Visual feedback influences antennal positioning in flying hawk moths

Abstract

Insect antennae serve a variety of sensory functions including tactile sensing, olfaction and flight control. For all of these functions, the precise positioning of the antenna is essential to ensure the proper acquisition of sensory feedback. Although antennal movements in diverse insects may be elicited or influenced by multimodal sensory stimuli, the relative effects of these cues and their integration in the context of antennal positioning responses are not well understood. In previous studies, we have shown that fields of Böhm's bristles located at the base of the antennae provide crucial mechanosensory input for antennal positioning in flying hawk moths. Here, we present electrophysiological and behavioral evidence to show that, in addition to the Böhm's bristles, antennal muscles of hawk moths also respond to bilateral visual input. Moreover, in contrast to the mechanosensorymotor circuit, which is entirely contained within the ipsilateral side, visual feedback influences antennal positioning on both contralateral and ipsilateral sides. Electromyograms recorded from antennal muscles show that the latency of muscle responses to visual stimulation ranged from 35 to 60 ms, considerably slower than their responses to mechanosensory stimuli (<10 ms). Additionally, the visual inputs received by antennal muscles are both motion-sensitive and direction-selective. We characterized the influence of visual feedback on antennal positioning by presenting open-loop translational and rotational visual stimuli to tethered flying moths. During rotational stimuli, we observed that the antenna contralateral to the direction of the turn moved forward through larger angles than the ipsilateral antenna. These observations suggest that whereas input from the Böhm's bristles mediates rapid corrections of antennal position, visual feedback may be involved in slower, bilaterally coordinated movements of the antenna during visually guided flight maneuvers. Thus, visual feedback can modulate the set point at which the antenna is held during flight in hawk moths.

Airflow and optic flow mediate antennal positioning in flying honeybees

“…Although arrangement of the hair plates in different insects varies, the underlying neural circuitry and hair plate function is conserved in moths, bees, and most other insect orders ( Krishnan and Sane, 2015 ). Previous studies in hawk moths have described only how the antenna, once positioned, reflexively maintains this position ( Krishnan et al, 2012 ), and also their response to visual cues ( Krishnan and Sane, 2014 ). However, the combinatorial role of these cues in antennal positioning behaviour during flight remained unclear.…”

“…Although this hypothesis remains unaddressed and is beyond the scope of this paper, our data clearly show that inflight antennal movements are precisely modulated, and product of both visual (from compound eyes) and mechanosensory (from the hair plates and JO) input. Visual feedback also induces directionally-sensitive antennal movements in other insects such as hawk moths ( Krishnan and Sane, 2014 ), Drosophila ( Mamiya et al, 2011 ), and many orthopteran insects ( Honegger, 1981 ; Ye et al, 2003 ). Unlike the hair plate reflexes which are strictly unilateral ( Krishnan et al, 2012 ), visual feedback drives the activity of both ipsi- and contralateral antennal motor neurons in moths ( Krishnan and Sane, 2014 ) and may therefore serve to coordinate the movements of both antennae.…”

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

“…Inputs from diverse modalities, including vision and Böhm's bristles, also arborize in the AMMC (Krishnan et al, 2012;Krishnan and Sane, 2014).…”

Vision does not impact walking performance in Argentine ants

“…The ability for vision to inform locomotion planning requires both visual detection of 49 environmental features and rapid processing of this information. Transduction speeds for 50 photoreceptors range from 30-150 ms in cockroaches (Heimonen et al, 2012;Ignatova et al, 51 2020), 35-60 ms in hawkmoths (Krishnan and Sane, 2014) and 30-250 ms in blowflies (Land 52 and Collett, 1974;Warzecha and Egelhaaf, 2000). Comparatively, neural conduction speeds are 53 relatively fast at 0.5-3.7 m/s in cockroaches (Pearson et al, 1970).…”

“…As a consequence, ants are likely capable of decelerating from 245 their average speed (25.9 mm/s on flat ground) to rest within a single step. The latency between 246 an antennal contact and reactionary behavior has not been measured in ants, however reaction 247 times are ~40 ms in stick insects (Schütz and Dürr, 2011), 25 ms in cockroaches (Ye and 248 Comer, 1996;Ye et al, 2003), and <10 ms in hawk moths (Krishnan and Sane, 2014). 249…”