A pair of motion-sensitive neurons in the locust encode approaches of a looming object

Abstract

Neurons in the locust visual system encode approaches of looming stimuli and are implicated in production of escape behaviours. The lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD) compute characteristics of expanding edges across the locust eye during a loom and DCMD synapses onto motor elements associated with behaviour. We identified another descending interneuron within the locust ventral nerve cord. We named this neuron the late DCMD (LDCMD) as it responds later during an approach, with the firing rate peaking at about the time of collision. LDCMD produced lower amplitude, broader action potentials that were associated with an afterhyperpolarization, whereas DCMD action potentials showed a brief afterhyperpolarization often followed by an afterdepolarization. Within the mesothoracic ganglion, the primary LDCMD axon located adjacent to the DCMD axon, was thinner and lacked collateral projections to the lateral region of the neuropil. When compared with DCMD, LDCMD fired with fewer spikes during a loom and showed weaker habituation to repeated approaches. Coincidence of LDCMD and DCMD firing increased during object approach. Our findings indicate the presence of an additional motion-sensitive descending neuron in the locust that encodes temporally distinct properties of an approaching object.

Bilateral flight muscle activity predicts wing kinematics and 3-dimensional body orientation of locusts responding to looming objects

“…Based on the equation of the linear regression line (Fig.10) we can predict changes in FWA and η angle using DA. This prediction will be used in computer-generated closed-loop experiments to provide appropriate visual feedback during flight steering while recording from suites of flight muscles and multiple motion-sensitive visual neurons (Gray et al, 2010), allowing for an unprecedented understanding of the neural mechanisms of adaptive behaviour in this model system. (r=0.42, y=0.97x-5.72), DA and η (r=0.46,y=0.73x+1.36),and FWA and η (r=0.55,).…”

Looming detection by identified visual interneurons during larval development of the locust,Locusta migratoria

“…It also plays a role in triggering jumps (Fotowat and Gabbiani, 2007;Santer et al, 2008), and recent evidence suggests that it plays distinct roles during different phases in preparing for and performing a jump (Fotowat et al, 2011). The DCMD acts in concert with other interneurons in the control of jumps, some of which respond to approaching stimuli (Gray et al, 2010;Simmons and Rind, 1997). The natural predators that chase locusts might differ according to the age and size of locusts, as has been shown for Nemobius crickets, in which early instars are particularly vulnerable to predation by wolf spiders (Dangles et al, 2007).…”

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

“…Investigations in the locust highlighted the role of the LGMD in the avoidance responses to looming stimuli, but also showed that other LSNs, such as the LGMD2 (Rind, 1996), are likely involved with the execution of those responses (see also Gray et al, 2010;Sztarker and Rind, 2014). While escaping from an approaching object, crabs continuously regulate their speed (Oliva and Tomsic, 2012) and direction of run (Medan et al, 2015).…”

“…Such neurons are commonly referred as looming sensitive neurons (LSNs). LSNs have been found in pigeons (Wang and Frost, 1992), fish (Preuss et al, 2006), monkeys (Maier et al, 2004) and different arthropod species such as locusts (Rind and Simmons, 1992;Gabbiani et al, 1999;Gray et al, 2010), flies (Borst, 1991;Fotowat et al, 2009), crayfish (Glantz, 1974) and crabs Oliva and Tomsic, 2014). But, how is the visual information of an approaching object actually processed, encoded and conveyed by LSNs to contribute to avoidance behaviors?…”

“…These mechanisms comprise feed-forward excitation and feed-forward inhibition, adaptation, lateral inhibition and synchronization (reviewed in Oliva, 2015). Another important conclusion from studies of the locust's response to looming stimuli is that the LGMD is important for the timely performance of the avoidance responses, but not entirely necessary for the behavioral execution of the escape (Santer et al, 2008;Simmons et al, 2010;, indicating that additional LSN elements work in parallel to achieve the task (Rind, 1996;Gray et al, 2010).…”