Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths

Abstract

During flight maneuvers, insects exhibit compensatory head movements which are essential for stabilizing the visual field on their retina, reducing motion blur, and supporting visual self-motion estimation. In Diptera, such head movements are mediated via visual feedback from their compound eyes that detect retinal slip, as well as rapid mechanosensory feedback from their halteres - the modified hindwings that sense the angular rates of body rotations. Because non-Dipteran insects lack halteres, it is not known if mechanosensory feedback about body rotations plays any role in their head stabilization response. Diverse non-Dipteran insects are known to rely on visual and antennal mechanosensory feedback for flight control. In hawkmoths, for instance, reduction of antennal mechanosensory feedback severely compromises their ability to control flight. Similarly, when the head movements of freely-flying moths are restricted, their flight ability is also severely impaired. The role of compensatory head movements as well as multimodal feedback in insect flight raises an interesting question: in insects that lack halteres, what sensory cues are required for head stabilization? Here, we show that in the nocturnal hawkmoth Daphnis nerii, compensatory head movements are mediated by combined visual and antennal mechanosensory feedback. We subjected tethered moths to open-loop body roll rotations under different lighting conditions, and measured their ability to maintain head angle in the presence or absence of antennal mechanosensory feedback. Our study suggests that head stabilization in moths is mediated primarily by visual feedback during roll movements at lower frequencies, whereas antennal mechanosensory feedback is required when roll occurs at higher frequency. These findings are consistent with the hypothesis that control of head angle results from a multimodal feedback loop that integrates both visual and antennal mechanosensory feedback, albeit at different latencies. At adequate light levels, visual feedback is sufficient for head stabilization. However, under dark conditions, antennal mechanosensory feedback is essential for the control of head movements.

Small-amplitude head oscillations result from a multimodal head stabilization reflex in hawkmoths

“…The moths were dorsally tethered by attaching a 3mm neodymium magnet with cyanoacrylate glue on the back of their thorax, which was attached to a magnet of opposite polarity on the tether pole. The tether pole was oscillated using a stepper motor to which it was attached (further details in (9)).…”

“…Using custom C++ program in a OpenCV library, we digitized and computed the following angles in MATLAB (also see (9), Fig. 1B)…”

“…In this context, flight-related reflexes in insects are particularly interesting as they are very rapid, and hence push the limits of nervous control. In particular, the head stabilization reflex is crucial for flight due to its intimate association with vision (9). Because insects cannot move their eyes relative to their heads, gaze stabilization is mostly achieved through compensatory head movements which help reduce motion blur of wide-field images during fast aerial maneuvers (7,10).…”

“…In Diptera, it is mediated by visual feedback from eyes and mechanosensory feedback from halteres (modified hindwings in flies) (7,11) in addition to neck prosternal organs (12). In non-Dipteran insects such as hawkmoths which lack halteres, head stabilization is mediated by visual and antennal mechanosensory feedback (Fig 1A; (9)), and also involve input from prosternal organs although these have not yet been described in moths. The antennal mechanosensory feedback is derived from the Johnston’s organ (JO), which is highly sensitive and spans the pedicel-flagellar joint thus monitoring the relative movements in this joint.…”

“…(A) A qualitative model illustrating the feedback loops in head stabilization (9) (B) A schematic illustrating the experimental set-up, head wobble and the angle used for analysis. (C, D) Representative raw plots showing time series of θ thorax (black line) and θ head-thorax (purple line) in presence of imposed roll in the control (C) and flagella-clipped (D) moths.…”