Tuneable reflexes control antennal positioning in flying hawkmoths

Abstract

Complex behaviours may be viewed as sequences of modular actions, each elicited by specific sensory cues in their characteristic timescales. From this perspective, we can construct models in which unitary behavioural modules are hierarchically placed in context of related actions. Here, we analyse antennal positioning reflex in hawkmoths as a tuneable behavioural unit. Mechanosensory feedback from two antennal structures, Böhm’s bristles (BB) and Johnston’s organs (JO), determines antennal position. At flight onset, antennae attain a specific position, which is maintained by feedback from BB. Simultaneously, JO senses deflections in flagellum-pedicel joint due to frontal airflow, to modulate its steady-state position. Restricting JO abolishes positional modulation but maintains stability against perturbations. Linear feedback models are sufficient to predict antennal dynamics at various set-points. We modelled antennal positioning as a hierarchical neural-circuit in which fast BB feedback maintains instantaneous set-point, but slow JO feedback modulates it, thereby elucidating mechanisms underlying its robustness and flexibility.

Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation

“…The motor organs/organelles, as the effectors of light responses, are muscle in most macroscopic animals and cilia in relatively small aquatic animals. Light-induced muscle activities, such as those involved in the pupillary light reflex of our eyes, the light avoidance behavior of earthworms, and the phototaxis of insects, have been well investigated [9][10][11]. Muscle-based light responses have been reported throughout the bilaterians [6,[9][10][11][12][13][14][15].…”

“…Light-induced muscle activities, such as those involved in the pupillary light reflex of our eyes, the light avoidance behavior of earthworms, and the phototaxis of insects, have been well investigated [9][10][11]. Muscle-based light responses have been reported throughout the bilaterians [6,[9][10][11][12][13][14][15]. On the other hand, in the planktonic larvae of flatworms, Annelida, and Mollusca, responses to light are supported mainly by changes in ciliary beating, with which the larvae show reflex behavior and/or phototaxis [16][17][18].…”

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

“…The Johnston's organ consists of hundreds of concentrically arranged scolopidial units that are range-fractionated 27 . Antennal mechanosensors contribute in sensing airflow [28][29][30] , and maintaining headwind orientation 31 .…”

Generating controlled gusts using vortex rings

“…For instance, ecologists are interested in understanding how locomotory ability sets the range over which they can disperse or migrate (Chapman et al 2011). Neurobiologists are interested in the mechanistic details of how animals sense, process and respond to perturbations to their trajectories (Dahake et al 2018; Natesan et al 2019). More recently, robotics engineers are interested in asking similar questions about the flight capability of their flappers and drones or swimming robots (Jafferis et al 2019; Breuer 2019).…”