The neural mechanisms of antennal positioning in flying moths

Abstract

SUMMARYIn diverse insects, the forward positioning of the antenna is often among the first behavioral indicators of the onset of flight. This behavior may be important for the proper acquisition of the mechanosensory and olfactory inputs by the antennae during flight. Here, we describe the neural mechanisms of antennal positioning in hawk moths from behavioral, neuroanatomical and neurophysiological perspectives. The behavioral experiments indicated that a set of sensory bristles called Böhmʼs bristles (or hair plates) mediate antennal positioning during flight. When these sensory structures were ablated from the basal segments of their antennae, moths were unable to bring their antennae into flight position, causing frequent collisions with the flapping wing. Fluorescent dye-fills of the underlying sensory and motor neurons revealed that the axonal arbors of the mechanosensory bristle neurons spatially overlapped with the dendritic arbors of the antennal motor neurons. Moreover, the latency between the activation of antennal muscles following stimulation of sensory bristles was also very short (<10ms), indicating that the sensorimotor connections may be direct. Together, these data show that Böhmʼs bristles control antennal positioning in moths via a reflex mechanism. Because the sensory structures and motor organization are conserved across most Neoptera, the mechanisms underlying antennal positioning, as described here, are likely to be conserved in these diverse insects.Supplementary material available online at

Visual feedback influences antennal positioning in flying hawk moths

“…Latencies to firing shift were significantly higher (P<0.01; Fig. 2C) than those reported for intrinsic muscle responses to stimulation of the Böhm's bristles (Krishnan et al, 2012). Additionally, the response latencies to ipsilateral and contralateral visual stimulation were not significantly different from each other.…”

“…1). This also contrasts with the mechanosensory input to the same muscles, which is thought to be ipsilaterally confined (Krishnan et al, 2012). In addition, we also observed that the latencies of muscle responses to contralateral and ipsilateral visual stimulation were similar ( Fig.…”

“…1D) and contralateral ( Fig. 1E) visual stimulation, in contrast to the responses to stimulation of the Böhm's bristles, which were ipsilaterally confined (Krishnan et al, 2012). The excitatory response typically consisted of an initial burst of spikes following the stimulus, followed by return to the baseline levels ( Fig.…”

“…Latency of visual input to the antennal muscles is 35-60 ms (or 1-2 wing strokes; wing beat frequency of Daphnis nerii~33 Hz), considerably slower than mechanosensory input from the Böhm's bristles (Fig. 2C), which activate the antennal muscles in <10 ms (Krishnan et al, 2012). Together, these data suggest that the reflex mediated by the Böhm's bristles provides rapid corrective feedback to the antennal muscles, whereas visual input may modify antennal position over longer time scales.…”

“…In moths, this behavior involves moving the antennae forward from rest to a flight position and maintaining this position during flight bouts (Dorsett, 1962). Antennal positioning is primarily mediated by the Böhm's bristles at the base of the antenna, which provide mechanosensory feedback to the antennal muscles at time scales of less than half a wing stroke (Krishnan et al, 2012). A complementary set of antennal mechanosensors, the Johnston's organs, sense antennal vibrations and are involved in flight control (Sane et al, 2007).…”