Responses of Descending Visually-Sensitive Neurons in the Hawkmoth,Manduca sexta, to Three-Dimensional Flower-Like Stimuli.

Abstract

Hawkmoths rely on vision to track moving flowers during hovering-feeding bouts. Visually guided flight behaviors require a sensorimotor transformation, where motion information processed by the optic ganglia ultimately modifies motor axon activity. While a great deal is known about motion processing in the optic lobes of insects, there has been far less exploration into the visual information available to flight motor axons. Visual information recorded at this stage has likely arisen from multiple visual pathways, and has potentially been modified by outside sensory information. As a first step, understanding the sensorimotor transformation from transduction of moving flower signals to active flower tracking behavior requires that the visual information available to the thoracic flight control centers be assayed. This paper investigated the response of descending visually sensitive neurons in the cervical connectives of the hawkmoth, Manduca sexta L. (Lepidoptera: Sphingidae), to flower-like stimuli. Because flower structure lends itself to oscillatory (vibratory) motion, the stimuli used in these experiments were discs oscillating in each axis of motion (horizontal, vertical, and looming). Object-sensitive descending-neurons (OSDNs) respond to multiple directions of object motion and do not clearly sort into classes of directional tuning. The broad spatial distribution of directional sensitivities exhibited by OSDNs indicates that the direction of object motion may be encoded on a population scale. Although OSDNs exhibit broad frequency response curves, over the range of frequencies that M. sexta are able to track (0–2 Hz) OSDNs exhibit monotonically increasing response. Additionally, OSDNs respond to discs oscillating at frequencies as high at 6 Hz, indicating that the visual information being sent to thoracic motor control centers is not likely the limiting factor in flower tracking ability.

Flight mechanics and control of escape manoeuvres in hummingbirds I. Flight kinematics

“…Except for broadbilled hummingbirds, all the birds had reaction times much lower than those reported for the visual feedback of insects. For example, hawkmoths have >50 ms delays in responding to moving flowers (Sprayberry, 2009), and fruit flies have ∼100 ms and ∼61 ms delays in responding to gust perturbation and looming-startling stimuli, respectively (Fuller et al, 2014;Muijres et al, 2014). These data reveal that hummingbirds are capable of faster visual processing than insects.…”

The mechanics and control of pitching manoeuvres in a freely flying hawkmoth (Manduca sexta)

“…We used values of   ranging from 0 to 2 wingbeats and  ranging from 0 to 0.5 wingbeats, assuming low latencies in the mechanosensor-based angular velocity sensing (Sane et al, 2007) and the larger latencies of typical of visual sensing (Sprayberry, 2009) for pitch angle detection. Similar to the no-delay case, K x , K a and K  can be obtained from fits to measured x(t) and b (t) with  b and b offset by the specified delays.…”

“…Sun and Xiong, 2005) and that angular velocity sensors likely operate with lower latency than visual angular position sensing (e.g. Sane et al, 2007;Sprayberry, 2009). Our stability analysis also revealed that, given sufficient derivative feedback, the moth could stabilize its pitch without use of proportional feedback, but that incorporating both modes substantially increased stability.…”

“…Hawkmoths are known to use their antennae as mechanosensor-based biological gyroscopes, providing low latency sensing of angular velocity; moths without antennae are reported to fly poorly (Sane et al, 2007). Sensing of angular orientation is likely visual, and thus subject to latencies of one to three wingbeats (Sprayberry, 2009).…”

Polarization-Sensitive Descending Neurons in the Locust: Connecting the Brain to Thoracic Ganglia

“…They modify the activity of thoracic networks to adapt specific behaviors depending on current stimulus conditions. Previous studies on descending visual neurons have analyzed looming-sensitive neurons mediating escape (Rind et al, 2008;Fotowat et al, 2009;Yamawaki and Toh, 2009), deviation detector neurons controlling flight balance (Griss and Rowell, 1986;Rowell and Reichert, 1986;Hensler, 1988Hensler, , 1992Hensler and Rowell, 1990), neurons coding for self-motion (Wertz et al, 2008(Wertz et al, , 2009a, targetselective neurons mediating prey detection (Olberg, 1986;Frye and Olberg, 1995), and figure-detecting neurons involved in flower recognition (Sprayberry, 2009). Descending neurons mediating sky compass-related polarization information should encode two important factors: the position of the sun and the daytime.…”