Encoding properties of the mechanosensory neurons in the Johnston's organ of the hawk moth, Manduca sexta

Abstract

Antennal mechanosensors play a key role in control and stability of insect flight. In addition to the well-established role of antennae as airflow detectors, recent studies have indicated that the sensing of antennal vibrations by Johnston's organs also provides a mechanosensory feedback relevant for flight stabilization. However, few studies have addressed how the individual units, or scolopidia, of the Johnston's organs encode these antennal vibrations and communicate it to the brain. Here, we characterize the encoding properties of individual scolopidia from the Johnston's organs in the hawk moth, Manduca sexta, through intracellular neurophysiological recordings from axons of the scolopidial neurons. We stimulated the flagellum-pedicel joint using a custom setup that delivered mechanical stimuli of various (step, sinusoidal, frequency and amplitude sweeps) waveforms. Single units of the Johnston's organs typically displayed phaso-tonic responses to step stimuli with short (3-5 ms) latencies. Their phase-locked response to sinusoidal stimuli in the 0.1-100 Hz frequency range showed high fidelity (vector strengths>0.9). The neurons were able to encode different phases of the stimulus motion and were also extremely sensitive to small amplitude (<0.05 deg) deflections with some indication of directional tuning. In many cases, the firing frequency of the neurons varied linearly as a function of the stimulus frequency at wingbeat and double wingbeat frequencies, which may be relevant to their role in flight stabilization. Iontophoretic fills of these neurons with fluorescent dyes showed that they all projected in the antennal mechanosensory and motor center (AMMC) area of the brain. Taken together, these results showcase the speed and high sensitivity of scolopidia of the Johnston's organs, and hence their ability to encode fine antennal vibrations.

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

“…Unlike the Böhm's bristles that detect large changes in antennal position, Johnston's organs, which span the pedicel–flagellar joint are extremely sensitive and detect subtle vibrations of the flagella relative to the pedicel (Gewecke, ; Gewecke & Schlegel, ; Göpfert, Briegel, & Robert, ; Sane et al, ; Dieudonné et al, ; Krishnan & Sane, ). In contrast to Böhm's bristles, the scolopidial neurons from various sub‐regions of the Johnston's organs are layered and segregated in the AMMC.…”

“…In addition to Böhm's bristles, antennae also house the Johnston's organs, which consists of circumferentially arranged mechanosensory units ( scolopidia ) that span the passive pedicel‐flagellar joint. The Johnston's organs sense motion of flagellum relative to the pedicel in a range‐fractionated manner; whereas each scolopidium is highly sensitive in a narrow range of flagellar frequencies, their peak sensitivity varies from one scolopidium to another (Kamikouchi et al, ; Sane et al, ; Ai et al, ; Yorozu et al, ; Dieudonné et al, ). This enables the Johnston's organs to encode diverse mechanosensory stimuli, from low‐frequency tactile or airflow cues to high‐frequency auditory or antennal vibration cues.…”

“…These include hair plates, or Böhm's bristles, organized as distinct fields at head-scape and scape-pedicel joints (Schneider, 1964). In addition, modified chordotonal organs called Johnston's organs are embedded in the pedicel-flagellar joint and are extremely sensitive to subtle flagellar vibrations (Dieudonné, Daniel, & Sane, 2014;Gewecke, 1970;Gewecke & Schlegel, 1970;Sane et al, 2007).…”

Orientation in high-flying migrant insects in relation to flows: mechanisms and strategies

“…Recent findings show that the Johnston's organs are range-fractionated, i.e. they are capable of encoding antennal vibrations of low to high frequencies with exquisite sensitivity [38,41]. Although such high-frequency sensors may serve as turbulence sensors, the ‘jerks’ mechanism proposed in the next section does not demand sensitive mechanoreceptors specialized for detecting the weak airflows.…”

Sensory basis of lepidopteran migration: focus on the monarch butterfly

“…In this case, Johnston's organ, a chordotonal organ found in the pedicel of the antenna (second antennal segment) of insects, is responsible for detecting mechanical stimuli [38–39]. …”