Background complexity affects response of a looming-sensitive neuron to object motion

Abstract

An increasing number of studies show how stimulus complexity affects the responses of looming-sensitive neurons across multiple animal taxa. Locusts contain a well-described, descending motion-sensitive pathway that is preferentially looming sensitive. However, the lobula giant movement detector/descending contralateral movement detector (LGMD/DCMD) pathway responds to more than simple objects approaching at constant, predictable trajectories. In this study, we presented Locusta migratoria with a series of complex three-dimensional visual stimuli presented while simultaneously recording DCMD activity extracellularly. In addition to a frontal looming stimulus, we used a combination of compound trajectories (nonlooming transitioning to looming) presented at different velocities and onto a simple, scattered, or progressive flow field background. Regardless of stimulus background, DCMD responses to looming were characteristic and related to previously described effects of azimuthal approach angle and velocity of object expansion. However, increasing background complexity caused reduced firing rates, delayed peaks, shorter rise phases, and longer fall phases. DCMD responded to transitions to looming with a characteristic drop in a firing rate that was relatively invariant across most stimulus combinations and occurred regardless of stimulus background. Spike numbers were higher in the presence of the scattered background and reduced in the flow field background. We show that DCMD response time to a transition depends on unique expansion parameters of the moving stimulus irrespective of background complexity. Our results show how background complexity shapes DCMD responses to looming stimuli, which is explained within a behavioral context.

Background visual motion affects responses of an insect motion-sensitive neuron to objects deviating from a collision course

“…These data show that the modulation of the DCMD firing rate reflects aspects of this type of complex visual motion in addition to those previously studied (McMillan and Gray ; Dick and Gray ; Silva et al. ). Overall, responses varied depending on the type of trajectory and background.…”

“…These responses are further modulated by the object's velocity (Dick and Gray ) and changes in background visual flow (Silva et al. ). However, no studies have addressed how this visual pathway responds to compound trajectories that transition away from the animal in complex visual environments.…”

A sublethal dose of a neonicotinoid insecticide disrupts visual processing and collision avoidance behaviour in Locusta migratoria

“…S represents a disc projected against a white background and FF represents a disc against a flow field consisting of vertically oriented, 2 cm wide bars moving outward from the azimuthal plan from the dome apex at 0.138 m/s. The latter elicits DCMD responses with lower peak firing rates, later peak time, shorter rise phase and a longer decay phase 32 . Doses of 0.1 and 1.0 ng/g did not significantly affect DCMD firing, while doses of 10 and 100 ng/g resulted in significant alterations of several features of DCMD firing (Fig.…”

“…The LGMD/DCMD pathway responds robustly to objects approaching on a direct collision course (looming) 29 , with peak firing rates occurring when the object surpasses an angular threshold on the retina 30 . These neurons also encode trajectory changes 31 and maintain robust responses with the addition of complex backgrounds 32, 33 . The response profile of the LGMD/DCMD results from an interplay of excitatory and inhibitory inputs.…”

Object approach computation by a giant neuron and its relation with the speed of escape in the crab Neohelice

“…Relationship between MLG2 firing activity and speed of escape to looming stimuli Contrasting with the progress made in understanding the multistage avoidance response to looming stimuli in the locust, where distinct features of the increasing firing activity of the LGMD neuron could be related to different stages of the behavioral response (Santer et al, 2008;Fotowat and Gabbiani, 2007;Silva et al, 2015), almost no advances have been made in relation to a continuously regulated response to looming stimuli in any animal.…”