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Model of feed-forward and visual feed-back control of head roll orientation in wasps (Polistes humilis, Vespidae, Hymenoptera).

Stéphane Viollet1* and Jochen Zeil2
  • 1 Aix-Marseille Université/CNRS, Biorobotics, France
  • 2 The Australian National University, ARC Centre of Excellence in Vision Science, Australia

Flying insects keep their visual system horizontally aligned suggesting that gaze stabilization is a crucial first step in flight control. Unlike flies, hymenopteran insects, such as bees and wasps do not have halteres that provide fast, feed-forward angular rate information to stabilize head orientation in the presence of body rotations (Hengstenberg, 1993; Nalbach, 1993, 1994, Nalbach and Hengstenberg, 1994, Dickinson, 1999; Sherman and Dickinson, 2003, Fox and Daniel, 2008; Huston and Krapp, 2009, Frye, 2009). We tested whether hymenopteran insects use inertial (mechano-sensory) information to control head orientation from other sources, such as the wings, by applying periodic roll perturbations to male Polistes humilis wasps flying in tether under different visual conditions indoors and in natural outdoor conditions (Viollet and Zeil 2013). We oscillated the insects’ thorax with frequency modulated sinusoids (chirps) with frequencies increasing from 0.2Hz to 2Hz at a maximal amplitude of 50° peak-to-peak and maximal angular velocity of ±245°/s. We found that head roll stabilization is best outdoors, but completely absent in uniform visual conditions and in darkness. Step responses confirm that compensatory head roll movements are purely visually driven. Modelling step responses indicates that head roll stabilization is achieved by merging information on head angular velocity presumably provided by motion-sensitive with information on head orientation, presumably provided by light level integration across the compound eyes and/or ocelli (dorsal light response). Body roll in free flight reaches amplitudes of ±40° and angular velocities greater than 1000°/s, while head orientation remains horizontal for most of the time to within ±10°. In free flight, we did not find a delay between spontaneous body roll and compensatory head movements and suggest that this is evidence for the contribution of a feed-forward control to head stabilization.
The feed-forward control proposed here relies only on an accurate internal model of the body’s dynamics . The control input signal Uroll is copied and sent to the feed-forward controller Cf(s). The latter improves dramatically the performance of the gaze stabilization system during spontaneous rotation of the body because it compensates for the negative phase shift inherent in the two visual feedback loops. Similar feed-forward control has been suggested to explain the high accuracy of vertebrate gaze stabilization during self-generated body movements (Combes et al., 2008) and has been successfully implemented in the gaze stabilization system of a sighted aerial robot (Kerhuel et al., 2010). We found no delay between head and thorax movements in freely flying Polistes wasps and take this as a strong indication that head roll stabilization does involve feed-forward control signals that are inherently difficult to detect and to study in tethered flight. One testable prediction would be that spontaneous changes in wing movements during tethered flight should trigger brief head movements in the opposite direction to the intended body roll rotation.

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References

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Viollet, S. and Zeil, J. (2013). Feed-forward and visual feed-back control of head roll orientation in wasps (Polistes humilis, Vespidae, Hymenoptera). .J Exp Biol. doi:10.1242/jeb.074773.

Keywords: Polistes wasps, Head roll control, Vision, efference copy, feed-forward control, modelling, Visuo-motor feedback loop, Gaze control.

Conference: International Conference on Invertebrate Vision, Fjälkinge, Sweden, 1 Aug - 8 Aug, 2013.

Presentation Type: Poster presentation preferred

Topic: The visual control of flight and locomotion

Citation: Viollet S and Zeil J (2019). Model of feed-forward and visual feed-back control of head roll orientation in wasps (Polistes humilis, Vespidae, Hymenoptera).. Front. Physiol. Conference Abstract: International Conference on Invertebrate Vision. doi: 10.3389/conf.fphys.2013.25.00117

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Received: 23 Feb 2013; Published Online: 09 Dec 2019.

* Correspondence: Dr. Stéphane Viollet, Aix-Marseille Université/CNRS, Biorobotics, Marseille, 13288, France, stephane.viollet@univ-amu.fr