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

Abstract

Stimulus complexity affects the response of looming sensitive neurons in a variety of animal taxa. The Lobula Giant Movement Detector/Descending Contralateral Movement Detector (LGMD/DCMD) pathway is well‐characterized in the locust visual system. It responds to simple objects approaching on a direct collision course (i.e., looming) as well as complex motion defined by changes in stimulus velocity, trajectory, and transitions, all of which are affected by the presence or absence of background visual motion. In this study, we focused on DCMD responses to objects transitioning away from a collision course, which emulates a successful locust avoidance behavior. We presented each of 20 locusts with a sequence of complex three‐dimensional visual stimuli in simple, scattered, and progressive flow field backgrounds while simultaneously recording DCMD activity extracellularly. DCMD responses to looming stimuli were generally characteristic irrespective of stimulus background. However, changing background complexity affected, peak firing rates, peak time, and caused changes in peak rise and fall phases. The DCMD response to complex object motion also varied with the azimuthal approach angle and the dynamics of object edge expansion. These data fit with an existing correlational model that relates expansion properties to firing rate modulation during trajectory changes.

Towards Computational Models and Applications of Insect Visual Systems for Motion Perception: A Review

“…3b). It can be clearly seen from the in locusts against a visually cluttered or dynamic background and more abundant visual stimuli including objects deviate from a collision course [231]. It can be seen from the Fig.…”

Three-dimensional shape and velocity changes affect responses of a locust visual interneuron to approaching objects

“…DCMD responses to changes in object motion reported here add to our understanding of how this pathway is adapted to complex natural stimuli, including changes in object trajectory (Dick and Gray, 2014;McMillan and Gray, 2012;Yakubowski et al, 2016). Our findings also have implications for general mechanisms of motion detection because size threshold encoding strategies are similar across many systems, including visual projection neurons of flies (de Vries and Clandinin, 2012), crabs (Carbone et al, 2018;Oliva and Tomsic, 2014) and the praying mantis (Sato and Yamawaki, 2014), as well as in the optic tectum of zebrafish (Dunn et al, 2016) and pigeons (Wu et al, 2005), and there is a positive linear relationship between the time of peak neural firing and l/|v| (Sun and Frost, 1998).…”

“…We characterized DCMD firing properties in response to object motion ( Fig. 3) using parameters measured from the PSTH response profiles (Gabbiani et al, 2005;McMillan and Gray, 2012;Yakubowski et al, 2016). For approaches at constant (C 50 , C 300 , C 550 ; Fig.…”

Complex object motion represented by context-dependent correlated activity of visual interneurones

“…) and the ability of the LGMD/DCMD pathway to respond to complex object motion (Guest and Gray ; McMillan and Gray ; Dick and Gray ) against complex visual backgrounds (Yakubowski et al. ), it is likely that other motion‐sensitive descending interneurons (Griss and Rowell ; Rowell and Reichert ; Gray et al. ) play a role in initiating and coordinating this complex behavior.…”

“…While there is much information on putative biophysical mechanisms that underlie LGMD computation of a looming object's visual properties (Rind and Bramwell 1996;Gabbiani et al 2004;Jones and Gabbiani 2010;Fotowat et al 2011), relatively few studies have attempted to directly relate the activity of this pathway to flight steering (Santer et al 2006). Given the variability of flight steering behaviors in locusts able to maneuver within six degrees of freedom (Chan and Gabbiani 2013;McMillan et al 2013) and the ability of the LGMD/DCMD pathway to respond to complex object motion (Guest and Gray 2006;McMillan and Gray 2012;Dick and Gray 2014) against complex visual backgrounds (Yakubowski et al 2016), it is likely that other motion-sensitive descending interneurons (Griss and Rowell 1986;Rowell and Reichert 1986;Gray et al 2010) play a role in initiating and coordinating this The diagram of the locust shows the relative position of the central nervous system (CNS) in red. The expanded (ventral) view of the CNS below shows the relative positions of the brain and the prothoracic (Pro), mesothoracic (Meso), and metathoracic (Meta) ganglia in the thorax.…”