo and Theobald, 2014). While fruit flies weigh ventral translational optic flow stronger than dorsal optic flow, the most extreme partitioning of the visual field in terms of optic flow-based flight control has been observed in hawkmoths (Bigge et al., 2021).

We recently described a unique example of functional visual field partitioning in the hummingbird hawkmoth Macroglossum stellatarum. This insect uses translational optic flow only in their ventral and lateral visual field for flight guidance, while the same stimuli in the dorsal visual field evoke a directional response (Bigge et al., 2021; Figure 1A). In this directional response, the hawkmoths orient their flight along the main axis of different types of patterns, which is reminiscent of the dorsal orientation responses of ants under tree canopies (Hölldobler, 1980). Yet, the nature of the dorsal response in hawkmoths remains largely elusive, lacking a comprehensive comparison of its features with the well-described translational optic flow response.

Figure 1

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The behavioural partitioning of the visual field matches the prevalence of translational optic flow and contrast cues across the different regions of the visual field (Bigge et al., 2021; Calow and Lappe, 2007; Zanker and Zeil, 2005; Figure 1B). Unlike other examples of visual field partitioning, such as landing and predator avoidance to looming stimuli in fruit flies (Tammero and Dickinson, 2002), the hawkmoth flight responses to dorsal and ventrolateral visual cues are not functionally exclusive, suggesting these processes might act in parallel. This poses the question whether the integration of the two systems also corresponds with the natural cue statistics when both systems are active at the same time.

To address these questions, we characterised the unique directional response of the hummingbird hawkmoth to compare it to translational optic flow-based flight responses using behavioural investigations in flight tunnels. To dissect the integration of the dorsal response and ventrolateral optic flow-based flight control, we applied cue conflict experiments, as are commonly used in multisensory integration studies (Dacke et al., 2019; Stöckl et al., 2016). We set these results into context with natural visual scene statistics to understand the ecological relevance of the integration hierarchies of the parallel pathways for flight guidance in the hummingbird hawkmoth.

We monitored the hawkmoths’ behaviour in flight tunnels, which they traversed on their way between two cages with hidden feeders (Figure 2A). To generate visual stimulation, we used semi-transparent red plastic sheets, through which the animals could be filmed and tracked (see ‘Materials and methods’, for an overview of all conditions and condition identifiers, Supplementary file 1). From the tracked and digitised flight paths (Figure 2B), we extracted features of their flight responses: the average frame-by-frame flight speed, the position relative to the midline, the relative proportion of movement along the long versus short axis of the tunnel, and the cross-index (difference in lateral position at the exit versus entrance, Figure 2C). We measured the magnitude of translational optic flow and contrast cues generated by the visual stimuli we used to evaluate the behavioural responses of the animals with respect to the external stimulus strength (Figure 2D–F). Due to the transparency of the tunnel floor and ceiling, and the lighting from above, the magnitude of translational optic flow (Figure 2E) and contrast cues (Figure 2F) was not exactly the same for the four sides of the tunnel, despite using the same set of stimuli.

Figure 2

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Response characteristics to dorsal versus ventrolateral stimuli in isolation

When gratings were presented on a lateral tunnel wall, oriented perpendicular to the tunnel’s major axis to generate translational optic flow (henceforth called optic flow) by the animals’ own movement through the tunnel, the hawkmoths kept a perpendicular distance to the respective walls, resulting in significant shifts in the median position relative to the midline when only one wall generated optic flow (Figure 3A, G1 and G2), or a centring of flight paths around the midline when both walls generated optic flow (Figure 3A, G3). We indirectly measured the relative vertical position of the hawkmoths in the tunnels, and thereby their distance to dorsal and ventral patterns, by the size of the moths’ image in the videos (see ‘Materials and methods’). While this indirect measure must be treated with caution, the general trends are indicative of optic flow responses: hawkmoths flew higher, and thus further away from ventral perpendicular gratings compared to flights without patterns (Figure 3—figure supplement 1D, G4 versus N). This was also the case when the perpendicular gratings only extended over one side of the ventral tunnel (Figure 3—figure supplement 1H, H1 and H2). Moreover, hawkmoths flew at a similar height with longitudinal ventral gratings (which generated little optic flow when the moths flew along the tunnel’s major axis, Figure 5—figure supplement 1C, L1) as without patterns (Figure 5—figure supplement 1C, N), and significantly lower than with perpendicular ventral gratings (Figure 5—figure supplement 1C, G10). Thus, both for lateral and ventral cues, hawkmoths kept a greater perpendicular distance from high compared to low optic flow patterns.

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Previous work has shown that the distance hawkmoths keep to lateral optic flow depends on its spatial frequency and contrast, and is the largest for the optimal frequency and highest contrast, while the effect of lateral optic flow on flight speed and flight straightness remained similar for all patterns that hawkmoths could perceive (Bigge et al., 2021; Stöckl et al., 2019). With the limited range of spatial frequencies tested for ventral patterns, we did not observe a significant difference in perpendicular distance for different spatial frequencies (Figure 3—figure supplement 1G). This might have been due to differences in the pattern structure (previous studies used sinewave and checkerboards rather than square-wave gratings), or the very coarse measure of distance applied here. Like lateral optic flow patterns (Figure 3B and C, G1–G3), ventral optic flow patterns induced a reduction in flight speed (Figure 3B, Figure 3—figure supplement 1F) and lateral movement (Figure 3C, Figure 3—figure supplement 1C). The magnitude of lateral movement varied significantly with the spatial frequency of the ventral patterns (Figure 3—figure supplement 1C, G4, G8–G9), and the speed with the finest spatial gratings was numerically larger, though not significantly different (Figure 3—figure supplement 1C, G8 versus G4, G9), suggesting that like for lateral patterns, the optic flow-based response to ventral stimuli could be spatial frequency dependent.

Directional responses were characterised by a much stronger reduction in flight speed than observed for lateral or ventral optic flow cues (Figure 3B, G5) and highly increased lateral movement (Figure 3C, G4). This increased lateral movement was caused by an alignment of the hawkmoths’ flight direction with the main axis of the dorsal cue. It was most clearly observable with a stimulus that crossed from one side of the tunnel to the other, which resulted in an according change in the hawkmoths’ lateral position across the tunnel (Figure 3D, S3 and S4). This directional flight behaviour was never observed with ventral switch stimuli (Figure 3D, Figure 3—figure supplement 1, Figure 4—figure supplement 1). To rule out that the dorsal directional behaviour was an avoidance response of the dorsal coverage generated by the stripe and was indeed a true alignment with the stripe’s direction, we presented a grating of switching lines, which uniformly covered the entire tunnel ceiling. It elicited qualitatively the same switching response as single stripes (Figure 3D, S5 and S6). Moreover, with dorsal gratings of different spatial frequencies, hawkmoths showed a proportional change in lateral movement, consistent with following the stripes’ directional information, more so for higher spatial frequencies (Figure 3E, G5–G7). For ventral gratings, the proportion of lateral movement and flight speed did not show a consistent variation with stripe frequency (Figure 3—figure supplement 1C, G4, G8–G9).

Together with increasing lateral movement, hawkmoths reduced their flight speed moderately even for a single dorsal line stimulus, which covered only a small portion of the dorsal visual field (Figure 3—figure supplement 1A, S1–S2) and drastically for all dorsal contrast patterns that covered at least half the tunnel ceiling, even if they did not generate strong optic flow cues (Figure 3—figure supplement 1A , B and I , S3–S6, H3–H8, G5–G7). If possible, hawkmoths strictly avoided flying under dorsal coverage of the tunnel (Figure 3F, H3–H8). They avoided cues that contrasted strongly against the flight direction more than those with little contrast changes (Figure 3F, H4 and H7 versus H3 and H6). This also became evident when directly comparing gratings aligned perpendicular and parallel to the flight direction as hawkmoths changed their median flight position in the tunnel to avoid the gratings perpendicular to the flight direction (Figure 3F, H5 and H8). On the other hand, hawkmoths did neither avoid nor seek out flying over contrasting structures in the ventral visual field (Figure 3F , H1–H2). Interestingly, unlike for lateral and ventral gratings, hawkmoths did not keep a greater perpendicular distance to dorsal gratings (Figure 3—figure supplement 1D and G , S3C, G5–G7, H3–H8). On the contrary, they flew closer to the tunnel ceiling in these conditions than in tunnels without patterns, and mostly at a similar height than with ventral patterns. In tunnels with dorsal gratings covering one side, in which the moths flew exclusively on the free side, they remained at a similar height than in tunnels without patterns (Figure 3—figure supplement 1I, , N versus H4 and H7).

Taken together, these observations suggest that the hummingbird hawkmoths’ directional responses to contrast patterns in the dorsal visual field did not bear hallmarks of optic flow-based flight response, as in the ventrolateral visual field. This strongly suggests that a different visuomotor pathway underlies this flight behaviour. We therefore asked next, whether the responses to dorsal versus ventrolateral stimuli resulted from independent control systems, which act in parallel.

Cue conflict: Lateral optic flow and dorsal directional cues

To test whether and how optic flow-based avoidance and dorsal direction-following combine to guide the flight position of hawkmoths, we generated a direct conflict by combining a dorsal directional and lateral optic flow cue, which both induce hawkmoths to fly to the same side of the tunnel (Figure 4A and B). For the optic flow cue, we presented vertical red stripes on one tunnel side, which the animals increased their distance to, when presented on their own (Figure 4C, G1 and G2). The dorsal directional cue was a red stripe, which switched tunnel sides towards the optic flow cue in the travel direction of the animals. On its own, this cue induced a cross-over in median tunnel position (Figures 4D,2, S1 and S2). When both cues were presented in combination, we observed mixed responses: the hawkmoths kept their distance to the optic-flow tunnel side with the same magnitude as before (Figure 4D, SG1 and SG2). Simultaneously, in the now more limited lateral space of half the tunnel width, they performed the switching behaviour, resulting in as high a cross-index as with only the dorsal directional cue alone (Figure 4E, SG1 and SG2). This is remarkable because it shows the animals were not simply following the red stripe as they were not flying under it after the switch to the other tunnel side occurred, but they followed the directional information of this stimulus. Thus, hawkmoths performed both optic flow-based distance regulation and dorsal directional manoeuvres at the same time, suggesting that these two control systems act in parallel, with similar weights on the final response. Moreover, these weights did not reflect the magnitude of translational optic flow or contrast edges generated by the two types of cues. The lateral grating presented a much higher amplitude of translational optic flow, as well as a higher magnitude of contrast averaged along the length of the tunnel (Figure 2E and F).

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To test whether the parallel action of the optic flow and dorsal directional control systems generalised across tasks and visual stimulation types, we tested hawkmoths with a variant of the optic flow-based lateral distance regulation, as well as a different contrast pattern: we used a centring task, as frequently used in other species (Collett, 2002; Egelhaaf, 2023; Srinivasan et al., 1999), by presenting black-and-white checkerboard patterns on both lateral tunnel walls. These were combined with the same dorsal red stripe that changed its lateral position between the first and last third of the tunnel (Figure 4—figure supplement 1). The checkerboard pattern on its own induced a centring response (Figure 4—figure supplement 1A, C1) and straight flights with a very low cross-index (Figure 4—figure supplement 1B, C1). The dorsal direction-switching red stripe presented on its own resulted in a significantly wider positional distribution across the tunnel width (Figure 4—figure supplement 1A, S3 and S4), as well as a high cross-index (Figure 4—figure supplement 1B, S3 and S4). Presenting both cues combined resulted in a response combination of both optic flow and directional control: the animals centred as strongly as in the optic flow-only condition (Figure 4—figure supplement 1A, SC1 and SC2), and their cross-index was similar in direction to the dorsal directional-only condition (Figure 4—figure supplement 1B, SC1 and SC2). The mixed response also manifested in flight speed, which was significantly lower for dorsal directional-only cues than optic flow-only cues and had an intermediate value for the mixed conditions (Figure 4—figure supplement 1C, SC1 and SC2).

Thus, hawkmoths performed optic flow-based flight control, including lateral distance regulation and speed control in parallel with dorsal directional manoeuvres across different visual stimuli.

Cue conflict: Lateral versus dorsal avoidance

In the previous set of conflict tests, both lateral optic flow-based distance regulation and dorsal directional responses could be enacted with the same strength as when presented individually. We next tested how the animals responded when dorsal and lateral responses were conflicted, so that it was not possible to enact both to their original magnitude simultaneously. To test this, we set the lateral distancing and dorsal avoidance responses in conflict by presenting a grating of vertical red stripes on one tunnel wall, which induced the animals to fly on the opposite side of the tunnel, coupled with a grating of the same type on one half of the tunnel’s ceiling (Figure 5A and B). On its own, the animals avoided the dorsal tunnel coverage by flying on the uncovered tunnel side (Figure 5C, H4 and H7). Similarly, animals avoided the lateral tunnel side that presented a grating in isolation (Figure 5C, G1 and G2). When combined, we observed a clear hierarchy in responses: the vast majority of animals flew on the side of the tunnel presenting lateral optic flow, thus avoiding the dorsally covered section (Figure 5C, GG1 and GG2). Yet, the animals’ median position was also significantly different from the dorsal-only condition and shifted closer towards the lateral-only condition (Figure 5C, GG1 and GG2). Moreover, not a single animal had their median flight position in the covered tunnel side in the dorsal-only condition, but a subset of animals did in the conflict situation (Figure 5C, GG1 and GG2). Thus, the animals responded to both cues, though with a higher weight for dorsal avoidance. This weighting of responses did not reflect a higher magnitude of translational optic flow or overall contrast in the dorsal versus the lateral visual field (Figure 2E and F).

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Noticeably, in these conflict experiments, the lateral movement of the animals (Figure 5D, GG1 and GG2), and their flight speed (Figure 5—figure supplement 1A, GG1 and GG2) was significantly different from the lateral optic flow only condition, but not from the dorsal-only condition. High lateral movement and very low speed were highly indicative of the dorsal directional responses and suggest that even in the presence of lateral optic flow in the conflict situation, which supports straight, moderately fast flight, the animals were strongly guided by dorsal cues. Since we previously found that the animals’ flight straightness and speed was guided stronger by ventral than lateral optic flow cues (Bigge et al., 2021), we simultaneously presented dorsal and ventral gratings to test whether dorsal cues would also take over flight guidance in combination with ventral cues. In the conflict situation, the lateral movement (Figure 5E, GG3) and flight speed (Figure 5F, GG3) were significantly different from the ventral-only condition (G10), but not significantly different from the dorsal-only one (G11). This demonstrates that in the presence of dorsal contrast cues, the optic flow-based control on flight straightness and speed was taken over by dorsal directional guidance, suggesting the latter has a greater weight in the control hierarchy. This was observed despite the fact that the ventral gratings generated about 50% stronger translational optic flow than dorsal ones, and a comparable magnitude of contrast cues (Figure 2E and F). Yet, when analysing the relative flight height (Figure 5—figure supplement 1C), we found that the hawkmoths kept a similar distance to ventral patterns in the conflict situation (GG3) than with ventral cues only (G10), and a significantly higher flight position than with dorsal-only cues (G11), suggesting that similar to lateral optic flow cues, the perpendicular distance regulation to ventral optic flow cues remained intact when dorsal cues were presented simultaneously.

In this study, we characterised the dorsal directional flight response of hummingbird hawkmoths and revealed that it is fundamentally different from the ‘canonical’ optic flow-based flight control (Srinivasan et al., 1999). Using conflict experiments, we demonstrated that optic flow-based and dorsal directional flight responses act in parallel, though with different relative weights.

The nature of the dorsal response

Our results demonstrate that the flight responses of hawkmoths to dorsal stimuli did not bear the typical hallmarks of translational optic flow-based flight control (Figure 6A) as it is known from bees (Baird et al., 2005; Baird et al., 2010; Dyhr and Higgins, 2010; Kirchner and Srinivasan, 1989), flies (David, 1982; Fry et al., 2009; Portelli et al., 2011; Srinivasan et al., 1999), or moths (Vickers and Baker, 1994; Willis and Card, 1990; Kennedy and Marsh, 1974; Kuenen and Baker, 1982; Stöckl et al., 2019) to ventrolateral stimuli, and for honeybees to dorsal ones as well (Portelli et al., 2011). In this paradigm, the magnitude of translational optic flow is thought to be kept constant by a reduction of speed and an increase in perpendicular distance to cues generating optic flow (Portelli et al., 2011; Franceschini et al., 2007). While the hawkmoths in our experiments slowed down upon perceiving translational optic flow dorsally, they did so much more than for the same stimuli ventrolaterally. Moreover, they aligned with the dominant contrast axis of the stimuli and thus generated a much higher proportion of lateral movement for gratings perpendicular to the tunnel axis. As previously shown in these hawkmoths, high degrees of lateral movement correlate with low flight speed (Stöckl et al., 2019), so that the low speed was likely a side effect of the lateral flight, not a response to the optic flow. This also fits the observation that the hawkmoths flew distinctly faster with longitudinal dorsal stripes (Figure 5—figure supplement 1B, L1).

Figure 6

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Given the hawkmoths’ flight responses, one might hypothesise that contrast in the dorsal visual field induced a behaviour aimed at minimising optic flow, rather than keeping it constant, as they would ventrolaterally. What fits the hypothesis is that animals avoided flying under any visual contrast when possible. If this was not possible, they flew under the less-optic flow-inducing portions of the tunnel (Figure 3F, H5 and H8). Aligning with the dominant contrast axis could be a strategy to minimise the perceived translational optic flow. However, hawkmoths did not show a perpendicular distance regulation in response to dorsal optic flow cues as they did for ventrolateral ones. If anything, they flew closer to dorsal stimuli than in a tunnel without patterns (Figure 3—figure supplement 1D, N versus G5). This suggests that the dorsal response is not an optic flow reduction response, but rather aims at minimising the perceived contrast (Figure 6A).

We therefore hypothesise that the dorsal response might be an adaptation to avoid flying under canopies: both the strong avoidance of any dorsal coverage, whether inducing translational optic flow or not, and the alignment with dominant contrast edges, which could be canopy borders, could help to remain flying in the open. The lack of a distance regulation to dorsal optic flow cues might also be explained by a canopy avoidance strategy: if hawkmoths avoided flying under canopies, they would rarely encounter any dorsal optic flow. All the more so, since the natural habitat of these hawkmoths is described as mostly open and semi-open (Pittaway, 1993). Moreover, even if a hawkmoth was trapped under dorsal coverage, their most common escape strategy is flying upwards towards a bright spot of sky, which would be impaired if the moths had a regulatory mechanism like for ventrolateral optic flow, which kept them at a safe distance from optic flow-inducing structures.

Source data for the behavioural experiments, as well as natural scenes and tunnel pattern imaging, and all statistical results files, are available from https://doi.org/10.6084/m9.figshare.26820091. Custom-written analysis code is available from (https://github.com/stoeckl-lab/Bigge_et_al_2025 copy archived at Stöckl, 2025).

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Author details

1. Ronja Bigge

   1. Behavioral Physiology and Sociobiology (Zoology II), University of Würzburg, Biozentrum am Hubland, Würzburg, Germany
   2. Department of Biology, University of Konstanz, Konstanz, Germany

   Contribution

   Data curation, Formal analysis, Validation, Investigation, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0005-0403-4800

2. Rebecca Grittner

   Behavioral Physiology and Sociobiology (Zoology II), University of Würzburg, Biozentrum am Hubland, Würzburg, Germany

   Contribution

   Formal analysis, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

3. Anna Lisa Stöckl

   1. Behavioral Physiology and Sociobiology (Zoology II), University of Würzburg, Biozentrum am Hubland, Würzburg, Germany
   2. Department of Biology, University of Konstanz, Konstanz, Germany

   Contribution

   Conceptualization, Resources, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Visualization, Methodology, Writing – original draft, Project administration, Writing – review and editing

   For correspondence

   Anna.Stoeckl@uni-konstanz.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-0833-9995

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