The mechanosensory‐motor apparatus of antennae in the Oleander hawk moth (Daphnis nerii, Lepidoptera)

Abstract

Insect antennae are sensory organs of great importance because they can sense diverse environmental stimuli. In addition to serving as primary olfactory organs of insects, antennae also sense a wide variety of mechanosensory stimuli, ranging from low-frequency airflow or gravity cues to high-frequency antennal vibrations due to sound, flight or touch. The basal segments of the antennae house multiple types of mechanosensory structures that prominently include the sensory hair plates, or Böhm's bristles, which measure the gross extent of antennal movement, and a ring of highly sensitive scolopidial neurons, collectively called the Johnston's organs, which record subtle flagellar vibrations. To fulfill their multifunctional mechanosensory role, the antennae of insects must actively move thereby enhancing their ability to sense various cues in the surrounding environment. This tight coupling between antennal mechanosensory function and antennal movements means that the underlying mechanosensory-motor apparatus constitutes a highly tuned feedback-controlled system. Our study aims to explore how the sensory and motor components of this system are configured to enable such functional versatility. We describe antennal mechanosensory neurons, their central projections in the brain relative to antennal motor neurons and the internal morphology of various antennal muscles that actuate the basal segments of the antenna. We studied these in the Oleander hawk moth (Daphnis nerii) using a combination of techniques such as neural dye fills, confocal microscopy, scanning electron microscopy and X-ray tomography. Our study thus provides a detailed anatomical picture of the antennal mechanosensory-motor apparatus, which in turn provides key insights into its multifunctional role.

Fuelling on the wing: sensory ecology of hawkmoth foraging

“…2a, d) consist of three main segments, the basal scapus and pedicellus as well as the long flagella with tens of annuli. The basal two segments carry important mechanosensory organs: Böhm’s bristles, a type of sensilla chaetica, are located in three distinct fields on the scapus (with ≈ 170 bristles each in the species Daphnis nerii ) and two fields with fewer bristles on the pedicellus (Sant and Sane 2018). Johnston’s organs are embedded within the cuticle, in the joint between scapus and pedicellus (Fig.…”

“…Johnston’s organs are embedded within the cuticle, in the joint between scapus and pedicellus (Fig. 2d), and are sensitive to fast passive antennal movements with low amplitudes (Sant and Sane 2018). Axons of sensory cells innervating these sensilla arborize in the antennal mechanosensory and motor centre in the deutocerebrum of the moths, close to the dendritic arborisations of antennal motor neurons (Kloppenburg et al 1997; Sant and Sane 2018).…”

Tuneable reflexes control antennal positioning in flying hawkmoths

“…JO is composed of ca. 140 scolopidial sensory neurons, and senses passive vibrations in pedicel–flagellum joint 15 . Previous studies have shown that JO sense flagellar vibrations ranging from low-frequency vibrations due to airflow and gravity 25–27 to high-frequency flight-related movements of the antennal base 2,27,28 .…”

“…Along with sensory inputs from the JO, the antennal motor system receives proprioceptive inputs from Böhm’s bristles 14,15 . Antennal movement stimulates neurons underlying these sensory hairs, in turn activating antennal motor neurons and associated muscles with latencies of ~10 ms 14 .…”

“…Ablating these bristles renders insects incapable of moving their antennae 12–14 , underscoring their importance in antennal positioning. In diverse insects, the axons of the Böhm’s bristles project into the antennal mechanosensory and motor centre (AMMC), where their arbours spatially overlap with dendritic arbours of antennal motor neurons 14,15 . This neural circuit allows swift antennal responses to perturbations while maintaining stable position.…”