Nonlinear Integration of Visual and Haltere Inputs in Fly Neck Motor Neurons

Abstract

Animals use information from multiple sensory organs to generate appropriate behavior. Exactly how these different sensory inputs are fused at the motor system is not well understood. Here we study how fly neck motor neurons integrate information from two well characterized sensory systems: visual information from the compound eye and gyroscopic information from the mechanosensory halteres. Extracellular recordings reveal that a subpopulation of neck motor neurons display "gating-like" behavior: they do not fire action potentials in response to visual stimuli alone but will do so if the halteres are coactivated. Intracellular recordings show that these motor neurons receive small, sustained subthreshold visual inputs in addition to larger inputs that are phase locked to haltere movements. Our results suggest that the nonlinear gating-like effect results from summation of these two inputs with the action potential threshold providing the nonlinearity. As a result of this summation, the sustained visual depolarization is transformed into a temporally structured train of action potentials synchronized to the haltere beating movements. This simple mechanism efficiently fuses two different sensory signals and may also explain the context-dependent effects of visual inputs on fly behavior.

Head roll stabilisation in the nocturnal bull ant Myrmecia pyriformis: Implications for visual navigation

“…One reason for the low gain may therefore be the state-and context-dependent processing of relevant information. For instance, in the blowfly C. vicina, a subpopulation of the neck motor neurons (NMN type II) integrates visual information from the compound eyes with mechanosensory information from the halteres (Huston and Krapp, 2009). Visual input only affects the activity of type II NMNs when a non-visual input from the halteres is present concurrently.…”

Behavioural evidence for a visual and proprioceptive control of head roll in hoverflies (Episyrphus balteatus, Dipteran)

“…The existence of multisensory contributions to gaze stabilization is not surprising in view of the many channels involved (Hengstenberg, 1993;Taylor and Krapp, 2007). In insects, multimodal sensory convergence was found by electrophysiological studies between the halteres and vision in flies (Huston and Krapp, 2009) or between proprioceptive and visual motion-sensitive neurons known as 'self-movement detectors', which are involved in the flight control feedback system in dragonflies (Olberg, 1981). Such an integration pattern is supported by neuro-anatomical convergence occurring around the neck motor neurons in flies (Strausfeld and Seyan, 1985;Milde et al, 1987).…”

“…The halteres form a mechanosensory gyroscopic system that is sensitive to Coriolis forces (Nalbach, 1993;Hengstenberg, 1993Hengstenberg, , 1998Huston and Krapp, 2009) and measure the rotational speed of the body during fast perturbations or manoeuvres and drive opposite head roll movements (Schwyn et al, 2011). An example of proprioceptive structure, the prosternal organs, consisting of a pair of mechanosensitive hair fields located symmetrically on the neck on the anterior part of the thorax of insects (Pringle, 1938;Preuss and Hengstenberg, 1992;Paulk and Gilbert, 2006), are stimulated by the head position through 'contact sclerites' (Peters, 1962).…”

An Olfactory Circuit Increases the Fidelity of Visual Behavior

“…In Drosophila, the timing of efferent motor output onto asynchronous steering muscles during flight is regulated by mechanosensory signals to coincide with the proper phase of the wingbeat cycle (Tu and Dickinson, 1996). Furthermore, fly neck motor neurons, which are active during gaze stabilization, require mechanosensory input as well as a central flight signal to produce suprathreshold responses to motion (Huston and Krapp, 2009;, Frye, 2010). Here we show that at least in Drosophila, an attractive food odorant also modifies visually mediated motor output.…”